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Regarding the kingdom Animalia, which phylogenic tree is more common: Molecular Comparisons or Body-Plan Grades

Regarding the kingdom Animalia, which phylogenic tree is more common: Molecular Comparisons or Body-Plan Grades



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In the picture below, which I obviously do not own:

it depicts two different phylogenic trees, one which is based on molecular comparisons and another one which is based on body-plan grades. My question is which is more common or accepted in the current Biology world?

Image reference: http://www.zo.utexas.edu/faculty/sjasper/images/32.12.gif">


Long story short, use sequence information if you can.

The long story long: Sequence information and the trees generated from them are strictly more reliable than morphological characters. For instance: sharks are pretty much the same shape they were millions of years ago, but they've been accumulating genetic differences 'invisibly' that allows us to group the different kinds of shark accurately. Where genetic data is unavailable (paleontology as a rule, certain kinds of field taxonomy where it's cheaper to code the morphological features of each new beetle than sequence them all) morphological trees are still used. So in terms of which tree type is more common: It depends.

In terms of which tree type is more accepted, it's genetic data by a landslide. Genetic data by and large is much less affected by homologous structures and convergent evolution. In addition, it works on species that all look pretty much identical (imagine trying to code hundreds of bacterial species that are all closely related). Using highly conserved cellular machinery, trees for very distant species can be constructed. Using unconserved noncoding sequences trees for very closely related individuals trees can be constructed with a reasonable degree of accuracy.

Some examples: Mitochondrial Eve would be impossible to date with morphological characters. There's just not enough morphological variation between humans. Opabinia is a really good example of how hard it is to classify things based on shape, especially when they're a weird shape. Something you can do yourself: Human and Thermodesulfator(seq) are about as morphologically distinct as two living things can be. One is you, and one eats carbon dioxide and breathes sulfate and hydrogen. It lives at the bottom of the sea and would be more at home in a cup of hot coffee than outside it. Nevertheless, the two species show ~50% sequence similarity using 16S, twice as much as would be expected by chance and easily enough to classify a third thing as more closely related to one or the other. Try it yourself if you like.


A multi-locus analysis of phylogenetic relationships within cheilostome bryozoans supports multiple origins of ascophoran frontal shields

Phylogenetic relationships within the bryozoan order Cheilostomata are currently uncertain, with many morphological hypotheses proposed but scarcely tested by independent means of molecular analysis. This research uses DNA sequence data across five loci of both mitochondrial and nuclear origin from 91 species of cheilostome Bryozoa (34 species newly sequenced). This vastly improved the taxonomic coverage and number of loci used in a molecular analysis of this order and allowed a more in-depth look into the evolutionary history of Cheilostomata. Maximum likelihood and Bayesian analyses of individual loci were carried out along with a partitioned multi-locus approach, plus a range of topology tests based on morphological hypotheses. Together, these provide a comprehensive set of phylogenetic analyses of the order Cheilostomata. From these results inferences are made about the evolutionary history of this order and proposed morphological hypotheses are discussed in light of the independent evidence gained from the molecular data.

Infraorder Ascophorina was demonstrated to be non-monophyletic, and there appears to be multiple origins of the ascus and associated structures involved in lophophore extension. This was further supported by the lack of monophyly within each of the four ascophoran grades (acanthostegomorph/spinocystal, hippothoomorph/gymnocystal, umbonulomorph/umbonuloid, lepraliomorph/lepralioid) defined by frontal-shield morphology. Chorizopora, currently classified in the ascophoran grade Hippothoomorpha, is phylogenetically distinct from Hippothoidae, providing strong evidence for multiple origins of the gymnocystal frontal shield type. Further evidence is produced to support the morphological hypothesis of multiple umbonuloid origins of lepralioid frontal shields, using a step-wise set of topological hypothesis tests combined with examination of multi-locus phylogenies.

Graphical abstract

Highlights

► We use multi-locus molecular analyses supported by topological hypothesis tests. ► Evidence that Ascophorina is polyphyletic. ► Data suggests more than one origination of the ascus and associated structures. ► Evidence for multiple origins of the gymnocystal frontal shield type. ► Evidence for multiple umbonuloid origins of lepralioid frontal shields.


Regarding the kingdom Animalia, which phylogenic tree is more common: Molecular Comparisons or Body-Plan Grades - Biology

43 notecards = 11 pages ( 4 cards per page)

Campbell Biology Chapter 32

1) Both animals and fungi are heterotrophic. What distinguishes animal heterotrophy from fungal heterotrophy is that only animals derive their nutrition by

C) consuming living, rather than dead, prey.

D) using enzymes to digest their food.

2) The larvae of some insects are merely small versions of the adult, whereas the larvae of other insects look completely different from adults, eat different foods, and may live in different habitats. Which of the following most directly favors the evolution of the latter, more radical, kind of metamorphosis?

A) natural selection of sexually immature forms of insects

B) changes in the homeobox genes governing early development

C) the evolution of meiosis

D) the development of an oxidizing atmosphere on Earth

3) Which of the following is (are) unique to animals?

A) cells that have mitochondria

B) the structural carbohydrate, chitin

C) nervous conduction and muscular movement

E) Two of these responses are correct.

4) What do animals as diverse as corals and monkeys have in common?

A) body cavity between body wall and digestive system

B) number of embryonic tissue layers

E) degree of cephalization

5) The Hox genes came to regulate each of the following in what sequence, from earliest to most recent?

  1. identity and position of paired appendages in protostome embryos
  2. anterior-posterior orientation of segments in protostome embryos
  3. positioning of tentacles in cnidarians
  4. anterior-posterior orientation in vertebrate embryos
  5. A) 4 → 1 → 3 → 2
  6. B) 4 → 2 → 3 → 1
  7. C) 4 → 2 → 1 → 3
  8. D) 3 → 2 → 1 → 4
  9. E) 3 → 4 → 1 → 2

6) In individual insects of some species, whole chromosomes that carry larval genes are eliminated from the genomes of somatic cells at the time of metamorphosis. A consequence of this occurrence is that

A) we could not clone a larva from the somatic cells of such an adult insect.

B) such species must reproduce only asexually.

C) the descendents of these adults do not include a larval stage.

D) metamorphosis can no longer occur among the descendents of such adults.

E) Two of these responses are correct.

7) The last common ancestor of all animals was probably a

8) Evidence of which structure or characteristic would be most surprising to find among fossils of the Ediacaran fauna?

9) Which statement is most consistent with the hypothesis that the Cambrian explosion was caused by the rise of predator-prey relationships?

A) increased incidence of worm burrows in the fossil record

B) increased incidence of larger animals in the fossil record

C) increased incidence of organic material in the fossil record

D) increased incidence of fern galls in the fossil record

E) increased incidence of hard parts in the fossil record

10) Which of the following genetic processes may be most helpful in accounting for the Cambrian explosion?

E) chromosomal condensation

11) Whatever its ultimate cause(s), the Cambrian explosion is a prime example of

D) All three of the responses are correct.

E) Only two of the responses are correct.

12) Fossil evidence indicates that the following events occurred in what sequence, from earliest to most recent?

  1. Protostomes invade terrestrial environments.
  2. Cambrian explosion occurs.
  3. Deuterostomes invade terrestrial environments.
  4. Vertebrates become top predators in the seas.
  5. A) 2 → 4 → 3 → 1
  6. B) 2 → 1 → 4 → 3
  7. C) 2 → 4 → 1 → 3
  8. D) 2 → 3 → 1 → 4
  9. E) 2 → 1 → 3 → 4

13) What is the probable sequence in which the following clades of animals originated, from earliest to most recent?

  1. tetrapods
  2. vertebrates
  3. deuterostomes
  4. amniotes
  5. bilaterians
  6. A) 5 → 3 → 2 → 4 → 1
  7. B) 5 → 3 → 2 → 1 → 4
  8. C) 5 → 3 → 4 → 2 → 1
  9. D) 3 → 5 → 4 → 2 → 1
  10. E) 3 → 5 → 2 → 1 → 4

14) Arthropods invaded land about 100 million years before vertebrates did so. This most clearly implies that

A) arthropods evolved before vertebrates did.

B) extant terrestrial arthropods are better adapted to terrestrial life than are extant terrestrial vertebrates.

C) ancestral arthropods must have been poorly adapted to aquatic life, and thus experienced a selective pressure to invade land.

D) vertebrates evolved from arthropods.

E) arthropods have had more time to coevolve with land plants than have vertebrates.

15) An adult animal that possesses bilateral symmetry is most certainly also

16) Soon after the coelom begins to form, a researcher injects a dye into the coelom of a deuterostome embryo. Initially, the dye should be able to flow directly into the

17) A researcher is trying to construct a molecular-based phylogeny of the entire animal kingdom. Assuming that none of the following genes is absolutely conserved, which of the following would be the best choice on which to base the phylogeny?

A) genes involved in chitin synthesis

D) genes involved in eye-lens synthesis

E) genes that cause radial body symmetry

18) At which developmental stage should one be able to first distinguish a diploblastic embryo from a triploblastic embryo?

19) At which developmental stage should one be able to first distinguish a protostome embryo from a deuterostome embryo?

20) What distinguishes a coelomate animal from a pseudocoelomate animal is that coelomates

A) have a body cavity, whereas pseudocoelomates have a solid body.

B) contain tissues derived from mesoderm, whereas pseudocoelomates have no such tissue.

C) have a body cavity completely lined by mesodermal tissue, whereas pseudocoelomates do not.

D) have a complete digestive system with mouth and anus, whereas pseudocoelomates have a digestive tract with only one opening.

E) have a gut that lacks suspension within the body cavity, whereas pseudocoelomates have mesenteries that hold the digestive system in place.

21) You have before you a living organism, which you examine carefully. Which of the following should convince you that the organism is acoelomate?

B) It has bilateral symmetry.

C) It possesses sensory structures at its anterior end.

D) Muscular activity of its digestive system distorts the body wall.

22) The blastopore is a structure that first becomes evident during

C) the eight-cell stage of the embryo.

23) The blastopore denotes the presence of an endoderm-lined cavity in the developing embryo, a cavity that is known as the

24) Which of the following is descriptive of protostomes?

A) spiral and indeterminate cleavage, blastopore becomes mouth

B) spiral and determinate cleavage, blastopore becomes mouth

C) spiral and determinate cleavage, blastopore becomes anus

D) radial and determinate cleavage, blastopore becomes anus

E) radial and determinate cleavage, blastopore becomes mouth

25) Which of the following characteristics generally applies to protostome development?

D) blastopore becomes the anus

26) Protostome characteristics generally include which of the following?

A) a mouth that develops secondarily, and far away from the blastopore

E) absence of a body cavity

27) The most ancient branch point in animal phylogeny is that between having

A) radial or bilateral symmetry.

B) a well-defined head or no head.

C) diploblastic or triploblastic embryos.

D) true tissues or no tissues.

E) a body cavity or no body cavity.

28) With the current molecular-based phylogeny in mind, rank the following from most inclusive to least inclusive.

  1. ecdysozoan
  2. protostome
  3. eumetazoan
  4. triploblastic
  5. A) 4, 2, 3, 1
  6. B) 4, 3, 1, 2
  7. C) 3, 4, 1, 2
  8. D) 3, 4, 2, 1
  9. E) 4, 3, 2, 1

29) What does recent evidence from molecular systematics reveal about the relationship between grades and clades?

A) There is no relationship.

B) Some, but not all, grades reflect evolutionary relatedness.

C) Grades have their basis in, and flow from, clades.

D) Each branch point on a phylogenetic tree is associated with the evolution of a new grade.

30) Phylogenetic trees are best described as

A) true and inerrant statements about evolutionary relationships.

B) hypothetical portrayals of evolutionary relationships.

C) the most accurate representations possible of genetic relationships among taxa.

E) the closest things to absolute certainty that modern systematics can produce.

31) According to the evidence collected so far, the animal kingdom is

32) If a multicellular animal lacks true tissues, then it can properly be included among the

33) Which of the following statements concerning animal taxonomy is (are) true?

  1. Animals are more closely related to plants than to fungi.
  2. All animal clades based on body plan have been found to be incorrect.
  3. Kingdom Animalia is monophyletic.
  4. Only animals reproduce by sexual means.
  5. Animals are thought to have evolved from flagellated protists similar to modern choanoflagellates.
  6. A) 5 only
  7. B) 1 and 3
  8. C) 3 and 5
  9. D) 3, 4, and 5

34) If the current molecular evidence regarding animal origins is well-substantiated in the future, then what will be true of any contrary evidence regarding the origin of animals derived from the fossil record?

A) The contrary fossil evidence will be seen as a hoax.

B) The fossil evidence will be understood to have been incorrect because it is incomplete.

C) The fossil record will henceforth be ignored.

D) Phylogenies involving even the smallest bit of fossil evidence will need to be discarded.

E) Only phylogenies based solely on fossil evidence will need to be discarded.

35) What is true of the clade Ecdysozoa?

  1. A) It includes all animals that molt at some time during their lives.
  2. B) It includes all animals that undergo metamorphosis at some time during their lives.
  3. C) It includes all animals that have body cavities known as pseudocoeloms.
  4. D) It includes all animals with genetic similarities that are shared with no other animals.
  5. E) It includes all animals in the former clade Protostomia that truly do have protostome development.

36) Which distinction is given more emphasis by the morphological phylogeny than by the molecular phylogeny?

A) metazoan and eumetazoan

C) true coelom and pseudocoelom

D) protostome and deuterostome

E) molting and lack of molting

37) The last common ancestor of all bilaterians is thought to have had four Hox genes. Most extant cnidarians have two Hox genes, except Nematostella (of β-catenin fame), which has three Hox genes. On the basis of these observations, some have proposed that the ancestral cnidarians were originally bilateral and, in stages, lost Hox genes from their genomes. If true, this would mean that

A) Radiata should be a true clade.

B) the radial symmetry of extant cnidarians is secondarily derived, rather than being an ancestral trait.

C) Hox genes play little actual role in coding for an animal's "body plan."


3 Are Rotifers Gene Stealers or Uniquely Engineered? Tue Dec 01, 2015 11:30 pm

Otangelo


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Authority Carl Woese has also observed that these problems extend well beyond the base of the tree of life, stating: “Phylogenetic incongruities [conflicts] can be seen everywhere in the universal tree, from its root to the major branchings within and among the various taxa to the makeup of the primary groupings themselves.𔄦 To reiterate, even among higher organisms, as the New Scientist article explains that “The problem was that different genes told contradictory evolutionary stories,” therefore leading one scientist to say regarding the relationships of these higher groups, “We’ve just annihilated the tree of life.” Many studies have reported such problems:
A 2009 paper in Trends in Ecology and Evolution notes that: “A major challenge for incorporating such large amounts of data into inference of species trees is that conflicting genealogical histories often exist in different genes throughout the genome.𔄧 Similarly, a paper in the journal Genome Research studied the DNA sequences in various animal groups and found that “different proteins generate different phylogenetic tree[s].𔄨
A study published in Science in 2005 tried to construct a phylogeny of animal relationships but concluded that “[d]espite the amount of data and breadth of taxa analyzed, relationships among most [animal] phyla remained unresolved.” Again, the problem lies in the fact that trees based upon one gene or protein often conflict with trees based upon other genes. Their study tried to avoid this problem by using a many-gene technique, yet still found that “[a] 50-gene data matrix does not resolve relationships among most metazoan phyla.𔄩
Striking admissions of troubles in reconstructing the “tree of life” also came from a 2006 paper in the journal PLoS Biology, entitled “Bushes in the Tree of Life.” The authors acknowledge that “a large fraction of single genes produce phylogenies of poor quality,” observing that one study “omitted 35% of single genes from their data matrix, because those genes produced phylogenies at odds with conventional wisdom.” The paper suggests that “certain critical parts of the [tree of life] may be difficult to resolve, regardless of the quantity of conventional data available.” The paper even contends that “[t]he recurring discovery of persistently unresolved clades (bushes) should force a re-evaluation of several widely held assumptions of molecular systematics.𔄪 Unfortunately one assumption they were not willing to re-evaluate is that of universal common ancestry.
Another study published in Science found that the molecular data implied that six-legged arthropods, or hexapods (i.e. insects) are not monophyletic, a conclusion that differed strikingly from virtually all previous wisdom. The article concluded “Although this tree shows many interesting outcomes, it also contains some evidently untenable relationships, which nevertheless have strong statistical support.𔄫
A paper in the Journal of Molecular Evolution found that molecule-based phylogenies conflicted sharply with previously established phylogenies of major mammal groups, concluding that this anomalous tree “is not due to a stochastic error, but is due to convergent or parallel evolution.󈭞 Likewise, a study published in Proceedings of the National Academy of Sciences USA explains that when evolutionary biologists tried to construct a phylogenetic tree for the major groups of birds using mitochondrial DNA (mtDNA), their results conflicted sharply with traditional notions of bird relationships. Strikingly, they even find “convergent” similarity between some bird mtDNA and the mtDNA of distant species such as snakes and lizards. The article suggests bird mtDNA underwent “multiple independent originations,” with their study making a “finding of multiple independent origins for a particular mtDNA gene order among diverse birds.󈭟
When testifying before the TSBOE, professor Hillis also made the inaccurate claim that “there’s overwhelming correspondence between the basic structures we have about the tree of life from anatomical data, from biochemical data, molecular sequence data.” Yet many evolutionary scientists have recognized that evolutionary trees based upon morphology (physical characteristics of organisms) or fossils, commonly conflict with evolutionary trees based upon DNA or protein sequences (also called molecule-based trees).

For example, a review paper by Darwinian leaders in this field stated, “As morphologists with high hopes of molecular systematics, we end this survey with our hopes dampened. Congruence between molecular phylogenies is as elusive as it is in morphology and as it is between molecules and morphology.󈭠 Another set of pro-evolution experts wrote, “That molecular evidence typically squares with morphological patterns is a view held by many biologists, but interestingly, by relatively few systematists. Most of the latter know that the two lines of evidence may often be incongruent.󈭡

The widespread prevalence of disagreement and non-correspondence between molecule-based evolutionary trees and anatomy-based evolutionary trees led a review article in Nature to report that “disparities between molecular and morphological trees” cause “evolution wars” because “Evolutionary trees constructed by studying biological molecules often don’t resemble those drawn up from morphology.󈭢

What Exactly Does Genetic Similarity Demonstrate? 1

Origin of genes with unresolved ancestry

The Main Issue: Unintelligent vs. Intelligent Mechanism

My hope is that one day thinking about Darwinian Theory will become clearer in the public square. Recall that Darwin made two claims: (1) all living beings descend from one or a few original ancestors, and (2) the mechanism driving the changes among species is the blind, unguided mechanism of natural selection.

The controversial claim, of course, is the second one--the idea that a purely material mechanism, without any intelligence involved, is responsible for all of the genetic information necessary for life (DNA) and hence for all of life's diversity.

Sequence Similarity Alone Does NOT Prove Common Ancestry

the 98.8% DNA sequence similarity between chimps and humans that Clines references does not even establish claim one (common ancestry). And "you don't have to take my word for it," as LeVar Burton always used to say on Reading Rainbow.

As Francis Collins, head of the project which mapped the human genome, has written of DNA sequence similarities
"This evidence alone does not, of course, prove a common ancestor" because an intelligent cause can reuse successful design principles.

We know this because we are intelligent agents ourselves, and we do this all the time. We take instructions we have written for one thing and use them for another. The similarity is not the result of a blind mechanism but rather the result of our intelligent activity.

Some design proponents think the evidence for common ancestry is good (e.g., Michael Behe), while others--citing the fossil record, especially The Cambrian Explosion--do not. But neither group thinks that sequence similarity alone proves either common ancestry or the Darwinian mechanism, as so many science writers of our day seem eager to assume.

As one specific example, textbooks often cite the phylogenetic tree based upon cytochrome c as purportedly matching and confirming the standard anatomy-based phylogenetic tree of many vertebrates. But one paper in Trends in Ecology and Evolution noted that the cytochrome b tree yielded “an absurd phylogeny of mammals, regardless of the method of tree construction” where “[c]ats and whales fell within primates, grouping with simians (monkeys and apes) and strepsirhines (lemurs, bush-babies and lorises) to the exclusion of tarsiers.” The paper concluded that “Cytochrome b is probably the most commonly sequenced gene in vertebrates, making this surprising result even more disconcerting.󈭣

This problem also exists among higher primates as molecular data often conflicts with the prevalent phylogenetic tree which claims humans are most closely related to chimpanzees.16 As one article in the journal Molecular Biology and Evolution found, “[f]or about 23% of our genome, we share no immediate genetic ancestry with our closest living relative, the chimpanzee.󈭥

The common textbook claim that a universal “tree of life” has been established by congruent molecular and morphological phylogenetic trees is contradicted by much data and scientific opinion – but this information is almost always omitted from textbook instruction given to students.

Are Rotifers Gene Stealers or Uniquely Engineered? 1

The tools of DNA sequencing are becoming cheaper to use and more productive than ever, and the deluge of DNA comparison results between organisms coming forth are becoming a quagmire for the evolutionary paradigm. To prop it up, biologists resort to ever more absurd explanations for discrepancies. A prime example of this trickery is in a recent DNA sequencing project performed in a microscopic aquatic multi-cellular animal called a rotifer.1
In this effort, the researchers targeted those gene sequences that are expressed as proteins for DNA sequencing because the genome was too large and complex to sequence and assemble all of its DNA. They recorded over 61,000 gene sequences that were expressed from rotifers grown in stressed and non-stressed conditions. Of these, they could only find sequence similarities between rotifers and other creatures for 28,922 sequences (less than half). The researchers tossed the unknown DNA sequences out of their analysis since the non-similar genes were novel, apparently specific to rotifer, and essentially difficult for evolution to explain.
Of the 28,922 sequences for which they could obtain a match in a public database of other creature's DNA and protein sequences, a significant proportion (more than in any other creature sequenced) did not fit evolutionary expectations of common descent. Further complicating this picture, the rotifer gene sequences were found in a diverse number of non-rotifer creatures! Some of the creatures that had gene matches to rotifers included a variety of plants, other multicellular animals, protists (complex single celled animals), archaea, bacteria, and fungi. Evolutionists have two options in which to categorize these unusual gene matches based on their naturalistic presuppositions. First, they can say that these genes evolved independently in separate creatures in a hypothetical process called "convergent evolution." However, in cases where there are literally hundreds of these DNA sequences popping up in multiple organisms, this scenario becomes so unlikely that even evolutionists have too much difficulty imagining it. The second option is called "horizontal gene transfer," or HGT. This involves the transfer of genes, perhaps via some sort of microbial host vector such as a bacterium.2
In the present report, the rotifer under study was asexual, limiting heredity as an option for aiding in gene transfer. So the researchers concluded that it stolehundreds of genes via HGT from a plethora of other creatures. HGT is considered somewhat common among bacteria because they form connective tubes (called pili) and exchange little bits of DNA, like sharing software. Also, HGT can occur rarely between a bacterium and a multicellular host that it interacts with during its life cycle.3
How will rotifer researchers account for the massive transfer of hundreds of genes from a broad range of hosts that they believe includes 533 supposed source genomes for which no biological host-based relationships exists? Some sort of causal host relationship must occur for the transfer of one gene, let alonehundreds of genes from hundreds of sources.1
Another problem is that the researchers showed that the so-called "stolen genes" were well-integrated into the rotifer cell biochemistry and its environmental adaptation mechanisms. A separate 2012 study showed that highly expressed native genes could not be shared via HGT, even among bacteria, because they would severely disrupt essential cell biochemistry.4 And these are exactly the types of genes that were surveyed in the rotifer.
In this case, evolutionary biologists have resorted to fictional stories cloaked in technical terminology to escape the straightforward conclusion that rotifer DNA was purposefully crafted. If a large bunch of newly discovered genes don't make evolutionary sense, then evolution proponents ascribe their origin to HGT despite the fact that HGT is not known to operate without any host-based relationship. HGT is also not known to occur en masse, and HGT of essential genes is in theory impossible.4
The unique mix of rotifer genes along with their flawless biochemical integration into the rotifer's cell system, clearly and abundantly supports the special creation described in the Bible.

PBS asserts that "shared amino acids" in genes common to many types of organisms indicate that all life shares a common ancestor. Intelligent design is not necessarily incompatible with common ancestry, but it must be noted that intelligent agents commonly re-use parts that work in different designs. Thus, similarities in such genetic sequences may also be generated as a result of functional requirements and common design rather than by common descent.

In fact, PBS's statement is highly misleading. Darwin's tree of life--the notion that all living organisms share a universal common ancestor--has faced increasing difficulties in the past few decades. Phylogenetic trees based upon one fundamental gene or protein often conflict with trees based upon another gene or protein. In fact, this problem is particularly acute when one studies the "ancient" genes at the base of the tree of life, which PBS wrongly claims demonstrate universal common ancestry. As W. Ford Doolittle explains, "[m]olecular phylogenists will have failed to find the 'true tree,' not because their methods are inadequate or because they have chosen the wrong genes, but because the history of life cannot properly be represented as a tree."1

Doolittle, a Darwinian biologist, elsewhere writes that "there would never have been a single cell that could be called the last universal common ancestor."2 Doolittle attributes his observations to gene-swapping among microorganisms at the base of the tree. But Carl Woese, the father of evolutionary molecular systematics, finds that such problems exist beyond the base of the tree: "Phylogenetic incongruities [conflicts] can be seen everywhere in the universal tree, from its root to the major branchings within and among the various taxa to the makeup of the primary groupings themselves."3

Looking higher up the tree, a recent study conducted by Darwinian scientists tried to construct a phylogeny of animal relationships but concluded that "[d]espite the amount of data and breadth of taxa analyzed, relationships among most [animal] phyla remained unresolved."4 The basic problem is that phylogenetic trees based upon one gene or other characteristic will commonly conflict with trees based upon another gene or macro-characteristic. Indeed, the Cambrian explosion, where nearly all of the major living animal phyla (or basic body plans) appeared over 500 million years ago in a geological instant, raises a serious challenge to Darwinian explanations of common descent.

The nice, neat, nested hierarchy of a grand Tree of Life predicted by Darwinian theory has not been found. Evolutionary biologists are increasingly appealing to epicycles like horizontal gene transfer, differing rates of evolution, abrupt molecular radiation, convergent evolution (even convergent molecular evolution), and other ad hoc rationalizations to reconcile discrepancies between phylogenetic hypothesis. Darwinian biology is not explaining the molecular data it is forced to explain away the data. PBS paints a rosy picture of the data, when the data isn't good news for Darwinism.

Strange Findings on Comb Jellies Uproot Animal Family Tree 3

Complete sequence of comb jelly genome reveals a separate course of evolution.

The new study on ctenophores, such as the American comb jelly above, "really shakes up how we think animal complexity evolved."

PHOTOGRAPH BY GEORGE GRALL, NATIONAL GEOGRAPHIC CREATIVE


A close look at the nervous system of the gorgeously iridescent animal known asthe comb jelly has led a team of scientists to propose a new evolutionary history: one for the comb jelly, and one for everybody else.
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"It's a paradox," said Leonid Moroz, a neurobiologist at the University of Florida in Gainesville and lead author of a paper in today's Nature about the biology of the comb jelly nervous system. "These are animals with a complex nervous system, but they basically use a completely different chemical language" from every other animal. "You have to explain it one way or another."
The way Moroz explains it is with an evolutionary scenario—one that's at odds with traditional accounts of animal evolution.
Moroz and his colleagues have been studying comb jellies, whose scientific name is ctenophores (pronounced TEN-o-fors), for many years, beginning with the sequencing of the genome of one species, the Pacific sea gooseberry, in 2007. The sea gooseberry has 19,523 genes, about the same number as are found in the human genome.
The scientists enlarged their library to the genes of ten other species of comb jelly (out of the 150 or so species known to exist) and compared them to the analogous genes in other animals. And when they looked at the genes involved in the nervous system, they found that many considered essential for the development and function of neurons were simply missing in the comb jelly.
Some of those missing genes are involved in building neurons in embryos. The cells in any animal start out in the embryo as stem cells, looking pretty much identical to one another and capable of turning into any particular type of cell. Only later in embryonic development do some stem cells switch on specific genes that transform them into neurons. This process is much the same in humans as it is in flies, slugs, and just about every other animal with a nervous system.
But comb jellies, Moroz and his colleagues found, lack those neuron-building genes altogether. Which means that comb jelly embryos must build their neurons from a different set of instructions—instructions no one yet understands.
Nor do comb jellies use the standard complement of neurotransmitters found in other animals, the scientists found. The genes for most of the neurotransmitters in other animals are either missing or silent in the comb jelly—except for one, the gene for the neurotransmitter glutamate. No wonder Moroz likes to call these creatures "aliens of the sea."
Instead of the typical neurotransmitter genes, the scientists found, comb jellies produce a huge diversity of receptors on the surface of their neurons. Moroz can't say yet what the receptors are doing there, but he says they're probably grabbing neurotransmitters, maybe as many as 50 to 100 neurotransmitters in all (comparable to the number of neurotransmitters in the human brain).
Rewriting Evolutionary History
The unique nature of the comb jelly nervous system led the Florida scientists to hypothesize a new evolutionary history for these marine animals, which they laid out in the Nature paper. The earliest animals, according to this new theory, had no nervous system at all. The cells of these early animals could sense their environment directly, and could send signals directly to neighboring cells.
Millions of years later, those signals and receptors became the raw material for the nervous system. But its evolution, according to Moroz, took place in two separate lineages. One led to today's ctenophores. The other led to all other animals with nervous systems—from jellyfish to us.
If there was indeed a parallel evolution with two separate lineages, the split would have happened long ago. Fossils that look a lot like modern-day ctenophores date back some 550 million years, making them among the oldest traces of complex animal life.
But precisely how and when the comb jelly split off from other animal lineages remains controversial. To draw the animal evolutionary tree, Moroz and his colleagues analyzed the similarity of DNA in different species. According to the authors, ctenophores belong to a lineage all their own that split off from the others at the tree's base.

Comb jellies, like this one at Monterey Bay Aquarium, California, are missing many genes considered essential for the development and function of neurons.

PHOTOGRAPH BY GEORGE GRALL, NATIONAL GEOGRAPHIC CREATIVE


In finding that relationship, the new paper confirms the findings of a team led byAndy Baxevanis, head of the Computational Genomics Unit at the National Human Genome Research Institute, who arrived at a similar conclusion in December after sequencing the genome of another ctenophore species, the American comb jelly (Mnemiopsis leidyi). "You couldn't ask for a better outcome," he said about Moroz's research. "It really shakes up how we think animal complexity evolved."
Gert Woerheide, an evolutionary geobiologist at Ludwig-Maximilians-Universität in Munich, who was not involved in the research, agreed that Moroz and his colleagues have made a thorough case for their revised view of brain evolution. "I think, in this respect, this is a great paper," he said.
But in terms of the actual shape of the animal family tree, Woerheide is less convinced. He isn't sure that comb jellies branched off at the base of the tree, he said sponges, for example, might have branched off first. In Woerheide's view, the exact reconstruction of the tree reaching so far back in evolutionary history remains an open question.
No matter how the nervous systems of comb jellies evolved, though, everyone agrees that they are weird—and thus worth getting to know better. As Casey Dunn, an evolutionary biologist at Brown University in Providence, Rhode Island, who was not involved in the research, pointed out, comb jellies are turning out to be "even more different from other animals than had previously been appreciated."

Encyclopedia of the tree of life 4

Presumably, “tree of life” is placed in quotation marks because it so little resembles a tree. Didn’t it used to be capped, as Tree of Life?

Octopuses ‘are aliens’, scientists decide after DNA study 5

Not to freak you out or anything, but scientists have just revealed that octopuses are so weird they’re basically aliens.
The first full genome sequence shows of that octopuses (NOT octopi) are totally different from all other animals – and their genome shows a striking level of complexity with 33,000 protein-coding genes identified, more than in a human.
There we were thinking it was quite freaky enough when they learned how to open jam jars.
US researcher Dr Clifton Ragsdale, from the University of Chicago, said: The octopus appears to be utterly different from all other animals, even other molluscs, with its eight prehensile arms, its large brain and its clever problem-solving abilities.
‘The late British zoologist Martin Wells said the octopus is an alien. In this sense, then, our paper describes the first sequenced genome from an alien.’
Octopuses: What even ARE they?
They inhabit every ocean at almost all depths and possess a range of features that call to mind sci-fi aliens.
These include prehensile sucker-lined tentacles, highly mobile, camera-like eyes sensitive to polarised light, sophisticated camouflage systems that alter skin colour and patterns, jet-propulsion, three hearts, and the ability to regenerate severed limbs.
The scientists estimate that the two-spot octopus genome contains 2.7 billion base pairs – the chemical units of DNA – with long stretches of repeated sequences.

1) http://www.icr.org/article/are-rotifers-gene-stealers-or-uniquely/
2) http://www.evolutionnews.org/2008/01/darwins_failed_predictions_sli_8004654.html
3) http://news.nationalgeographic.com/news/2014/05/140521-comb-jelly-ctenophores-oldest-animal-family-tree-science/
4) http://www.uncommondescent.com/tree-of-life/encyclopedia-of-the-tree-of-life/
5) http://metro.co.uk/2015/08/12/octopuses-are-aliens-scientists-decide-after-dna-study-5339123/#ixzz3ievvjMOZ

Last edited by Otangelo on Mon Jun 14, 2021 4:32 pm edited 4 times in total


Shared Flashcard Set

- We need characteristics that describe the vast majority of animals and sufficiently defines the group.

- All animals are heterotrophs. Must consume other organisms to gain energy. Can't make their own food.

CELL STRUCTURE AND SPECIALIZATION

Their cells lack __ __. The __ __ comes from something else.

Their bodies are held together by __. What is this?

All cells have __ functions.

cell walls, support structure

collagen, which is a type of protein.

REPRODUCTION AND DEVELOPMENT

How do most animals reproduce?

__ stage usually dominating the life cycle.

__ of these genes can create a __ __, or development.

Hox genes are genes in which only animals have. They regulate the development of body form.

can produce a wide diversity of animal morphology.

Manipulation, diverse morphology.

What is the common ancestor of living animals?

There is no exact answer to how old animals are but as of now, the oldest animal is marked to be 625 million years old.

common ancestor - choanoflagellates - was probably itself a colonial, flagellated protist.

What do the animals look like?

- The __ explosion: marks the __ __ of many major groups of living animals.

What are 3 of the several current hypotheses concerning the fast evolution of animals?

They look foreign. Not like modern animals.

Cambrian, earliest appearance.

1. predator-prey interactions - increasing competition is causing evolution to speed up.

2. atmospheric oxygen - O2 itself will change DNA of animals because it is a mutagen.

3. Hox genes - causes rapid development of animals which causes rapid evolution

Mesozoic Era (251 - 65.5 MYA)

What do the animals look like?

__ life dominated by several forms of __.

animals look more normal. Jurassic era also part of this era.

Cenozoic Era (65.5 MYA to present)

Terrestrial dominated by __ and __.

Change in dominance often precipitated by __ __.

In order to classify animals we need to develop __ that all animals have and we can __.

The more __ that organisms share the more __ they are.

What two types of characteristics can we use?

morphological and molecular/genetic (DNA, RNA, etc.)

the second way we present evolutionary relationships is with __ __.

The distance determines the __ between organisms.

CLASSIFICATION OF BODY PLAN

What is a way that zoologists categorize the diversity of animals?

"these" charaters include what four characteristics?

What are the two types of symmetry in Animalia?

Radial symmetry - The organism can be cut in half multiple times.

Bilateral symmetry - organism can be only cut in half once.

What are the parts of the animal's bilateral symmetry called?

dorsal (top), ventral (bottom)

anterior (head), posterior (tail)

Cephalization is the development of a head.

Animal embryos form __ layers, __ tissues including __, __, and __.

What is it called to have 2 germ layers? 3 germ layers?

tissues are collections of specialized celles isolated from other tissues by membranous layers.

germ, embryonic, ectoderm, endoderm, and mesoderm.

The presence and complexity of a __ __ can also be used to organize animals into __. This means it can determine who is related to who.

What is it called to have a body cavity?

What are organisms without body cavities called?

have a true body cavity. these are the most common.

is called a coelom and is derived from mesoderm.

We classify animals by __ in development.

what are the two development modes?

protostome and deuterostome

In protostome development cleavage is __ and __.

In deuterostome development cleavage is __ and __.

what is protosome development?

what is deuterostome development?

protosome - the splitting of initially solid masses of mesoderm to form the coelomic cavity is called schizocoelous development

deuterostome - formation of the body cavity is described as enterocoelous development

in protostome development - the blastopore becomes the __.

in deuterostome development - the blastopore becomes the __.

Zoologists currently recognize about __ animal phyla.

there is __ on the relationships among phyla

there is two __ hypotheses.

what are these two hypotheses?

a morphology hypothesis: based on morphological and developmental comparisons.

molecular hypothesis: based on molecular data

all animals share a common ancestor: __.

__ is a clade of animals with __ tissues.

most animal phyla belong to the clade __.

vertebrates and some other phyla belong to the clade __.

DISAGREEMENT OVER THE BILATERIANS

The morphology-based tree: divides the bilaterians into what two clades?

in contrast, serveral recent molecular studies.. generally assign two siter taxa to the protostomes rather than one:the __ and __.


Results and discussion

Adding a new placozoan genome and improving the T. adhaerens genome annotation

Based on mitochondrial 16S ribosomal DNA (rDNA) analyses, the genetic lineage H13 is among the most distantly related haplotype to T. adhaerens (lineage H1) [5], whose nuclear genome has been sequenced previously [22]. We hypothesized that the substantial 16S rDNA divergence might also be reflected on the whole-genome scale and, therefore, targeted H13 for nuclear genome sequencing. To assemble the genome of H13—a new species described here, called H. hongkongensis nov. gen., nov. spec. (Fig 1, S1 Fig see species description in Material and methods Tables 1 and 2)—we generated 24 Gb of paired-end reads and 320 Mb of Moleculo (Illumina Artificial Long Synthetic) reads. Our final, highly complete 87-megabase assembly contained 669 high-quality and contamination-filtered contigs with an N50 of 407 kb (S1 Table S2–S4 Figs), 7 megabases smaller than the T. adhaerens contig assembly. The overall calculated genome heterozygosity (based on single-nucleotide polymorphism [SNP] counts, see S2 Table) was 1.6%, which is moderate for a marine animal but about average when compared to arthropods and high in comparison to terrestrial chordates [33]. This value cannot be compared to T. adhaerens because of the low genome coverage of the latter, which does not allow haplotype phasing.

We annotated the genome with a combination of 15.3 Gb of RNA-Seq and ab initio methods to yield 12,010 genes (S1 Table, S1 & S2 Data). A high percentage of raw reads mapped back to the genome (S3 Table), and between 90.8%–95.3% of the 978 genes in the BUSCO v3 Metazoa dataset were identified in the transcriptome and the ab initio gene models, respectively (S4 Table). Together, this suggests an almost complete assembly and annotation, in which 96.5% of the genes in the H. hongkongensis genome were expressed in what are commonly considered adult animals. In our gene set, H. hongkongensis had 490 more genes than the 11,520 genes reported in the original T. adhaerens annotation from 2008 [22]. We reannotated T. adhaerens with AUGUSTUS and found an additional 1,001 proteins and also managed to complete formerly partial proteins (for T. adhaerens Blast2GO protein annotations see S3 Data). This approach added 4.4 Mb of exons to the T. adhaerens annotation, an increase of 28% of exonic base pairs to the original annotation. The new T. adhaerens annotation now has 511 more genes than H. hongkongensis, which accounts for some portion of the size difference between the two genomes.

Genomic rearrangements are commonplace

Moleculo reads also enabled us to assemble very large reference contigs, the longest being over 2 Mb. We compared the organization of genes in H. hongkongensis to the 10 longest scaffolds in the T. adhaerens genome (size range 2.4–13.2 Mb accounting for 66% of the T. adhaerens assembly). We found 144 contigs >100 kb from H. hongkongensis that aligned to these 10 scaffolds, accounting for 69% of the H. hongkongensis assembly (Fig 2A). Mean gene collinearity (i.e., the same genes in the same direction) in this reduced genome representation was in the range of 69.5% to 78.8% (mean 73.6% ± 5.5% see S5 Table). The mean number of genes per syntenic block was 33.8 (±25.2) in the reduced set and 33.9 (±24.7) when comparing full genomes (S5 Fig), which indicates that the reduced set is representative for both complete genomes.

(A) Scaled schematic drawings of the 10 longest T. adhaerens scaffolds on the left (ta1–ta10) and matching H. hongkongensis contigs on the right. While a general macrosynteny between the two placozoan species is present (gray lines), 25% of the genes are translocated (blue lines) or inverted (orange lines) relative to the order of the respective T. adhaerens scaffold (illustrated for ta1). Often, entire gene blocks are translocated (different colors in boxed H. hongkongensis contigs). Black stretches mark genomic regions not matching any of the 10 T. adhaerens scaffolds, while white stretches mark gaps in the T. adhaerens scaffolds. (B) Pairwise protein and CDS distances for 6,554 one-to-one orthologous genes. A significant fraction of orthologs have larger protein than CDS distance, but only three of these are, in fact, positively selected (reflected by dN/dS ratios > 1, gray line). Orthologs are sorted by increasing dN/dS. Calculated distances can be found in the H. hongkongensis data repository at https://bitbucket.org/molpalmuc/hoilungia-genome/src/master/orthologs/. CDS, coding sequence dN/dS, nonsynonymous to synonymous nucleotide substitutions.

Although much of the gene order is conserved between the two species, we counted 2,101 genes (out of the 8,260 genes in the 10 scaffolds) that were inverted or translocated within the same scaffold relative to the order in the T. adhaerens scaffolds. These numbers seem low when compared to the fast-evolving bilaterian genus Drosophila [34,35] or Caenorhabditis [36], but they are in the range of rearrangements found between mouse and human [37]. Comparison to Bilateria, however, might be misleading (see also results on genetic distances below), and genome rearrangement events might be more favored in some bilaterian taxa because of inherent genomic traits such as transposon-induced rearrangement hotspots [38]. Nonetheless, the high percentage of rearrangements between T. adhaerens and H. hongkongensis is clear evidence for a deep genetic separation of both lineages.

Sequence divergence analyses identify unexpectedly high genetic distances between H. hongkongensis and T. adhaerens

To estimate how divergent the two placozoan genomes are at the sequence level, we calculated genetic distances for 6,554 one-to-one orthologs. Between H. hongkongensis and T. adhaerens, genetic distances ranged from 0.9% to 80.1% (mean 28.3% ± 12.9%) for proteins and 7.4% to 80.7% (mean 28.5% ± 9.9%) for coding sequences (CDSs), respectively (Fig 2B). To assess if certain genes are under positive (diversifying) selection, indicative of functional evolution, we calculated the ratio of nonsynonymous to synonymous nucleotide substitutions (dN/dS ratio [39]) for each H. hongkongensis and T. adhaerens one-to-one ortholog pair. Results show that most orthologs (97%) are under strong purifying selection (dN/dS < 0.5). One might hypothesize that strong purifying selection pressure is the reason for the phenotypic stasis we see in modern placozoans. However, more placozoan genomes in the phylum are clearly needed to test this hypothesis. Despite this strong tendency toward purifying selection, a high proportion of orthologs (46%) showed larger protein distance than CDS distance and, therefore, an accumulation of double or triple mutations in already mutated codons, which led to amino acid substitutions (S6 Fig).

Only 3 of the 6,554 one-to-one orthologs had dN/dS ratios slightly >1, indicating positive selection (S7 Data see S6 Fig for an estimate of mutation saturation in codons). One of these seems placozoan specific, since it could not be annotated because of missing UniProt BLAST hits and InterPro domains, respectively. For the second, GO annotation and InterPro IDs indicate a role in telomere maintenance. The third positively selected gene (CYP11A1) is putatively a cholesterol side-chain cleavage enzyme acting in the mitochondrion.

The roughly 4x coverage of the genome with long Moleculo reads (N50 of 5.4 kb) allowed the assembly of large haplocontigs (i.e., contigs representing both haplotypes of the genome). This phasing information for large parts of the genome facilitated the isolation of 2,870 one-to-one orthologs with both full-length alleles after a highly stringent filtering procedure. Only by using the phasing information we were able to show that many orthologs with high allelic variation in H. hongkongensis were also profoundly different between the species (S7 Fig). This indicates that genetic sequence adaptation already takes place at the population level and is further magnified between species in the same genes.

Adaptation by gene duplication is one key mechanism for speciation in the Placozoa

The Markov cluster (MCL) analysis identified 6,644 true one-to-one orthologs (for an overview of ortholog categories, see Material and methods and [40]) for both placozoan species (55% of all proteins in H. hongkongensis and 53% in T. adhaerens, respectively) (S8 Fig). A fraction of 465 (3.8%) H. hongkongensis and 1,036 (8.3%) T. adhaerens proteins, respectively, did not have reciprocal BLAST hits. The difference in the non-BLAST hits almost perfectly matches the differences in total gene numbers, which is probably an indication that genes without a homolog in H. hongkongensis account at least partially for the slightly higher gene number in T. adhaerens. A high proportion of proteins had BLAST hits to the UniProt database, and only 15.4% (1,859) and 19.0% (2,384) of H. hongkongensis and T. adhaerens proteins, respectively, did not have BLAST hits to metazoans included in UniProt.

Placozoan-specific duplications constitute a significant proportion of both proteomes, with 3,943 (32.8%) co-orthologs in H. hongkongensis and 3,484 (27.8%) in T. adhaerens. The enrichment analyses for the proteins in each non-BLAST-hit bin identified unique GO terms in all three GO categories among the first five most significantly enriched GO terms (S4 & S5 Data). The same applies to one-to-many and many-to-one co-orthologs in both species.

The enrichment analyses further indicate that both placozoan species have multiple co-orthologs associated with G-protein-coupled receptor (GPCR) signaling. A rich repertoire of GPCRs has been identified in T. adhaerens [22], but here, we were able to identify independent GPCR duplications in H. hongkongensis and T. adhaerens, respectively (S6 Data). Furthermore, we identified multiple enriched GO terms related to synaptic activity in all co-ortholog categories (S5 Data) and both placozoan species. This points to a plethora of independent duplication events in gene families related to sensory capacities. Despite lacking neurons (based on traditional morphological classifications), T. adhaerens has previously been shown to stain positive for FMRFamide [10,41] and recently even to change behavior when exposed to physiologically relevant levels of neuropeptides [31].

Based on the identification of vast and independent gene family expansions in both placozoans, we propose that adaptation in the Placozoa, ultimately leading to speciation, is coupled with independent gene duplications as suggested, for example, for bacteria, yeast, plants, and other animals (compare [42–45]). H. hongkongensis was isolated from a stream running through a mangrove with rapid drops in salinity and temperature, especially during heavy rainfall in the summer. We hypothesize that the presence of multiple divergent copies of genes involved in various processes, such as behavior and metabolism (compare [42,43]), in addition to a situation-dependent expressional fine-tuning of these copies was necessary for adaptation to this habitat and would facilitate speciation. We furthermore propose that the presence of multiple copies of genes and their expression does not affect the phenotype but instead provides a genetic toolkit for gradual physiological responses to (changes in) the environment.

Allele sharing analyses identify reproductive isolation between placozoan clades

All internal Linnaean ranks within the Placozoa are, as yet, undefined [5]. Despite efforts to identify them, reliable diagnostic morphological characters, commonly used for defining animal species, are lacking in the Placozoa [46]. Thus, all present taxonomic definitions in the phylum must solely rely on diagnostic molecular characters. In other taxonomic groups (e.g., bacteria and archaea [47], protists [48,49], and fungi [50]), purely sequence-based approaches and working models for the distinction of taxa have been proposed and are generally well established and widely accepted [51]. In animals, such methods (which may be based on distances, on trees, or on allele sharing [52]) are currently under development and have been used in rare cases to identify and describe cryptic species [53].

In a first step to converting the identified genomic differences into a taxonomically meaningful system, we studied reproductive isolation by addressing allele sharing within placozoan isolates from different localities. To identify reproductive isolation, a conspecificity matrix (CM) was generated [54]. The CM was based on three nuclear genes encoding ribosomal proteins and clearly identified reproductive isolation between placozoan clades (Fig 3). This approach extends a previous study that has uncovered sexual reproduction only within one placozoan haplotype (H8) [20] and provides clear evidence that the previously established placozoan clades (based on 16S genotyping) are reproductively isolated biological species.

The CM for three nuclear-encoded ribosomal proteins (rpl9, rpl32, and rpp1) was generated by calculating (for each pair of isolates) the number of markers supporting their conspecificity in haploweb analyses (i.e., different individuals can be assigned to one species by shared alleles) minus the number of markers supporting the premise that they belong to different species. The CM was visualized as a heat map with different colors representing various amounts of shared alleles from −3 (no shared alleles) to +3 (3 shared alleles). Higher scores (red), therefore, indicate conspecific isolates, while gray tones support reproductive isolation, i.e., separate biological species. The number of sequenced markers per isolate is given in brackets beside the isolate (see S6 Table for details on isolates). The CM shows that allele sharing can occur between haplotypes within but never between clades. This is the first evidence for reproductive isolation between placozoan clades and the first molecular support for the existence of biological species in the Placozoa. The CM furthermore supports the phylogenetic split between Trichoplax (clade I note: no data available for clade II) and the new placozoan genus Hoilungia (clades III–VII), as shown in the dendrogram on top of the heatmap. These clades are consistent with those recovered from analyses of the mitochondrial ribosomal large subunit (16S) [5] and compensatory base changes in the ITS2 [55]. Data underlying this figure can be found at https://bitbucket.org/molpalmuc/hoilungia-genome/src/master/reproductive_isolation/. CM, conspecificity matrix ITS2, internal transcribed spacer 2.

Cross-phylum comparative distance analyses allows the establishment of a new genus in the Placozoa

We have shown that biological species exist in the Placozoa. Previous studies have furthermore provided first indications for the existence of deeper differences between placozoan lineages [1,3], with as-yet-unknown correspondence to, for example, the Linnaean ranks of genus, family, order, and class. However, these observed deeper divergences were based on single marker genes only, and no diagnostic morphological traits could be identified to establish a firm, higher-level, systematic framework in the Placozoa. To further estimate the level of taxonomic relatedness between T. adhaerens and the new placozoan species H. hongkongensis (strain H13), and in an attempt to initiate a higher-level taxonomic system for the Placozoa, we performed cross-phylum multimarker sequence divergence analyses. To do so, we compared the variation between the two placozoans to variation within the other three nonbilaterian phyla, Cnidaria, Ctenophora, and Porifera (compare [1]), as well as the bilaterian phylum Chordata. Marker sets included a nuclear protein set of 212 concatenated proteins (dataset 1, a taxon-extended matrix from [56] S7–S9 Tables see Fig 4) as well as 5 selected genes with different substitution rates (S9–S14 Figs), all commonly used for DNA barcoding and molecular systematics.

Mean group distances for different taxonomic ranks in three nonbilaterian phyla (Cnidaria, Ctenophora, and Porifera) and the bilaterian phylum Chordata. The interspecific protein distance of 9.6% between H. hongkongensis and T. adhaerens (right) is comparable to mean group distances between genera within families in the Ctenophora. With respect to the Cnidaria, the placozoan distance is even comparable to the mean group distance between families within orders. Measured distances for families within orders in Ctenophora and genera within families in Porifera indicate that classical morphological taxonomies are incongruent with the calculated genetic distances in these two phyla (see also S9–S14 Figs). The internal phylogeny of these two phyla appears to be in urgent need of further reevaluation with the inclusion of molecular data (compare [57–60]). Measured distances in chordates fall way below distances calculated for the nonbilaterian taxa for all levels of comparison. Numbers in brackets are total taxa in the final matrix of 212 concatenated proteins. For calculated distances, see S8 Data.

Across individual markers, it appears that the phylogenetic ranks are most robust in the Cnidaria, in which the partitioning of molecular variation matches the established taxonomy, in that Linnaean ranks consistently correspond to the greater distance between groups (Fig 4 S9–S14 Figs). The same is true for the Chordata, which was included in our distance calculations for the 212 nuclear protein set as an example of a bilaterian phylum with a high taxonomic coverage (many genomes are available for this group). However, distances in chordates are, in general, much lower when compared to the overall more similar nonbilaterian phyla. This indicates that (i) genetic distances and corresponding Linnaean rank assignments in Chordata cannot be compared to nonbilaterian lineages and (ii) that comparisons among nonbilaterians are better suited to guide taxonomic ranking of the two placozoan species. We consequently used genetic distances in the Cnidaria as an approximation and comparative guideline for the higher systematic categorization of the new placozoan species.

Genetic distances between H. hongkongensis and T. adhaerens were higher than those for the Cnidaria in five of the six marker sets at the generic level but lower at the family level for all markers (S14 Fig, S10 Table), which, cautiously interpreted, supports genus-level genetic differences between the two placozoans.

A clear split of the Placozoa in the molecular groups “A” and “B” was previously shown by the rearrangement pattern of mitochondrial genomes [61] and compensatory base changes in the internal transcribed spacer 2 (ITS2) [55]. The conspecificity analysis, the high amount of genomic rearrangement, and the large-scale independent gene duplication history, as well as the genetic distances in six independent datasets, strongly support this split (Fig 3). Since clades were identified as the primary taxonomic units—i.e., biological species—these two previously identified higher-level placozoan “groups” consequently represent at least the genus level in the Linnaean hierarchical system. We therefore establish the new genus Hoilungia for the former group “A” (clades III–VII), which is, so far, the single sister genus to Trichoplax (former group “B” clades I and II).

Future research efforts focusing on genome sequencing of additional placozoan clades/species will likely help to establish a broader and more detailed systematic framework for the Placozoa and provide further insights into the mechanisms and driving forces of speciation in this enigmatic marine phylum.

The H. hongkongensis genome adds support to the phylogenetic placement of the Placozoa in the animal tree of life

Recent discussions about the phylogenetic position of placozoans have largely been based on the T. adhaerens genome. A better sampling of placozoan genomic diversity is, however, needed [62] to address their placement in the metazoan tree of life. In this context, it is important to first assess if adding another placozoan genus would break up the long placozoan branch. The inclusion of a single representative of a clade with a very long terminal branch, or fast-evolving taxa that can have random amino acid sequence similarities, may result in erroneous groupings in a phylogeny (so-called “long-branch attraction artefacts”) [63,64]. To address these questions, we generated a highly (taxa) condensed version of the full protein matrix from Cannon and colleagues [56] (termed dataset 2 with less than 11% missing characters and 194 genes). We additionally created a Dayhoff 6-state recoded matrix [65,66] of this second set to reduce amino acid compositional heterogeneity, which is also known to be a source of phylogenetic error [67,68]. Phylogenetic analyses were performed on these two matrices (protein and Dayhoff-6 recoded), using the site-heterogeneous CAT-GTR model in PhyloBayes-MPI [69] and using the site-homogenous GTR model both in Phylobayes-MPI and RAxML (RAxML, protein only) [70], as well as the LG model in RAxML (protein only). The resulting trees (S15–S20 Figs) of the highly dense gene matrix (S21 Fig) suggest a sister group relationship of the Placozoa to a Cnidaria + Bilateria clade with both CAT-GTR (Protein, Dayhoff-6 recoded, S15–S17 Figs) and GTR models (Protein, S18 Fig) in PhyloBayes, or these relationships are unresolved (RAxML, protein, both GTR, S19 Fig, and LG, S20 Fig). This is in agreement with some previous findings [56,64,71–74] and with recent studies using a large gene set and intense quality controls [64] as well as improved modeling of compositional heterogeneity [68]. In addition, the sister group relationship of the Placozoa to the Cnidaria + Bilateria clade is corroborated by independent data—namely, the analysis of metazoan genome gene content [73,75,76].


Regarding the kingdom Animalia, which phylogenic tree is more common: Molecular Comparisons or Body-Plan Grades - Biology

74 notecards = 19 pages ( 4 cards per page)

Campbell Biology Chapter 32 (powell_h)

1) Both animals and fungi are heterotrophic. What distinguishes animal heterotrophy from fungal heterotrophy is that only animals derive their nutrition by
A) preying on animals.
B) ingesting it.
C) consuming living, rather than dead, prey.
D) using enzymes to digest their food.

2) The larvae of some insects are merely small versions of the adult, whereas the larvae of other insects look completely different from adults, eat different foods, and may live in different habitats. Which of the following most directly favors the evolution of the latter, more radical, kind of metamorphosis?
A) natural selection of sexually immature forms of insects
B) changes in the homeobox genes governing early development
C) the evolution of meiosis
D) the development of an oxidizing atmosphere on Earth
E) the origin of a brain

3) Which of the following is (are) unique to animals?
A) cells that have mitochondria
B) the structural carbohydrate, chitin
C) nervous conduction and muscular movement
D) heterotrophy
E) Two of these responses are correct.

4) What do animals as diverse as corals and monkeys have in common?
A) body cavity between body wall and digestive system
B) number of embryonic tissue layers
C) type of body symmetry
D) presence of Hox genes
E) degree of cephalization

5) The Hox genes came to regulate each of the following in what sequence, from earliest to most recent?

1. identity and position of paired appendages in protostome embryos
2. anterior-posterior orientation of segments in protostome embryos
3. positioning of tentacles in cnidarians
4. anterior-posterior orientation in vertebrate embryos

A) 4 → 1 → 3 → 2
B) 4 → 2 → 3 → 1
C) 4 → 2 → 1 → 3
D) 3 → 2 → 1 → 4
E) 3 → 4 → 1 → 2

6) In individual insects of some species, whole chromosomes that carry larval genes are eliminated from the genomes of somatic cells at the time of metamorphosis. A consequence of this occurrence is that
A) we could not clone a larva from the somatic cells of such an adult insect.
B) such species must reproduce only asexually.
C) the descendents of these adults do not include a larval stage.
D) metamorphosis can no longer occur among the descendents of such adults.
E) Two of these responses are correct.

7) The last common ancestor of all animals was probably a
A) unicellular chytrid.
B) unicellular yeast.
C) multicellular algae.
D) multicellular fungus.
E) flagellated protist.

8) Evidence of which structure or characteristic would be most surprising to find among fossils of the Ediacaran fauna?
A) true tissues
B) hard parts
C) bilateral symmetry
D) cephalization
E) embryos

9) Which statement is most consistent with the hypothesis that the Cambrian explosion was caused by the rise of predator-prey relationships?
A) increased incidence of worm burrows in the fossil record
B) increased incidence of larger animals in the fossil record
C) increased incidence of organic material in the fossil record
D) increased incidence of fern galls in the fossil record
E) increased incidence of hard parts in the fossil record

10) Which of the following genetic processes may be most helpful in accounting for the Cambrian explosion?
A) binary fission
B) mitosis
C) random segregation
D) gene duplication
E) chromosomal condensation

11) Whatever its ultimate cause(s), the Cambrian explosion is a prime example of
A) mass extinction.
B) evolutionary stasis.
C) adaptive radiation.
D) All three of the responses are correct.
E) Only two of the responses are correct.

12) Fossil evidence indicates that the following events occurred in what sequence, from earliest to most recent?

1. Protostomes invade terrestrial environments.
2. Cambrian explosion occurs.
3. Deuterostomes invade terrestrial environments.
4. Vertebrates become top predators in the seas.

A) 2 → 4 → 3 → 1
B) 2 → 1 → 4 → 3
C) 2 → 4 → 1 → 3
D) 2 → 3 → 1 → 4
E) 2 → 1 → 3 → 4

13) What is the probable sequence in which the following clades of animals originated, from earliest to most recent?

1. tetrapods
2. vertebrates
3. deuterostomes
4. amniotes
5. bilaterians

A) 5 → 3 → 2 → 4 → 1
B) 5 → 3 → 2 → 1 → 4
C) 5 → 3 → 4 → 2 → 1
D) 3 → 5 → 4 → 2 → 1
E) 3 → 5 → 2 → 1 → 4

14) Arthropods invaded land about 100 million years before vertebrates did so. This most clearly implies that
A) arthropods evolved before vertebrates did.
B) extant terrestrial arthropods are better adapted to terrestrial life than are extant terrestrial vertebrates.
C) ancestral arthropods must have been poorly adapted to aquatic life, and thus experienced a selective pressure to invade land.
D) vertebrates evolved from arthropods.
E) arthropods have had more time to coevolve with land plants than have vertebrates.

15) An adult animal that possesses bilateral symmetry is most certainly also
A) triploblastic.
B) a deuterostome.
C) eucoelomate.
D) highly cephalized.

16) Soon after the coelom begins to form, a researcher injects a dye into the coelom of a deuterostome embryo. Initially, the dye should be able to flow directly into the
A) blastopore.
B) blastocoel.
C) archenteron.
D) pseudocoelom.

17) A researcher is trying to construct a molecular-based phylogeny of the entire animal kingdom. Assuming that none of the following genes is absolutely conserved, which of the following would be the best choice on which to base the phylogeny?
A) genes involved in chitin synthesis
B) collagen genes
C) β-catenin genes
D) genes involved in eye-lens synthesis
E) genes that cause radial body symmetry

18) At which developmental stage should one be able to first distinguish a diploblastic embryo from a triploblastic embryo?
A) fertilization
B) cleavage
C) gastrulation
D) coelom formation
E) metamorphosis

19) At which developmental stage should one be able to first distinguish a protostome embryo from a deuterostome embryo?
A) fertilization
B) cleavage
C) gastrulation
D) coelom formation
E) metamorphosis

20) What distinguishes a coelomate animal from a pseudocoelomate animal is that coelomates
A) have a body cavity, whereas pseudocoelomates have a solid body.
B) contain tissues derived from mesoderm, whereas pseudocoelomates have no such tissue.
C) have a body cavity completely lined by mesodermal tissue, whereas pseudocoelomates do not.
D) have a complete digestive system with mouth and anus, whereas pseudocoelomates have a digestive tract with only one opening.
E) have a gut that lacks suspension within the body cavity, whereas pseudocoelomates have mesenteries that hold the digestive system in place.

21) You have before you a living organism, which you examine carefully. Which of the following should convince you that the organism is acoelomate?
A) It is triploblastic.
B) It has bilateral symmetry.
C) It possesses sensory structures at its anterior end.
D) Muscular activity of its digestive system distorts the body wall.

22) The blastopore is a structure that first becomes evident during
A) fertilization.
B) gastrulation.
C) the eight-cell stage of the embryo.
D) coelom formation.
E) cleavage.

23) The blastopore denotes the presence of an endoderm-lined cavity in the developing embryo, a cavity that is known as the
A) archenteron.
B) blastula.
C) coelom.
D) germ layer.
E) blastocoel.

24) Which of the following is descriptive of protostomes?
A) spiral and indeterminate cleavage, blastopore becomes mouth
B) spiral and determinate cleavage, blastopore becomes mouth
C) spiral and determinate cleavage, blastopore becomes anus
D) radial and determinate cleavage, blastopore becomes anus
E) radial and determinate cleavage, blastopore becomes mouth

25) Which of the following characteristics generally applies to protostome development?
A) radial cleavage
B) determinate cleavage
C) diploblastic embryo
D) blastopore becomes the anus
E) archenteron absent

26) Protostome characteristics generally include which of the following?
A) a mouth that develops secondarily, and far away from the blastopore
B) radial body symmetry
C) radial cleavage
D) determinate cleavage
E) absence of a body cavity

27) The most ancient branch point in animal phylogeny is that between having
A) radial or bilateral symmetry.
B) a well-defined head or no head.
C) diploblastic or triploblastic embryos.
D) true tissues or no tissues.
E) a body cavity or no body cavity.

28) With the current molecular-based phylogeny in mind, rank the following from most inclusive to least inclusive.

1. ecdysozoan
2. protostome
3. eumetazoan
4. triploblastic

A) 4, 2, 3, 1
B) 4, 3, 1, 2
C) 3, 4, 1, 2
D) 3, 4, 2, 1
E) 4, 3, 2, 1

29) What does recent evidence from molecular systematics reveal about the relationship between grades and clades?
A) There is no relationship.
B) Some, but not all, grades reflect evolutionary relatedness.
C) Grades have their basis in, and flow from, clades.
D) Each branch point on a phylogenetic tree is associated with the evolution of a new grade.

30) Phylogenetic trees are best described as
A) true and inerrant statements about evolutionary relationships.
B) hypothetical portrayals of evolutionary relationships.
C) the most accurate representations possible of genetic relationships among taxa.
D) theories of evolution.
E) the closest things to absolute certainty that modern systematics can produce.

31) According to the evidence collected so far, the animal kingdom is
A) monophyletic.
B) paraphyletic.
C) polyphyletic.
D) euphyletic.
E) multiphyletic.

32) If a multicellular animal lacks true tissues, then it can properly be included among the
A) eumetazoans.
B) metazoans.
C) choanoflagellates.
D) lophotrochozoans.
E) bilateria.

33) Which of the following statements concerning animal taxonomy is (are) true?

1. Animals are more closely related to plants than to fungi.
2. All animal clades based on body plan have been found to be incorrect.
3. Kingdom Animalia is monophyletic.
4. Only animals reproduce by sexual means.
5. Animals are thought to have evolved from flagellated protists similar to modern choanoflagellates.

A) 5 only
B) 1 and 3
C) 3 and 5
D) 3, 4, and 5

34) If the current molecular evidence regarding animal origins is well-substantiated in the future, then what will be true of any contrary evidence regarding the origin of animals derived from the fossil record?
A) The contrary fossil evidence will be seen as a hoax.
B) The fossil evidence will be understood to have been incorrect because it is incomplete.
C) The fossil record will henceforth be ignored.
D) Phylogenies involving even the smallest bit of fossil evidence will need to be discarded.
E) Only phylogenies based solely on fossil evidence will need to be discarded.

35) What is true of the clade Ecdysozoa?
A) It includes all animals that molt at some time during their lives.
B) It includes all animals that undergo metamorphosis at some time during their lives.
C) It includes all animals that have body cavities known as pseudocoeloms.
D) It includes all animals with genetic similarities that are shared with no other animals.
E) It includes all animals in the former clade Protostomia that truly do have protostome development.

36) Which distinction is given more emphasis by the morphological phylogeny than by the molecular phylogeny?
A) metazoan and eumetazoan
B) radial and bilateral
C) true coelom and pseudocoelom
D) protostome and deuterostome
E) molting and lack of molting

37) The last common ancestor of all bilaterians is thought to have had four Hox genes. Most extant cnidarians have two Hox genes, except Nematostella (of β-catenin fame), which has three Hox genes. On the basis of these observations, some have proposed that the ancestral cnidarians were originally bilateral and, in stages, lost Hox genes from their genomes. If true, this would mean that
A) Radiata should be a true clade.
B) the radial symmetry of extant cnidarians is secondarily derived, rather than being an ancestral trait.
C) Hox genes play little actual role in coding for an animal's "body plan."
D) Cnidaria may someday replace Acoela as the basal bilaterians.
E) Two of the responses above are correct.

38) Which of these, if true, would support the claim that the ancestral cnidarians had bilateral symmetry?

1. Cnidarian larvae possess anterior-posterior, left-right, and dorsal-ventral aspects.
2. Cnidarians have fewer Hox genes than bilaterians.
3. All extant cnidarians, including Nematostella, are diploblastic.
4. β-catenin turns out to be essential for gastrulation in all animals in which it occurs.
5. All cnidarians are acoelomate.

A) 1 only
B) 1 and 4
C) 2 and 3
D) 2 and 4
E) 4 and 5

39) Some researchers claim that sponge genomes have homeotic genes, but no Hox genes. If true, this finding would
A) strengthen sponges' evolutionary ties to the Eumetazoa.
B) mean that sponges must no longer be classified as animals.
C) confirm the identity of sponges as "basal animals."
D) mean that extinct sponges must have been the last common ancestor of animals and fungi.
E) require sponges to be reclassified as choanoflagellates.

The previous figure shows a chart of the animal kingdom set up as a modified phylogenetic tree. Use the diagram to answer the following question.

40) Which group contains diploblastic organisms?
A) I
B) II
C) III
D) IV
E) V

The previous figure shows a chart of the animal kingdom set up as a modified phylogenetic tree. Use the diagram to answer the following question.

41) Which two groups are most clearly represented in the Ediacaran fauna?
A) I and II
B) I and III
C) II and IV
D) II and V
E) IV and V

The previous figure shows a chart of the animal kingdom set up as a modified phylogenetic tree. Use the diagram to answer the following question.

42) Which of these is the basal group of the Eumetazoa?
A) I
B) II
C) III
D) IV
E) V

The previous figure shows a chart of the animal kingdom set up as a modified phylogenetic tree. Use the diagram to answer the following question.

43) Which two groups have members that undergo ecdysis?
A) I and II
B) II and III
C) III and IV
D) III and V
E) IV and V

44) According to the phylogenies depicted in the previous pair of figures, if one were to create a taxon called Radiata that included all animal species whose members have true radial symmetry, then such a taxon would be
A) paraphyletic.
B) polyphyletic.
C) monophyletic.
D) a clade.
E) More than one of these responses are correct.

45) What is true of the deuterostomes in the molecular phylogeny (B) that is not true in the traditional phylogeny (A)?
A) Deuterostomia is a clade.
B) To maintain Deuterostomia as a clade, some phyla had to be removed from it.
C) Deuterostomia now includes the Acoela.
D) It is actually a grade, rather than a clade.
E) It diverged from the rest of the Bilateria earlier than did the Acoela.

46) In the traditional phylogeny (A), the phylum Platyhelminthes is depicted as a sister taxon to the rest of the protostome phyla, and as having diverged earlier from the lineage that led to the rest of the protostomes. In the molecular phylogeny (B), Platyhelminthes is depicted as a lophotrochozoan phylum. What probably led to this change?
A) Platyhelminthes ceased to be recognized as true protostomes.
B) The removal of the acoel flatworms (Acoela) from the Platyhelminthes allowed the remaining flatworms to be clearly tied to the Lophotrochozoa.
C) All Platyhelminthes must have a well-developed lophophore as their feeding apparatus.
D) Platyhelminthes' close genetic ties to the arthropods became clear as their Hox gene sequences were studied.

Placozoan evolutionary relationships to other animals are currently unclear, and different phylogenies can be created, depending on the character used to infer relatedness. Sponges have no tissues, but about 20 cell types. Tp (Trichoplax adhaerens) produces a neuropeptide almost identical to one found in cnidarians. The genome of Tp, though the smallest of any known animal, shares many features of complex eumetazoan (even human!) genomes. The next three questions refer to the phylogenetic trees that follow.

47) Which phylogeny has been created by emphasizing genomic features of placozoans?
A) I
B) II
C) III

Placozoan evolutionary relationships to other animals are currently unclear, and different phylogenies can be created, depending on the character used to infer relatedness. Sponges have no tissues, but about 20 cell types. Tp (Trichoplax adhaerens) produces a neuropeptide almost identical to one found in cnidarians. The genome of Tp, though the smallest of any known animal, shares many features of complex eumetazoan (even human!) genomes. The next three questions refer to the phylogenetic trees that follow.

48) Which phylogeny has been created by emphasizing the structural simplicity of placozoans?
A) I
B) II
C) III

Placozoan evolutionary relationships to other animals are currently unclear, and different phylogenies can be created, depending on the character used to infer relatedness. Sponges have no tissues, but about 20 cell types. Tp (Trichoplax adhaerens) produces a neuropeptide almost identical to one found in cnidarians. The genome of Tp, though the smallest of any known animal, shares many features of complex eumetazoan (even human!) genomes. The next three questions refer to the phylogenetic trees that follow.

49) Which phylogeny has been created by emphasizing a protein found in placozoans?
A) I
B) II
C) III

50) Cycliophorans have two types of larvae. One type of larvathe Prometheus larvadevelops into a male. The male, which lacks a digestive system, attaches to the outside of a feeding stage (a female) and impregnates her digestive system, which develops into a different type of larva. What must be true of the digestive system of the feeding-stage female while she is still a virgin?

1. At least some of its cells are haploid.
2. It consists only of highly specialized cells.
3. It is the same size as the male.

A) 1 only
B) 2 only
C) 3 only
D) 1 and 3
E) 2 and 3

Trichoplax adhaerens (Tp) is the only living species in the phylum Placozoa. Individuals are about 1 mm wide and only 27 μm high, are irregularly shaped, and consist of a total of about 2,000 cells, which are diploid (2n = 12). There are four types of cells, none of which are nerve or muscle cells, and none of which have cell walls. They move using cilia, and any "edge" can lead. Tp feeds on marine microbes, mostly unicellular green algae, by crawling atop the algae and trapping it between its ventral surface and the substrate. Enzymes are then secreted onto the algae, and the resulting nutrients are absorbed. Tp sperm cells have never been observed, nor have embryos past the 64-cell (blastula) stage.

51) If Tp sperm are observed by future researchers, how many chromosomes should be found in a Tp sperm nucleus?
A) 2
B) 3
C) 6
D) 12

Trichoplax adhaerens (Tp) is the only living species in the phylum Placozoa. Individuals are about 1 mm wide and only 27 μm high, are irregularly shaped, and consist of a total of about 2,000 cells, which are diploid (2n = 12). There are four types of cells, none of which are nerve or muscle cells, and none of which have cell walls. They move using cilia, and any "edge" can lead. Tp feeds on marine microbes, mostly unicellular green algae, by crawling atop the algae and trapping it between its ventral surface and the substrate. Enzymes are then secreted onto the algae, and the resulting nutrients are absorbed. Tp sperm cells have never been observed, nor have embryos past the 64-cell (blastula) stage.

52) In how many of the following ways is Tp unlike the typical animal?

1. Tp is multicellular.
2. Tp lacks muscle and nerve cells.
3. Tp has cilia.
4. Tp has a different place where digestion of food occurs.
5. Tp lacks cell walls.

A) only one way
B) two ways
C) three ways
D) four ways
E) all five ways

Trichoplax adhaerens (Tp) is the only living species in the phylum Placozoa. Individuals are about 1 mm wide and only 27 μm high, are irregularly shaped, and consist of a total of about 2,000 cells, which are diploid (2n = 12). There are four types of cells, none of which are nerve or muscle cells, and none of which have cell walls. They move using cilia, and any "edge" can lead. Tp feeds on marine microbes, mostly unicellular green algae, by crawling atop the algae and trapping it between its ventral surface and the substrate. Enzymes are then secreted onto the algae, and the resulting nutrients are absorbed. Tp sperm cells have never been observed, nor have embryos past the 64-cell (blastula) stage.

53) On the basis of information in the previous paragraph, which of these should be able to be observed in Tp?
A) the act of fertilization
B) the process of gastrulation
C) eggs
D) All three of the responses above are correct.
E) Two of the responses above are correct.

Trichoplax adhaerens (Tp) is the only living species in the phylum Placozoa. Individuals are about 1 mm wide and only 27 μm high, are irregularly shaped, and consist of a total of about 2,000 cells, which are diploid (2n = 12). There are four types of cells, none of which are nerve or muscle cells, and none of which have cell walls. They move using cilia, and any "edge" can lead. Tp feeds on marine microbes, mostly unicellular green algae, by crawling atop the algae and trapping it between its ventral surface and the substrate. Enzymes are then secreted onto the algae, and the resulting nutrients are absorbed. Tp sperm cells have never been observed, nor have embryos past the 64-cell (blastula) stage.

54) In its native environment, a Tp cell neither gains nor loses water. What should one expect to occur when Tp is placed into fresh water?
A) no change from the above, as fresh water is its native environment
B) lysis
C) plasmolysis
D) slight shrinkage

Trichoplax adhaerens (Tp) is the only living species in the phylum Placozoa. Individuals are about 1 mm wide and only 27 μm high, are irregularly shaped, and consist of a total of about 2,000 cells, which are diploid (2n = 12). There are four types of cells, none of which are nerve or muscle cells, and none of which have cell walls. They move using cilia, and any "edge" can lead. Tp feeds on marine microbes, mostly unicellular green algae, by crawling atop the algae and trapping it between its ventral surface and the substrate. Enzymes are then secreted onto the algae, and the resulting nutrients are absorbed. Tp sperm cells have never been observed, nor have embryos past the 64-cell (blastula) stage.

55) Tp's body symmetry seems to be most like that of
A) most sponges.
B) cnidarians.
C) worms.
D) tetrapods.
E) Two of the responses above are correct.

Trichoplax adhaerens (Tp) is the only living species in the phylum Placozoa. Individuals are about 1 mm wide and only 27 μm high, are irregularly shaped, and consist of a total of about 2,000 cells, which are diploid (2n = 12). There are four types of cells, none of which are nerve or muscle cells, and none of which have cell walls. They move using cilia, and any "edge" can lead. Tp feeds on marine microbes, mostly unicellular green algae, by crawling atop the algae and trapping it between its ventral surface and the substrate. Enzymes are then secreted onto the algae, and the resulting nutrients are absorbed. Tp sperm cells have never been observed, nor have embryos past the 64-cell (blastula) stage.

56) In an experiment, several Tp individuals were stained different colors. The stained individuals were then passed through a strainer, disaggregated to the level of single cells, and collected into a common container of seawater. Which subsequent finding would be most surprising if the Tp individuals used in this experiment had been produced by sexual, rather than asexual, means?
A) If all of the cells from a given individual reaggregated to form the same individual, and if each cell had retained its original identity, as far as cell type goes.
B) If all of the cells from a given individual reaggregated to form the same individual, but if each cell had a different identity than it had before disaggregation.
C) If cells from different original individuals reaggregated together to form new individual organisms.
D) If cells from different original individuals reaggregated together to form new species.

A student encounters an animal embryo at the eight-cell stage. The four smaller cells that comprise one hemisphere of the embryo seem to be rotated 45 degrees and to lie in the grooves between larger, underlying cells (i.e., spiral cleavage).

57) This embryo may potentially develop into a(n)
A) turtle.
B) earthworm.
C) sea star.
D) fish.
E) sea urchin.

A student encounters an animal embryo at the eight-cell stage. The four smaller cells that comprise one hemisphere of the embryo seem to be rotated 45 degrees and to lie in the grooves between larger, underlying cells (i.e., spiral cleavage).

58) If we were to separate these eight cells and attempt to culture them individually, then what is most likely to happen?
A) All eight cells will die immediately.
B) Each cell may continue development, but only into a nonviable embryo that lacks many parts.
C) Each cell may develop into a full-sized, normal embryo.
D) Each cell may develop into a smaller-than-average, but otherwise normal, embryo.

The most recently discovered phylum in the animal kingdom (1995) is the phylum Cycliophora. It includes three species of tiny organisms that live in large numbers on the outsides of the mouthparts and appendages of lobsters. The feeding stage permanently attaches to the lobster via an adhesive disk, and collects scraps of food from its host's feeding by capturing the scraps in a current created by a ring of cilia. The body is sac-like and has a U-shaped intestine that brings the anus close to the mouth. Cycliophorans are eucoelomate, do not molt (though their host does), and their embryos undergo spiral cleavage.

59) Which of these features is least useful in assigning the phylum Cycliophora to a clade of animals?
A) having a true coelom as a body cavity
B) having a body symmetry that permits a U-shaped intestine
C) having embryos with spiral cleavage
D) lacking ecdysis (molting)

The most recently discovered phylum in the animal kingdom (1995) is the phylum Cycliophora. It includes three species of tiny organisms that live in large numbers on the outsides of the mouthparts and appendages of lobsters. The feeding stage permanently attaches to the lobster via an adhesive disk, and collects scraps of food from its host's feeding by capturing the scraps in a current created by a ring of cilia. The body is sac-like and has a U-shaped intestine that brings the anus close to the mouth. Cycliophorans are eucoelomate, do not molt (though their host does), and their embryos undergo spiral cleavage.

60) Basing your inferences on information in the previous paragraph, to which clade(s) should cycliophorans belong?

1. Eumetazoa
2. Deuterostomia
3. Bilateria
4. Ecdysozoa
5. Lophotrochozoa

A) 1 only
B) 1 and 3
C) 1, 3, and 5
D) 2, 3, and 4
E) 2, 3, and 5

The most recently discovered phylum in the animal kingdom (1995) is the phylum Cycliophora. It includes three species of tiny organisms that live in large numbers on the outsides of the mouthparts and appendages of lobsters. The feeding stage permanently attaches to the lobster via an adhesive disk, and collects scraps of food from its host's feeding by capturing the scraps in a current created by a ring of cilia. The body is sac-like and has a U-shaped intestine that brings the anus close to the mouth. Cycliophorans are eucoelomate, do not molt (though their host does), and their embryos undergo spiral cleavage.

61) If harboring large populations of cycliophorans neither helps nor harms their lobster hosts, then cycliophorans can be properly considered to be

1. parasites.
2. mutualists.
3. commensals.
4. symbionts.
5. endosymbionts.

A) 1 and 4
B) 2 and 4
C) 3 and 4
D) 2 and 5
E) 3 and 5

The most recently discovered phylum in the animal kingdom (1995) is the phylum Cycliophora. It includes three species of tiny organisms that live in large numbers on the outsides of the mouthparts and appendages of lobsters. The feeding stage permanently attaches to the lobster via an adhesive disk, and collects scraps of food from its host's feeding by capturing the scraps in a current created by a ring of cilia. The body is sac-like and has a U-shaped intestine that brings the anus close to the mouth. Cycliophorans are eucoelomate, do not molt (though their host does), and their embryos undergo spiral cleavage.

62) On the basis of the cleavage pattern of cycliophoran embryos, which of these should be true?
A) It has determinate development.
B) The blastopore becomes the anus.
C) They are deuterostomes.
D) A cell separated from a four-cell embryo should develop into a complete organism.

The most recently discovered phylum in the animal kingdom (1995) is the phylum Cycliophora. It includes three species of tiny organisms that live in large numbers on the outsides of the mouthparts and appendages of lobsters. The feeding stage permanently attaches to the lobster via an adhesive disk, and collects scraps of food from its host's feeding by capturing the scraps in a current created by a ring of cilia. The body is sac-like and has a U-shaped intestine that brings the anus close to the mouth. Cycliophorans are eucoelomate, do not molt (though their host does), and their embryos undergo spiral cleavage.

63) Using similarities in embryonic development, body symmetry, and other anatomical features to assign an organism to a clade involves

1. cladistics based on body plan.
2. molecular-based phylogeny.
3. morphology-based phylogeny.

A) 1 only
B) 2 only
C) 3 only
D) 1 and 2
E) 1 and 3

The most recently discovered phylum in the animal kingdom (1995) is the phylum Cycliophora. It includes three species of tiny organisms that live in large numbers on the outsides of the mouthparts and appendages of lobsters. The feeding stage permanently attaches to the lobster via an adhesive disk, and collects scraps of food from its host's feeding by capturing the scraps in a current created by a ring of cilia. The body is sac-like and has a U-shaped intestine that brings the anus close to the mouth. Cycliophorans are eucoelomate, do not molt (though their host does), and their embryos undergo spiral cleavage.

64) Which of these, if discovered among cycliophorans, would cause the most confusion concerning our current understanding of cycliophoran taxonomy?
A) if the ciliated feeding ring is a lophophore
B) if embryos are diploblastic
C) if the body cavity is actually a pseudocoelom
D) if the organisms show little apparent cephalization

The most recently discovered phylum in the animal kingdom (1995) is the phylum Cycliophora. It includes three species of tiny organisms that live in large numbers on the outsides of the mouthparts and appendages of lobsters. The feeding stage permanently attaches to the lobster via an adhesive disk, and collects scraps of food from its host's feeding by capturing the scraps in a current created by a ring of cilia. The body is sac-like and has a U-shaped intestine that brings the anus close to the mouth. Cycliophorans are eucoelomate, do not molt (though their host does), and their embryos undergo spiral cleavage.

65) What is true of the feeding stage of cycliophorans?

1. It is chemoheterotrophic.
2. It is sessile.
3. It captures food in a manner similar to that of animals with lophophores.
4. It has radial symmetry.

A) 1 and 2
B) 1 and 3
C) 2 and 4
D) 1, 2, and 3
E) 2, 3, and 4

The most recently discovered phylum in the animal kingdom (1995) is the phylum Cycliophora. It includes three species of tiny organisms that live in large numbers on the outsides of the mouthparts and appendages of lobsters. The feeding stage permanently attaches to the lobster via an adhesive disk, and collects scraps of food from its host's feeding by capturing the scraps in a current created by a ring of cilia. The body is sac-like and has a U-shaped intestine that brings the anus close to the mouth. Cycliophorans are eucoelomate, do not molt (though their host does), and their embryos undergo spiral cleavage.

66) Cycliophorans have two types of larvae. One type of larva is produced when the digestive system of a female is impregnated by a male. The digestive system then collapses and develops into a larva, which swims away in search of a new host after the surrounding female dies. Which is the embryonic tissue that is apparently most important in forming this type of larva?
A) mesohyl
B) mesoderm
C) ectoderm
D) endoderm
E) mesoglea

67) What conclusion is apparent from the data in the table?
A) Land animals have more Hox genes than do those that live in water.
B) All bilaterian phyla have had the same degree of expansion in their numbers of Hox genes.
C) Acoel flatworms should be expected to contain seven Hox genes.
D) The expansion in number of Hox genes throughout vertebrate evolution cannot be explained merely by three duplications of the ancestral vertebrate Hox cluster.
E) Extant insects all have seven Hox genes.

68) All things being equal, which of these is the most parsimonious explanation for the change in the number of Hox genes from the last common ancestor of insects and vertebrates to ancestral vertebrates, as shown in the table?
A) The occurrence of seven independent duplications of individual Hox genes.
B) The occurrence of two distinct duplications of the entire seven-gene cluster, followed by the loss of one cluster.
C) The occurrence of a single duplication of the entire seven-gene cluster.

69) Two competing hypotheses to account for the increase in the number of Hox genes from the last common ancestor of bilaterians to the last common ancestor of insects and vertebrates are: (1) a single duplication of the entire four-gene cluster, followed by the loss of one gene, and (2) three independent duplications of individual Hox genes. To prefer the first hypothesis on the basis of parsimony requires the assumption that
A) the duplication of a cluster of four Hox genes is equally likely as the duplication of a single Hox gene.
B) there is an actual process by which individual genes can be duplicated.
C) genes can exist is spatial groupings called clusters.
D) clusters of genes can undergo disruption, with individual genes moving to different chromosomes during evolution.


Deep phylogeny, ancestral groups and the four ages of life

Organismal phylogeny depends on cell division, stasis, mutational divergence, cell mergers (by sex or symbiogenesis), lateral gene transfer and death. The tree of life is a useful metaphor for organismal genealogical history provided we recognize that branches sometimes fuse. Hennigian cladistics emphasizes only lineage splitting, ignoring most other major phylogenetic processes. Though methodologically useful it has been conceptually confusing and harmed taxonomy, especially in mistakenly opposing ancestral (paraphyletic) taxa. The history of life involved about 10 really major innovations in cell structure. In membrane topology, there were five successive kinds of cell: (i) negibacteria, with two bounding membranes, (ii) unibacteria, with one bounding and no internal membranes, (iii) eukaryotes with endomembranes and mitochondria, (iv) plants with chloroplasts and (v) finally, chromists with plastids inside the rough endoplasmic reticulum. Membrane chemistry divides negibacteria into the more advanced Glycobacteria (e.g. Cyanobacteria and Proteobacteria) with outer membrane lipolysaccharide and primitive Eobacteria without lipopolysaccharide (deserving intenser study). It also divides unibacteria into posibacteria, ancestors of eukaryotes, and archaebacteria—the sisters (not ancestors) of eukaryotes and the youngest bacterial phylum. Anaerobic eobacteria, oxygenic cyanobacteria, desiccation-resistant posibacteria and finally neomura (eukaryotes plus archaebacteria) successively transformed Earth. Accidents and organizational constraints are as important as adaptiveness in body plan evolution.

1. Introduction

The nature of the deepest branches in the evolutionary tree and the last common ancestor of all life are key questions in biology having wide ramifications. Currently, we are in the early stages of a paradigm shift in which the prevailing view on these matters should be replaced by a sounder one. This review summarizes recent insights into bacterial and protozoan large-scale evolution and the tree of life for non-specialists and argues that much more intense research into the little-known phylum Chlorobacteria is needed for better understanding the nature of our last common ancestor. To avoid burdening you with excessive detail, I do this rather briefly in the second half of this essay, giving references to specialist literature for those wanting more detail or evidence for my conclusions.

The first half is a broader historical/philosophical discussion of the contrast between ancestral and derived groups and how taxonomists should handle them. The past three decades have seen a dramatic increase in the use of DNA sequences for reconstructing phylogeny and a parallel shift in emphasis from evolutionary taxonomy (Mayr 1974) towards Hennig's (1966) ‘phylogenetic systematics’, often accompanied by much controversy. Great advances in knowledge and understanding of organismal history have been made, but some fashions, attitudes and dogmas have spread more widely and dominated other viewpoints more than their scientific merits justify. The significance of the stasis of ancestral body plans over billenia and the non-uniformity of evolutionary modes and rates is insufficiently appreciated. Much discussion has been among students of recently derived branches of the tree (Hennig insects Mayr birds) or among those whose focus is biochemistry or computer algorithms, rather than organisms and the needs and principles of taxonomy. I offer the perspective of a biologist especially interested in unicellular organisms, ancestral groups and in explaining the major transitions of life, perhaps more conscious than most of flaws in some aspects of recent phylogenetic fashions.

Soon after it was founded, the Royal Society published Micrographia in which Hooke (1664) applied the word cell for the first time to the walled units of dead plant tissues that he first depicted. However, the modern concept of cells as living units that multiply by division grew up only in the mid nineteenth century simultaneously with that of evolution by variation and selection. Weismann (1889) made the first synthesis of cell biology and evolution, in which cell lineages were seen as the physical basis for inheritance and evolution, but his emphasis was all on nucleated cells, as was Wallace's (1911) claim that only a creative mind could have made them. Understanding the big picture of organismal history requires more attention than hitherto to the main features of the evolution of sexless bacterial cells which exclusively dominated the biosphere for three-quarters of its history. More than all eukaryotes together, bacteria still largely manipulate biogeochemical cycles and global climate.

Though I shall not dwell on it, another limitation of Weismann's synthesis has become apparent in the past two decades. Superimposed on the vertical inheritance of cell lineages that Weismann recognized is the horizontal transfer of individual genes or small clusters of genes among organisms of separate cell lineages, which can affect the evolution of extremely distantly related organisms. In bacteria, such lateral gene transfer (LGT) occurs mainly by viruses, plasmids or the uptake of naked DNA from dead cells. In eukaryotes, feeding by phagocytosis followed by inefficient digestion of prey DNA and its accidental incorporation into nuclear chromosomes is probably how protozoa most often get foreign genes (Doolittle 1998). Although LGT of DNA independently of cell lineages is evolutionarily important, especially among bacteria and protozoa (see Cavalier-Smith submitted a), it seems to have played no role in the evolution of the major cellular body plans that I focus on here.

2. Early perceptions of cell lineages and the unity of life

Shall we conjecture that one and the same kind of living filaments is and has been the cause of all organic life?

The nucleated vesicle, the fundamental form of all organization, we must regard as the meeting point between the inorganic and the organic—the end of the mineral and beginning of the animal and vegetable kingdoms … We have already seen that this nucleated vesicle is itself a type of mature and independent being in the infusory animalcule [now called Protozoa, following von Siebold (1845)] … The first step in the creation of life upon this planet was a chemico-electric operation, by which simple germinal vesicles were produced … What were the next steps? … an advance under favour of peculiar conditions, from the simplest forms of being to the next most complicated, and this through the ordinary process of generation.

Lamarck in French and Chambers in English first proposed phylogenetic trees for real organisms. Darwin (1859) scrupulously avoided doing that. Unmerited ridicule as they suffered would have jeopardized his threefold mission: demonstrating the fact of evolution showing how the struggle for existence explains adaptation and attempting to explain evolutionary change (transformation) by genetic variation and the differential multiplication of genotypes. When emphasizing how common ancestry plus divergence into novel phenotypes explain the striking patterns of similarity and differences that enable us to classify organisms into successively nested taxa within higher taxa, Darwin cleverly used an abstract tree immune to ridicule or phylogenetic error. He correctly argued that the body plan shared by members of a phylum was present in their last common ancestor and has been stably inherited generation after generation, with no fundamental change for hundreds of millions of years. Proceeding down the hierarchy of categories through class, order, family, genus and species, each successive subordinate group differs from its closest relatives in characters of decreasing long-term stability (Lamarck 1809).

Chambers wrote shortly after Meyen (1839), Dujardin (1841) and Barry (1843) unified biology by showing that protozoa are single nucleated cells homologous with those forming animal and plant bodies and that continuous cell lineages are the physical basis of life. (The more famous Schleiden (1838) and Schwann (1839) whom text books call ‘the’ authors of ‘cell theory’ did not realize this.) But a century elapsed before electron microscopy clarified the fundamental distinction between bacteria and nucleated (eukaryotic) cells. We now know that life did not begin with protozoa having cells like ours, as Chambers thought, but with much simpler bacterial (prokaryotic) cells. On the most conservative estimate, nucleated cells evolved only approximately 800–850 Myr ago (Cavalier-Smith 2002b, 2006a). For the first 2.6 billion years, only bacteria inhabited the world. Microscopically simple, but structurally exceedingly complex in their atomic arrangements, their fantastic diversity and biochemical ingenuity is mediated by thousands of intricate macromolecular machines whose three-dimensional structure and interactions are revealed only by X-ray crystallography. As noted above, bacterial evolution has depended only on the evolutionary divergence of cell lineages plus the horizontal transfer of DNA. The much later origin of protozoa with their sexual gamete fusion and predation by phagocytosis (Cavalier-Smith 2009b) made the merger of cell lineages a novel factor in evolution and population genetics (commonly by sex and extremely rarely by symbiogenesis of foreign engulfed cells to form organelles, like mitochondria and chloroplasts Cavalier-Smith 2000, 2006b).

3. Common ancestry, stasis and divergence in the history of life

Explaining stasis is as important as explaining change. Darwin correctly divined the key role of selection in promoting adaptation and in channelling the historical divergence of related members of a taxon. But he did not sufficiently realize its importance also in ensuring stable inheritance over billions of generations of ancestral body plans, though unlike Chambers he refused to attribute such plans ultimately to a creative mind. Only after twentieth-century understanding of the physical inevitability of mutations affecting every single nucleotide of a genome could we appreciate the fundamental significance of purifying and stabilizing selection in preserving body plans over billenia (Schmalhausen 1949). Inheritance alone is too imperfect to achieve this. About half the nucleotides in ribosomal RNA (rRNA) molecules have an identical sequence in every bacterium, animal, plant and fungus, despite every nucleotide regularly mutating, some in every generation in every species. Since you started reading this paper, at least one cell of your body will have one or more new mutations in regions of rDNA where the ancestral sequence in the last common ancestor of all life has never actually been supplanted by evolution over 3.5 billion years. The same applies to hundreds of other genes essential for life. Stasis stems from the lethality (or dramatically lower fertility) of such variants (purifying selection) and is not inherent to the genetic material. Without death, life could not persist. Contrary to what Darwin thought, and many creationists still do, the problem is less to explain how genetic variation occurs, than to understand why some organismal properties never change while others frequently do. Differential reproductive success (anthropomorphically ‘natural selection’) biases genotypes of successive generations subjected to a perpetual, physically inevitable, barrage of mutations in every part of the genome. This beautifully explains both long-term stasis and radical organismal transformation. Both stasis and change are needed to explain the patterns of similarity and difference that enable hierarchical Linnean classification.

4. The kingdoms and tree of life

Except for Lamarck's and Chambers’ ridiculed attempts and Goldfuss (1820), who introduced the name Protozoa (first in 1817) for the microscopic Infusoria that Lamarck put at the base of the animal kingdom, tracing the actual history of life in detail and explaining the origins of specific novel groups of organisms were begun in a bold and detailed way only by Darwin's contemporary and admirer Haeckel (1866). Haeckel coined the word phylogeny for the evolutionary history of a group, to contrast it with the development of an individual organism within one generation. Even Haeckel was ridiculed by some of my Cambridge zoology teachers, such was the antipathy to phylogeny among mechanistic biologists. Undiscriminating critics who attribute to him nasty social views he did not hold also unfairly denigrate his scientific genius. Haeckel made the important distinction between a group that shared ancestral characters because of their single (monophyletic) origin prior to their common ancestor (e.g. vertebrates whose last common ancestor already had a skull and vertebral column and many other features) and groupings of organisms (e.g. ‘flying animals’ or ‘parasitic plants’) that share characters that evolved several times independently, i.e. are polyphyletic.

Prior to Haeckel, organisms were generally divided into just two kingdoms: animals and vegetables, even though Necker (1783) and others later made a third kingdom for fungi, and Owen (1858) had placed unicellular organisms such as bacteria, amoebae and diatoms in a separate kingdom, Protozoa. Haeckel (1866) divided the tree of life into three branches, kingdoms Animalia, Plantae and Protista, each of which he thought arose monophyletically from the primordial slime. His kingdom Protista was heterogeneous, including heterotrophic bacteria, diatoms, amoebae and sponges later, he moved amoebae and sponges to the animal kingdom and supposed that the residual Protista and life itself were highly polyphyletic. His three-kingdom system did not catch on, as critics thought it somewhat arbitrary what he placed in each. Only in a very loose sense was it a precursor of modern multikingdom systems. He placed heterotrophic bacteria in Protista and cyanobacteria (blue-green algae) in Plantae and thus failed to appreciate the basic unity of prokaryotes (first clearly recognized, as Schizophyta, by Cohn (1875), who visited Darwin in 1876) and the fundamental difference between prokaryotes and eukaryotes. This became accepted only after electron microscopy showed their ultrastructural differences: notably the absence of nuclei, mitochondria, an endomembrane system and internal cytoskeleton in all prokaryotes—and their universal presence in eukaryotes, coupled with the totally different ultrastructure of bacterial flagella and the unrelated eukaryotic cilia/flagella and basic differences in chromosome organization and cell division machinery. Stanier was chiefly responsible for recognizing the prokaryote–eukaryote dichotomy as the most fundamental in the living world (Stanier & Van Niel 1962 Stanier et al. 1963). Recent misguided criticisms notwithstanding, this two-fold division reflects a profound evolutionary truth (Cavalier-Smith 1991a,b, 2006a, 2007b).

Acceptance of prokaryotes as a distinct kingdom followed the influential paper by Whittaker (1969) who called it Monera, based on seminal work by Copeland (1956). The name Monera is best forgotten. Haeckel invented it for mythical organisms with contractile protoplasm and no nucleus that probably never existed. All Haeckel's candidates turned out to be amoeboid protozoa where the nucleus had escaped detection by available primitive microscopes or in one instance an artifactual chemical precipitate in sea water. Naming prokaryotes Monera, as Copeland did just because they lack a nucleus, is misleading as they lack contractile cytoplasm. I use the oldest name, Bacteria, known to most laymen, for the kingdom comprising all prokaryotes, following the first proponent of bacteria as a distinct kingdom (Enderlein 1925). Contrary to Haeckel's ideas, the most primitive surviving organisms are not contractile slime blobs, but rigid bacteria. Bacteria generally have rigid cell walls, never the branching filaments of actin protein that form an internal skeleton for all eukaryote cells. Bacteria equally lack the motor protein myosin that actively moves along actin filaments, causing the contraction of muscles, movements of amoebae and slime moulds and internal movements in all eukaryote cells including those of plants and fungi that evolved cell walls secondarily—entirely independently of each other and bacteria.

The origin of actin and myosin from known bacterial precursors was central to the origin of the eukaryote cell as Stanier (1970) first suggested and I explained in detail (Cavalier-Smith 1975, 1987a, 2002b, 2009b, in press), numerous radical innovations in cell structure that made eukaryotes were tied up with the origin of predation on other cells by engulfing them by phagocytosis, an ancestral property for protozoa and animals. By contrast, no bacteria can eat other cells by engulfment, though several groups of bacteria became predators by evolving enzymes to digest prey externally, just as do some fungi and carnivorous plants.

Erasmus and Charles Darwin's fascination with insectivorous plants such as sundews and pitcher plants and with climbing plants probably stemmed from seeing them as potential missing links between the plant and animal kingdoms, offering clues how animals, classically characterized by eating and motility, might have evolved from plants. However, the evolutionary link between animals and plants is indirect, via unicellular protozoa. The carnivorous habits of certain plants and fungi arose entirely independently of those of animals, though the secretory mechanisms of their digestive enzymes evolved in their protozoan common ancestors—many of the enzymes themselves dating back still earlier to their bacterial ancestors. Although bacteria and protozoa were discovered long before, in 1675 (van Leeuwenhoek 1677), 1 the central importance of unicellular organisms for reconstructing deep phylogeny was only obvious after the lingering notion of ongoing spontaneous generation (which Barry (1843) and Leeuwenhoek denied) was more decisively rejected in the 1860s by Pasteur. This reinforced the recognition of universal cell lineage continuity in 1852 by Remak and Virchow (Baker 1953). Virchow (1859) popularized the much earlier dictum ‘omnis cellula e cellula’ more influentially in the very year, 1858, when Darwin and Wallace (1858) publicized natural selection. The later elucidation of chromosome structure, mitosis and meiosis effectively proved the monophyly of the eukaryote cell, allowing Weismann (1889) to portray multicellular organisms as lineages of adhering cells within which vertical inheritance dominated and the germ line is relatively immune from environmental influences and direct effects of use and disuse, and paved the way for proper interpretation of Mendelian ratios.

The virtual universality of the genetic code and pervasive sequence similarity of numerous genes and of central biochemical pathways in all organisms have proved the monophyly of all life. The unity of cell machinery for inserting nascent proteins directly into membranes and of key membrane proteins shows that all cells are lineal, vertical descendants of the very first cell (Cavalier-Smith 2001, 2006c), notwithstanding the dramatic structural differences between bacteria and eukaryotes or the unique membrane lipid chemistry of archaebacteria—which evolved from conventional bacteria (eubacteria) by lipid replacement, not independently from membrane-free naked-gene precursors as has sometimes been claimed. Figure 1 emphasizes that the fundamental differences between plants, animals and fungi reflect their independent origins from unicellular protozoan ancestors.

Figure 1. The six-kingdom, two-empire classification of life. Three major lineage mergers (symbiogeneses involving cell enslavement after phagocytic engulfment) are shown as dashed lines four additional mergers that transferred chloroplasts from green plants or chromists into different protist lineages to make novel kinds of algae (Cavalier-Smith 2007c) are omitted for clarity (figure 6). The ancestrally photosynthetic kingdoms (Bacteria, Plantae and Chromista) are in green, but in each many lineages have lost photosynthesis. Chloroplasts originated when a biciliate protozoan internally enslaved a cyanobacterium bounded by two membranes to become the first plant. Chloroplasts are in the cytosol in Plantae, but inside two extra membranes in most Chromista: the ex-plasma membrane of the enslaved red alga, plus an RER membrane. Photosynthetic chromists include brown seaweeds, diatoms, haptophytes and cryptomonads. To portray early evolution in more detail, one must expand the two ancestral kingdoms by subdividing them more finely, as in figures 3 and 4 for Bacteria and figures 4 and 6 for Protozoa. But showing such basal groups in a phylogenetic tree as a single paraphyletic taxon, as here, is perfectly permissible and better focuses on the major steps in progressive evolution that generated the kingdoms than would excessive subdivision into a forest of ancient branches.

Lamarck (1809) insightfully contrasted the true natural order of life (what we now call phylogeny) with all classifications of life into discrete groups, which he correctly viewed as artificial human creations for our ends. Classification's purpose is not to ‘represent genealogy’ (that is the purpose of phylogeny) but to establish named coherent groups that are sensibly distinguishable from other groups, ideally by common ancestrally shared features, in an evolutionarily sound hierarchical system (Cavalier-Smith 1998). Taxonomy necessarily involves simplification and judgement about which characters to emphasize for human comprehension of biodiversity, without overtaxing our brains by its immensity. It cannot be done by algorithms delegatable to computers or inexperienced graduate students. Phylogenetically, even ‘biological species’ are artificial, as they are not unambiguously demarcated from their ancestors—except for allopolyploids, the only taxon that arises instantaneously.

5. Grades, clades and the big picture of organismal evolution

All six kingdoms are monophyletic in Haeckel's classical sense, i.e. each arose by one major evolutionary transformation (figure 1). For the origin of plants, the transformation was the enslavement by a protozoan of a phagocytosed cyanobacterium, turning it into a chloroplast by evolving novel membrane proteins able to extract chemicals for the host's benefit and evolving a novel protein-import machinery that targets such proteins to the chloroplast (Cavalier-Smith 1982, 2000). Thus, unbeknown to Haeckel, Darwin or Weismann, the tree of life involves not only divergence of cellular lineages, but on extremely rare occasions also mergers of distantly related lineages into one evolutionarily chimaeric cell. Such cell enslavement and profound integration, called symbiogenesis by Mereschkovsky (1910) who first proposed it for chloroplasts (Mereschkovsky 1905), yields more dramatic innovation than can mutation and selection alone. Symbiogenesis is analogous to Empedocles’ almost 2500-year-old idea of evolution by chimaera formation among body parts, impossible for multicells but not for unicells of course, each symbiogenesis also involves thousands of mutations and their selection through benefiting host reproductive success. Symbiogenesis much more profoundly influenced megaevolution than did sex, which arose during the origin of eukaryotes, enabling closely related cells to fuse and pool their genetic and other resources—mainly of microevolutionary significance. Sex on the microscale and much rarer symbiogenesis reticulate cell lineages over history, making nonsense of cladistic dogma (Hennig 1966) assuming only divergence without mergers. LGT which occurs occasionally in Protozoa and plants independently of symbiogenesis (Keeling & Palmer 2008), but extremely seldom in animals because of their segregated germ line, and rather commonly in bacteria (Doolittle et al. 2003), also invalidates a purely cladistic vertical inheritance model for evolutionary history. Real evolution often ignores Germanic cladistic logic its messiness and lack of rules makes classification an art where compromise is necessary and rigid formalism harmful.

Nonetheless, the distinction between a terminal branch of the evolutionary tree (a clade), e.g. animal or fungal kingdoms, and a basal, ancestral segment of the tree, e.g. Protozoa or Bacteria (each a distinctive grade of organization, not a clade), is important, especially when discussing extinction and origin of groups. Haeckel (1868) introduced cladus as a taxonomic category just below subphylum, but Huxley (1957, 1959) gave clade the general meaning of any monophyletic branch of the evolutionary tree. He did so when contrasting the two fundamental ‘vertical’ phylogenetic processes: cladistic splitting of lineages and progressive change along a lineage (among ‘horizontal’ phylogenetic processes, only sex was then appreciated, symbiogenesis and LGT being unproven). Huxley, like Darwin and Haeckel, correctly emphasized the equal importance of splitting and progressive change for understanding phylogeny and evolutionary history. Oddly, the school of ‘phylogenetic systematics’ founded by Hennig (1966) grossly downplayed the phylogenetic importance of progressive change compared with splitting, seen by them as so all-important that many Hennigian devotees dogmatically insist that ancestral groups like Bacteria, Protozoa and Reptilia be banned. Hennig called such basal groups with a monophyletic origin ‘paraphyletic’ and redefined monophyly to exclude them and embrace only clades, likewise redefined as including all descendants of their last common ancestor. This redefinition of ‘clade’ is universally accepted, but Hennig's extremely confusing and unwise redefinition of monophyly is not. Though accepted by many, sadly probably the majority (especially the most vociferous and over self-confident, and those fearful of bullying anonymous referees, of whom I have encountered dozens mistakenly insisting without reasoned arguments that paraphyletic taxa are never permissible), it is rightly firmly rejected by evolutionary systematists who consider the classical distinction between polyphyly and paraphyly much more important than distinguishing two forms of monophyly (paraphyly and holophyly, using the precise terminology of Ashlock (1971), where holophyletic equals monophyletic sensu Hennig).

Monophyly and polyphyly were invented to clarify origins distinguishing between paraphyly and holophyly has nothing to do with the origin of a group, but with how taxonomists cut up the continuous phylogenetic tree into discrete named units. The phrase ‘paraphyletic origin’ that one sometimes sees is conceptual nonsense. This controversy is much more fundamental and broadly biologically important than a mere difference in preferred nomenclature. It reflects a pervasive difference in philosophy excluding ancestral groups from the concept of monophyly perverts Haeckel's evolutionary definition. I agree with Mayr (1974), Halstead (1978) and others that the Hennigian perspective impedes realistic scientific discussion of phylogenetic history, because of its evolutionarily unrealistic formalism based on an intellectually impoverished view of the complexities of actual phylogenies, especially its failure to come to grips with evolutionary transformation, the reality of ancestors, and not least its dogmatism.

Let me illustrate the importance of distinguishing polyphyly and paraphyly by considering the case of Fungi and Pseudofungi in relation to figure 1. Classically, oomycetes, e.g. Phytophthora infestans that caused the 1844 Irish potato famine, were considered fungi, being included in kingdom Fungi in Whittaker's (1969) five-kingdom system. We are now certain that oomycetes are actually more closely related to heterokont algae (e.g. diatoms, brown seaweeds) and belong with them in the superphylum Heterokonta within the kingdom Chromista they belong with hyphochytrids (also once wrongly considered fungi) and the phagotrophic flagellate Developayella in the heterokont phylum Pseudofungi (Cavalier-Smith & Chao 2006). Cellulose walls, often-filamentous body forms, and saprotrophic or parasitic lifestyles of oomycetes, which led to their incorrect classification as fungi, evolved entirely independently from the chitinous walls, hyphae and saprotrophy of true fungi. Oomycetes and fungi evolved independently from naked unicellular heterotrophic eukaryotes that fed by phagocytically engulfing prey. As similarities between fungi and pseudofungi are convergent and relatively superficial, a ‘fungoid’ group embracing both but not protozoa would be polyphyletic and unacceptable as a taxon. (Interestingly, a fair number of genes appear to have been laterally transferred from fungi to pseudofungi, which might have played a minor role in their convergence (Richards et al. 2006).)

In marked evolutionary contrast to the polyphyletic fungoids, the shared common features of an ancestral (paraphyletic) group like Protozoa evolved once only and were inherited continuously from a common ancestry, making their similarity much more fundamental and unified. The naked phagotrophic lifestyle and often flagellate and/or amoeboid motility of most members of kingdom Protozoa evolved once only in their last common ancestor, as part of an extremely complex set of over 60 major innovations, the most radical in the history of life (Cavalier-Smith 2009b). Thus, the evolutionary status of polyphyletic groups such as fungoids and paraphyletic ones such as protozoa differs radically recognition of the important contrast between them (figure 2) depends on correctly deducing the phenotype of common ancestors. Even fungoids ultimately had a last common ancestor (but one of non-fungoid phenotype) it so happens that it was also the common ancestor of all four derived (holophyletic) eukaryotic kingdoms and the paraphyletic subkingdom Sarcomastigota of the paraphyletic kingdom Protozoa. An analogous purely hypothetical example of shared common ancestry led Hennig (1974) to assert that there is therefore ‘no difference’ between paraphyletic and polyphyletic groups ‘in the structure of their genealogical relationships’ (figure 2a). His implication that distinguishing paraphyly and polyphyly is therefore unimportant for systematics or arbitrary does not remotely follow it merely underlines the casual neglect of actual ancestors and their phenotypes, and differing degrees of phenotypic change generally, by Hennigian cladistic philosophy. There being in these instances a shared common ancestor between a paraphyletic and a polyphyletic group does not nullify the importance of the distinction, which depends entirely on the historical phenotypes along the stems of the phylogenetic tree (figure 2), and not on the branching order. I am repeatedly irritated when indoctrinees of Hennig's narrow, biased viewpoint assert that they have shown a taxon to be ‘non-monophyletic’ (they mean non-holophyletic) this umbrella term conflates paraphyly and polyphyly—evolutionarily very different and of contrasting taxonomic implications. Polyphyletic taxa must be split into monophyletic ones a paraphyletic one already is monophyletic in phylogenetic origin and need not necessarily be abandoned or radically revised, though sometimes this is advisable if it is excessively heterogeneous. Non-monophyletic conceals information, contrary to Hennig's wish to make terminology more informative and precise.

Figure 2. Contrasts between paraphyletic (ancestral) and polyphyletic groups. (a) The special case used by Hennig (1974) to claim that there is no cladistic difference between them because both have the same common ancestor (A) and an identical ancestral branching pattern. (b) A more realistic case where the three black-circle taxa do not have the same last common ancestor as the white-circle group, but have a different last common ancestor (B) which also has a different phenotype (black square) from A and from themselves. Case (b) shows that Hennig's claim for cladistic equivalence between paraphyletic and polyphyletic taxa lacks generality and rested on a cunningly chosen exceptional example. A paraphyletic group includes its last common ancestor and a polyphyletic one does not, a key fact partially concealed by Hennig misleadingly putting the same-sized box around both groups to have correctly represented paraphyly the lower box should have included A, as it does in (b), where the obvious monophyly (single origin) of the paraphyletic white-circle taxon is much clearer than in Hennig's tendentious figure. The figure on the right also more strongly makes the point that the difference between polyphyly and paraphyly lies in the shared defining character (white circle) of the paraphyletic group having had a single origin, whereas the shared defining character of the polyphyletic group had three separate origins, i.e. a strongly contrasting phylogenetic history. Moreover, in (b) taxa 1 and 2 evolved black circleness in parallel from separate but phenotypically similar white-circle ancestors, whereas taxon 3 evolved it convergently from a cladistically and phenotypically more distinct black-square ancestor. It should be obvious that classifying white-circle taxa together is phylogenetically sound, i.e. they have a shared white-circle history, whereas classifying the black-circle ones together is unsound—being strongly contradicted by the lack of shared black-circle history. Unlike (a), (b) is a proper phylogeny with all ancestors and phenotypes shown ignoring ancestral phenotypes makes nonsense of phylogeny. Cladistic aversion to paraphyletic groups, and lumping of paraphyly and polyphyly as ‘non-monophyly’, are logically flawed and anti-evolutionary (see also Cavalier-Smith (1998) which explains that clades, grades and taxa are all useful but non-equivalent kinds of group and that all taxa need not be clades and all clades need not be taxa).

Hennig (1974) insisted that a monophyletic group must not share a last common ancestor with another monophyletic group. He would reject calling protozoa monophyletic because their last common ancestor is identical to that of Eukaryota—a silly argument because protozoa has lower rank within the more inclusive Eukaryota. Comparing equally ranked taxa, each of the five eukaryotic kingdoms has a different last common ancestor. Evolutionary classification, which I and many other taxonomists practice, recognizes the reality of ancestors and the importance in principle of classifying them thus, the last common ancestor of a monophyletic group is always included in the taxon, so every taxon corresponds with a single segment of the evolutionary tree having only one species at its base (figure 2b). One cannot emphasize too strongly that a Hennigian cladogram is not a phylogenetic tree cladograms have no ancestors, only extant species. Sequence trees are also not phylogenetic trees of organisms, being agnostic about ancestral phenotypes. Hennig (1974) and many followers condemned using degree of phenotypic difference in phylogeny and classification because there is no single objective measure of it. This stupidly throws the taxonomic baby out with the bathwater. The very reason we wish to classify organisms is their phenotypic differences, not their genealogical history. If all organisms had the same phenotype but a known genealogical history, it would be pointless to classify them by subdividing the tree into named pieces. Cladistic reasoning uses groups defined by phenotypic differences, so is just as sensitive as evolutionary taxonomy to there being no quantitative scale for them.

Do not misinterpret me as claiming that the distinction between the two types of monophyly (paraphyly and holophyly) is unimportant. For some purposes it may be, but in two situations the distinction is crucial: when discussing extinction or origins.

It is well known that discussions of group extinction must distinguish between real extinction of a holophyletic group such as trilobites, which genuinely left no descendants, and pseudoextinction of a paraphyletic group such as dinosaurs, which left descendants (birds) that differ so greatly from the ancestral group that they are not classified within it.

It is less widely appreciated that when considering origins or reconstructing ancestral characters treating a paraphyletic group as holophyletic causes even more serious misinterpretations. Most papers discussing the nature of the ancestral cell make this very mistake by treating eubacteria as holophyletic, whereas they are almost certainly paraphyletic (see §§7–9). As figure 3 indicates, eubacteria are much more structurally diverse than archaebacteria. Contrary to widespread practice, I do not treat them as a taxon—not because it would be paraphyletic, but because the contrast between cells with two bounding membranes (Negibacteria) is more fundamentally important than the differences between Posibacteria and Archaebacteria, derived phyla which I have grouped as subkingdom Unibacteria (Cavalier-Smith 1998). Lumping all three eubacterial groups of figure 3 as one taxon conceals the profound importance of their structural differences wrongly treating it as holophyletic makes it impossible to reconstruct the last common ancestor of life correctly. Most biologists since Iwabe et al. (1989) and Gogarten et al. (1989) have assumed that the root of the tree lies between neomura and eubacteria, but there is no sound evidence for this more protein paralogue trees place the root within eubacteria, as in figure 3, than between eubacteria and neomura (making paralogue rooting self-contradictory and unreliable despite its attractions in theory: Cavalier-Smith 2006c). Arguments based on cell evolution and the fossil record strongly indicate that eubacteria are ancestral to neomura and thus paraphyletic (Cavalier-Smith 2006a,b). By failing to recognize this, most who discuss the last common ancestor of all life have reached entirely incorrect conclusions about its nature and do not even realize the necessity of deciding where the root of the tree really is within the immensely diverse eubacteria before deducing the ancestral phenotype. This error vitiates the conclusions of hundreds of papers. It also misled a generation of researchers into thinking that studying archaebacteria is especially relevant to the origin of life, which is not so if eubacteria really are paraphyletic.

Figure 3. The tree of life, emphasizing major evolutionary changes in membrane topology and chemistry. The most basic distinction is between ancestral Negibacteria, with a cell envelope of two distinct lipid bilayer membranes, and derived unimembrana, with but one surface membrane. Negibacteria were ancestrally photosynthetic (green), while unimembrana were ancestrally heterotrophs. A photosystem duplication enabled oxygenic photosynthesis (approx. 2.5 Gy ago: Kopp et al. 2005 Kirschvink & Kopp 2008) roughly when the outer membrane (OM) dating from the first cell acquired novel impermeable lipopolysaccharide and transport machinery. The late date of the neomuran revolution involving 20 major novelties is based on morphological fossils of eukaryotes and the argument that archaebacteria cannot be substantially older than their eukaryote sisters (Cavalier-Smith 2006a,c). Eubacteria, characterized ancestrally by cell wall murein, is an ancestral paraphyletic group that I do not make a taxon because I rather subdivide bacteria into subkingdoms Negibacteria and Unibacteria (comprising the phyla Posibacteria and Archaebacteria figure 6), as their differences in membrane topology are more fundamental and significant (and more rarely change) than wall chemistry. Neomura is an important named clade that I chose not to make a taxon to avoid conflict with the much more radical differences between bacteria and eukaryotes. This exemplifies the principle that taxonomists should (and generally do) choose points on the continuous phylogenetic tree of maximal phenotypic disparity for artificially cutting it into taxa—NOT points of greatest cladistic depth irrespective of phenotype. Taxa have an initial capital grades and clades that are not taxa have lower-case initials. Previously, hydrocarbon biomarkers were misinterpreted to give much earlier dates for eukaryotes and cyanobacteria, but these are invalidated by isotopic proof of hydrocarbon mobility from much younger strata (Rasmussen et al. 2008). Justification for the topology of this tree and its being correctly rooted and thus historically correct is elsewhere (Cavalier-Smith 2006a,c Valas & Bourne 2009). A widespread contrary view that the root is between eubacteria and neomura stems from protein paralogue trees with long-branch topological artifacts and ignoring palaeontological evidence that negibacteria are immensely older than eukaryotes. For simplicity, the fact that the nucleus (N) has a double envelope that is part of a pervasive endomembrane system is not shown. The ancestral eukaryote is shown with a single cilium and centriole, but both had probably doubled in number prior to the earliest divergence among extant eukaryotes (Cavalier-Smith submitted b).

To avoid such misinterpretation of paraphyletic groups, we need not abolish them it is sufficient to flag them as paraphyletic (if we know that) and to teach biologists to use phylogenies directly, not classifications, for evolutionary reasoning about origins and extinction.

6. Evolutionists must be allowed to classify, rank and discuss ancestral groups

The amount of modification which the different groups have undergone has to be expressed by ranking them under different so-called genera, subfamilies, families, sections, orders and classes.

The evolutionary unreality of Hennig's antipathy to ancestral taxa is highlighted by allopolyploidy, by the nature of bacteria and by symbiogenesis.

Allopolyploidy involves lineage fusion that is beyond the scope of cladistics, which unrealistically assumes only divergence. The view of Linnaeus and Erasmus Darwin (1794, p. 507) that most species arose by hybridization is wrong. Yet allopolyploidy is common, especially in flowering plants two historically distinct species (sometimes from different genera) hybridize and the typically sterile hybrid becomes fertile by ploidy doubling. The resulting allopolyploid is an instantaneously evolved new species of novel phenotype, unable to breed with either parent. Several cases have been observed in nature (e.g. Spartina anglica, Primula kewensis Haldane 1932 Baumel et al. 2001 Salmon et al. 2005), proving that species sometimes evolve just as Linnaeus and Lamarck thought. Both parent species generally survive and are unchanged by the origin of the third new species, which invalidates the biologically nonsensical cladistic dogma that a sister group to a new species must be considered a different species from its parent even if phenotypically identical. Moreover, both ancestral species are valid taxa, despite being paraphyletic typically, each has at least some derived characters not shared by their descendant holophyletic allopolyploid species. Thus another spurious justification of antipathy to paraphyletic taxa is mistaken, i.e. that they have no characters not also shared by their derivatives.

The falsity of this dogma is still more strikingly shown by the kingdom Bacteria, which has several universal positive characters never found in eukaryotes, their descendants. This came about because the drastic nature of eukaryogenesis destroyed many bacterial synapomorphies that arose in the last common ancestral bacterium (Cavalier-Smith 1981, 1991a, 2009b, in press). This is often not so many paraphyletic groups lack obvious ancestral characters not shared with any descendant group. Thus, when fungi and oomycetes evolved, ancestral protozoan phagotrophy was lost through the origins of their cell walls, but when chromists evolved phagocytosis was not lost, the cells remaining naked. Instead, a key event in the origin of Chromista was the fusion of the phagocytic vacuole membrane containing the enslaved red alga with the nuclear envelope, placing it and its plastid ever afterwards inside the rough endoplasmic reticulum (RER), giving plastid-bearing chromists a cell membrane topology fundamentally different from both of their ancestral groups: Plantae and Protozoa (Cavalier-Smith 1986, 2003, 2007c). The ancestral chromist was a mixotroph it photosynthesized and phagocytosed prey, as several groups of naked chromistan algae still do (e.g. many chrysophytes, haptophytes and pedinellids) placing them outside the familiar animal–plant dichotomy. But other chromistan algae evolved cell walls (e.g. brown algal cellulose walls and diatom silica shells), dispensing with phagotrophy and becoming purely phototrophs. Other chromists abandoned photosynthesis, relying either on their ancestral phagotrophy (becoming phenotypically confusable with protozoa: zooflagellates, e.g. the heterokonts Developayella, Cafeteria and many Cercozoa the giant pseudopodial ‘heliozoan’ Actinosphaerium the whole infrakingdom Rhizaria ancestrally characterized by net-like pseudopodia and the centrohelid heliozoa see Cavalier-Smith submitted b) or on saprotrophy like oomycetes or Blastocystis, a walled anaerobic human gut parasite (confusable with fungi Cavalier-Smith & Chao 2006). Thus, chromist evolution was messy because of multiple independent losses of ancestral characters. For generations, this concealed their unity and distinctiveness from Protozoa and Plantae.

Naming Hennigian formalism ‘phylogenetic systematics’ was extremely misleading, as it focuses on only one of the two vertical processes of evolution (splitting), ignoring and contradicted by all three modes of horizontal evolution that make the true universal phylogeny a reticulating net, not an ever diverging tree (sex/allopolyploidy, symbiogenesis and LGT) if we remember that branches of real trees sometimes fuse, tree metaphors are useful.

I agree with cladists’ criticisms that Simpson's (1961) redefinition of classical monophyly was bad. His criterion that descent of a group from ‘one immediately ancestral taxon of the same or lower rank’ suffices for monophyly is far too loose. Such woolliness would allow animals and plants to be classified together in a supposedly ‘monophyletic’ kingdom merely because both evolved from Protozoa, despite their evident independent origin from two entirely separate groups of protozoa, or grouping birds and mammals because they evolved from reptiles. Though neither Simpson nor any sensible taxonomist would do either, the defence of Simpson by Mayr & Ashlock (1991) was illogical and counterproductive. Much more precision is needed, attainable by insisting that monophyly requires descent from a single ancestral species itself classified within the group in question as its first species (Mayr & Ashlock 1991), as classical taxonomists did long before Hennig (Mayr 1942). Simpson was probably led into that woolliness by problems in applying synapomorphies for extant mammals (hair, lactation and penis) to fossils and substituting a surrogate definition based on ear ossicle evolution that exhibits parallelism within reptiles. With respect to reptiles, Hennig (1974) accepted that many would regard his antipathy to Reptilia being a taxon as ‘shocking and absurd’ he even wrote with respect to the great magnitude of the differences between birds and mammals and their ancestral reptiles, the reason for treating each as distinct classes, that ‘it seems pure formalism, and perfectionism transcending any reasonable purpose to neglect these facts in a hierarchical system’. Well said. I would change ‘seems’ to ‘is’.

Recognizing paraphyletic groups like bacteria and protozoa facilitates evolutionary discussion of how major groups arose from an ancestral group and of major advances in evolution such as the origin of eukaryotes from bacterial ancestors. If we are not allowed to classify and name ancestral groups, rational discussion of such evolutionary advances is severely hampered. Cladism deals only with sister relations, but evolution and phylogeny require analysis of ancestor descendent relationships, which is greatly impeded by the straitjacket of an exclusively cladistic perspective. Its linguistic and conceptual harmfulness is illustrated by the recent fashion among cladists to reclassify tetrapods, including themselves, as Osteichthyes—bony fish. It would be impossible to express the truth that tetrapods evolved from a bony fish if we call tetrapods bony fish moreover, to call birds or elephants bony fish is stupid such is the reductio ad absurdum of Hennigian nomenclatural dicta by some cladists. A cladist actually asserted at a meeting that ‘trees and humans are flagellates’—just because both ultimately descended from flagellate protozoa. Such quirky attitudes make discussion of real phylogeny impossible. If the name of an ancestral group should expand to embrace all descendant clades, the logical conclusion would be to make all organisms bacteria, all eukaryotes protozoa and (should sponges be confirmed as paraphyletic) all animals sponges logically consistent cladists of that sort must accept that they are bacteria. If not, they should accept that such nomenclatural dogmas are deeply flawed, harmful to biology and abandon them forthwith. A philosophy that evades the reality of ancestors and denies the validity of ancestral groups is wrongly called ‘phylogenetic systematics’.

The reality of stasis and rarity of major transitions make it imperative to name ancestral groups for sensibly discussing progressive evolution. Showing decisively that pennate diatoms evolved from centric diatoms by changing cell symmetry and evolving a sternum was an important evolutionary advance (Mann & Evans 2007), not a taxonomic problem as myopic cladists misrepresent it (Williams 2007). There is no need whatever to abandon centric diatoms as a taxon because it is paraphyletic it had a single origin and has an unambiguously definable phenotype not shared by any pennates. The idea that evolutionists and taxonomists must express relationships only in terms of sister groups, never parent or descendant groups, is most harmful. Citing Darwin to support a thesis does not prove it right (like everyone he made mistakes), but he undeniably accepted ancestral groups. His famous Origin diagram was a proper phylogenetic tree with labelled ancestors, some explicitly called parent genera, not a cladogram. He would surely consider banning paraphyletic taxa an absurd impediment to evolutionary discussion and comprehensive classifications that include fossils and ancestors (Cavalier-Smith 1998).

7. The four major kinds of bacteria

For the layman and lower schoolchild, six kingdoms are sufficient to summarize the diversity and history of life in a readily graspable manner (figure 1). For a biologist interested in deep phylogeny, each kingdom must be subdivided. Consider first Bacteria, where even a non-microbiologist wishing to understand early evolution of life only in relatively broad terms ought to appreciate the fundamental differences between four major types of cell (figure 3). Bacteria comprise two subkingdoms of contrasting membrane topology: Unibacteria and Negibacteria (figure 3).

Unibacteria have one surface membrane, like eukaryote cells that evolved from them they comprise two phyla with radically different membrane chemistry: the ancestral Posibacteria and the derived Archaebacteria. Posibacteria have essentially the same membrane chemistry as eukaryotes: phospholipids with a glycerol backbone and two fatty acids attached by ester links (i.e. acyl ester lipids). Archaebacteria are sisters to eukaryotes (Cavalier-Smith 1987a, 2002a, 2006c Yutin et al. 2008), not as often incorrectly thought their ancestors (Van Valen & Maiorana 1980 a recent paper favouring an ancestral rather than a sister relationship (Cox et al. 2008) is unconvincing, as within eukaryotes the topology of all their trees is wrong in half a dozen ‘statistically well-supported’ respects, indicating that the data and methods fail to reconstruct trees accurately for these branches, making it unwise to accept that the reported sister relationship between eukaryotes and crenarchaeotes is less suspect than these known errors). Unlike eubacteria and eukaryotes, archaebacteria make their membranes of glycerol phospholipids in which isoprenoids are attached by ether links to the glycerol backbone, which also has a novel stereochemistry. These novel lipids arguably arose to enable hyperthermophily—tolerating extremely high temperatures, sometimes over 100°C, when the ancestral archaebacterium replaced acyl esters by stabler isoprenoid ethers (Cavalier-Smith 1987a,b, 2002a, 2006c). This replacement enabled covalent bonds to link phospholipids in the two leaflets of the cytoplasmic membrane into a single layer, enabling these specialized bacteria to colonize the highest temperature habitats available on Earth in geothermally active areas. This specialization arguably also involved loss of many ancestral enzymes unable to cope with such extremes and to a greatly reduced genome size of archaebacteria compared with their posibacterial ancestors and eukaryotic sisters (Cavalier-Smith 2002b, 2007a). Later, some archaebacterial lineages, notably halobacteria, colonized similarly previously unexploited but lower temperature habitats, reacquiring many enzymes suitable for mesophilic habitats by LGT from eubacteria and making their membranes more fluid by losing covalent bonding between the bilayers (Cavalier-Smith 2002b). No unibacteria are photosynthetic fixers of carbon dioxide. None contain chlorophyll, though some halobacteria use sunlight trapped by carotenoids related to visual purple of animal retinas to make ATP.

Negibacteria, in marked contrast, are bounded by two membranes and are often photosynthetic, five different phyla containing members able to fix carbon dioxide using energy trapped by chlorophyll (Cyanobacteria typically generating oxygen) or bacteriochlorophyll (Chlorobacteria, Sphingobacteria, Proteobacteria, Eurybacteria all anoxygenic—never generating oxygen). Their inner bounding membrane is homologous with and ancestral to the bounding membrane of unibacteria and eukaryotes, having typical acyl ester phospholipids (except in Chlorobacteria) as in eukaryotes and Posibacteria and related membrane proteins. Their outer membrane (OM) has more variable chemistry, the basis for classification into two infrakingdoms: Eobacteria and Glycobacteria (Cavalier-Smith 2006c). The glycobacterial OM is homologous with and ancestral to the OM of mitochondria and chloroplasts but was lost in the ancestral unibacterium (Cavalier-Smith 2006c). Membrane continuity throughout evolution since before the origin of the last cell is a very basic evolutionary principle (Cavalier-Smith 1987a,b, 2001, 2004) as Blobel (1980) put it, ‘omnis membrana e membrana’. Membrane multiplication involves membrane heredity (Cavalier-Smith 2001, 2004) in which the different genetic membranes of a single cell are perpetuated by lipid- and protein-insertion mechanisms and machinery of high specificity. Thereby the inner membrane and OM of negibacteria, mitochondria (Cavalier-Smith 2006b) and chloroplasts, and the plasma membrane, peroxisomes and endomembrane systems of eukaryotes, remain distinct over hundreds of millions of years, perpetuated by growth and division of membranes always of the same kind. At the molecular level, membrane heredity involves self-complementarity between targeted proteins and membrane-embedded receptor proteins (Cavalier-Smith 2000), just as DNA heredity depends on DNA self-complementarity and three-dimensional complementarity between DNA and DNA-handling enzymes, e.g. DNA polymerases.

In glycobacteria, the inner leaflet of the OM lipid bilayer comprises typical acyl ester phospholipids but the outer leaflet is made of much more complex and substantially more impermeable lipolysaccharides. Glycobacteria can therefore only grow because the OM also has cylindrical pores made of oligomeric β-barrel proteins called porins that allow nutrient uptake from the environment. Their OMs uniquely have other macromolecular complexes mediating exchanges of larger molecules across it. All photosynthetic bacteria except Chlorobacteria are glycobacteria. In Eobacteria (comprising Chlorobacteria and Hadobacteria), the OM is simpler, with lipolysaccharide absent Eobacteria have glycolipids based on long-chain diols instead of glycerolipids (Pond et al. 1986 Woese 1987 Wait et al. 1997), unlike all other organisms. This chemical simplicity of eobacterial OMs is considered primitive, not a derived trait, in contrast to the topological simplicity of unibacterial membranes which arose by secondary loss of the OM as explained in detail elsewhere (Cavalier-Smith 2006c). Recent contrary claims that Posibacteria preceded Negibacteria are refuted by Valas & Bourne (2009). Porins and the universal mechanism for inserting β-barrel proteins into the OM apparently evolved prior to glycobacteria, as they are also present in Hadobacteria (heterotrophs such as the heat-loving Thermus and the extremely radiation resistant Deinococcus and their relatives). Ancestors of Hadobacteria, and of the purely heterotrophic glycobacterial phyla Spirochaetae and Planctobacteria, must have lost photosynthesis. Photosynthesis was also lost on several occasions within the holophyletic Chlorobacteria, Proteobacteria, Sphingobacteria and the paraphyletic Eurybacteria, arguably the ancestors of the non-photosynthetic Posibacteria (figure 4, which summarizes inferred relationships among the bacterial phyla forming the deepest branches in the tree of life). Only Cyanobacteria never lost photosynthesis and remain almost as uniform today in basic physiology as when they first evolved just over 2.4 billion years ago (though some fix nitrogen and some do not, several lineages lost their ancestral red/blue phycobilin pigments that makes them blue-green or red and one even lost photosystem II Zehr et al. 2008).

Figure 4. The tree of life, emphasizing the deepest branches. Ancestral groups of figures 1 and 3 are subdivided. Protozoa are resolved into two subkingdoms highlighted in yellow: the basal Eozoa (i.e. Euglenozoa plus Excavata), ancestrally characterized by a rigid cell pellicle supported by microtubules and the absence of pseudopodia (Cavalier-Smith submitted b) and the derived Sarcomastigota, ancestrally amoeboflagellates—probably with pointed pseudopodia, which gave rise to animals and fungi. Posibacteria comprise two subphyla: Endobacteria (putatively holophyletic) and Actinobacteria, which are probably the ancestors of neomura, having phosphatidylinositol lipids and proteasomes that both played key roles in eukaryogenesis (Cavalier-Smith 2009b). Glycobacteria are split into six phyla: three holophyletic, three paraphyletic (Cyanobacteria being ancestors of chloroplasts and thus partially of all Plantae, Chromista and those euglenoid eozoan Protozoa that secondarily acquired a plastid from green plants (figure 6) Proteobacteria being ancestors of mitochondria and thus in part of all eukaryotes ancestral to Posibacteria are Eurybacteria). Eurybacteria include Thermotogales, Aquificales (now see Bousseau et al. 2008), Heliobacteria and endospore-forming heterotrophs they are often unwisely lumped with Endobacteria as ‘Firmicutes’ merely because they group on sequence trees, despite being structurally negibacteria. Ancestrally photosynthetic groups are in green. The ancestral (paraphyletic) Eobacteria are split into two putatively holophyletic phyla: Chlorobacteria (often photosynthetic, i.e. non-sulphur green filamentous bacteria like Chloroflexus) and the heterotrophic Hadobacteria (e.g. Thermus, Deinococcus). Bacteria ancestrally lacked flagella soon after eubacterial rotary flagella evolved, one lineage relocated them to the periplasmic space to become spirochaetes (thumbnail sketch). Many lineages lost flagella, e.g. most Sphingobacteria and ancestors of neomura: archaebacteria re-evolved flagella and eukaryotes cilia, both entirely unrelated to eubacterial flagella. The higher proportion of holophyletic groups in figure 4 than figure 1 or 3 is bought at the expense of losing simplicity that more strikingly portrays major body-plan differences within eukaryotes (figure 1) and prokaryotes (figure 3). The extra cladistic resolution at the base of figure 4 is important for some purposes but irrelevant to others. Figures 1, 3, 4 and 5 are different ways of acceptably summarizing distinct aspects of the single true historical tree (which is reticulated and has ancestors and is thus not a cladogram or sequence tree). For more details on the 10 bacterial phyla and their relationships see Cavalier-Smith (2002a, 2006c). Oxygenic photosynthesis can have evolved no later than where shown by the upper blue arrow, immediately before the divergence of Cyanobacteria, but one reasonable non-decisive argument favours a marginally earlier origin before Hadobacteria diverged (lower blue arrow, when phospholipids arose Cavalier-Smith 2006c). A sound hierarchical classification with ranks can simply represent both the fundamental shared similarities within ancestral groups, such as Posibacteria, Eobacteria, Bacteria and Protozoa, and the profound differences between their major subgroups.

Just a few major innovations and many losses created the patchwork of bacterial phenotypes seen across the tree in addition, LGT complicated the story by introducing numerous archaebacterial thermophilic genes into eubacterial ancestors of the eurybacteria Thermotoga and Aquifex (Nesbø et al. 2001 Nesbø & Doolittle 2003 Bousseau et al. 2008), possibly endowing them with hyperthermophilic phenotypes that eubacteria might not have evolved without such foreign help. Eubacteria probably originated as the first cells in cool habitats where organic molecules would be most stable during the origin and early evolution of life (Cavalier-Smith 2001). Other useful enzymes have been transferred piecemeal among very distantly related bacterial lineages and from bacteria to eukaryotes (occasionally the reverse), but LGT never transferred major organismal properties dependent on numerous tightly interacting gene products, e.g. oxygenic photosynthesis, cell envelope structure or cell wall chemistry, from one bacterial lineage to another (only symbiogenesis by cell mergers managed that in eukaryotes). Non-laterally transferred morphology or macromolecular assemblies, being also immune to sequence tree reconstruction biases, were crucial for reconstructing the phylogeny of figures 3 and 4.

When mitochondria and chloroplasts evolved from enslaved cyanobacteria and α-proteobacteria (both glycobacteria), the OM lipolysaccharide was lost, being replaced by host phosphatidylcholine, but porins remained, some even being recruited for the novel protein-import machinery that made these enslaved bacteria integrated organelles. Porins are β-barrel proteins, a class of proteins absent from all membranes except the negibacterial OM and these two organelle OMs. Chlorobacteria are the only negibacteria that lack porins or other β-barrel OM proteins they are therefore considered the most primitive form of cell and most ancient ancestral type of negibacteria, because one can rule out the alternative idea of secondary simplification by loss of β-barrel OM proteins because loss of ability to insert them is lethal (Cavalier-Smith 2006c) only if the OM was lost at the same time as when Posibacteria originated could cells already dependent on β-barrel proteins survive. Some evolutionary innovations are effectively irreversible, e.g. many during the origin of eukaryotes.

Much writing on bacteria lumps Negibacteria and Posibacteria together as eubacteria (sometimes the prefix eu- is dropped (Woese et al. 1990) extremely unwise and confusing). Eubacteria ancestrally had walls of the peptidoglycan murein, never present in archaebacteria (now sadly often called archaea to conceal their truly bacterial nature (Woese et al. 1990) established taxonomic names should not be changed merely to promote a partisan view). In eukaryotes, murein is present only in the envelope of glaucophyte chloroplasts, as a relic of the cyanobacterial ancestor of plastids lost in the common ancestor of green and red algae, thus absent from other eukaryotes (its persistence in glaucophytes alone for 600 Myr puts the lie to the inevitability of evolutionary change and to using such archaisms to argue for the recency of events). A major event in the history of life, second in its revolutionary importance only to the origin of the eukaryote cell, was the replacement of murein walls (which are covalently three-dimensionally cross-linked to form an encasing sacculus molecule bigger than the cell), by walls of N-linked glycoproteins, which are not thus interlinked. This replacement occurred in the common ancestor of eukaryotes and archaebacteria, which are therefore grouped as clade neomura (‘new walls’ Cavalier-Smith 1987a). Glycoproteins are potentially freely mobile in the fluid phospholipid surface membranes, which the ancestor of eukaryotes exploited by converting the wall into a flexible surface coat. Its sister ancestor of archaebacteria prevented mobility by evolving rigid isoprenoid ether lipids and a crystalline glycoprotein wall. Potential flexibility of the neomuran cell surface was a prerequisite for the origin of phagocytosis by prey engulfment (which indirectly made the eukaryote cell Cavalier-Smith 2002b, 2009b) and sexual cell fusion.

Negibacteria are another ancestral group that universally shares a positive character (OM) absent in the clade (unimembrana) derived from it, which shares only the absence of the OM. As for Bacteria, this refutes cladistic dogma that paraphyletic groups are inadmissible because they necessarily lack positive traits that unify them.

8. The three-domain view of life is flawed: sequence trees are often misrooted

Many who use only RNA and protein sequences to interpret organismal history overlook the importance of the unique dramatic evolutionary transitions in cell structure in figures 3 and 4 for unravelling deep phylogeny. As I have shown (Cavalier-Smith 2002a, 2006a,c), ignoring organismal structure, cell biology and palaeontology led to a now widespread fundamental misinterpretation of the history of life, the three-domain system, in which it is incorrectly assumed that eubacteria are holophyletic and not substantially older than archaebacteria and eukaryotes and that the tree is rooted between neomura and eubacteria (Woese et al. 1990). These serious errors stemmed not only from failing to integrate sequence evidence with other data, but also from unawareness of the often extremely non-clock-like nature of sequence evolution and of grossly misleading systematic errors in sequence trees for molecules that do not evolve according to naive statistical preconceptions (see Cavalier-Smith 2002a, 2006a,c). Transition analysis using complex three-dimensional characters less prone to phylogenetic artefact than sequences provides powerful evidence that Posibacteria are ancestral to neomura, negibacteria ancestral to unibacteria and eobacteria ancestral to glycobacteria (Cavalier-Smith 2002a, 2006a,c Valas & Bourne 2009). Palaeontology provides equally strong evidence that Cyanobacteria are substantially older than eukaryotes and that eubacteria are an ancient ancestral group, not a clade (Cavalier-Smith 2006a). Statistics cannot adequately model the historically unique exceedingly rare events of megaevolution, for which assumptions of uniformism are entirely invalid (Cavalier-Smith 2006b). However, taking into account their known and inferred biases, sequence trees are compatible with the position of the root, the directions of the transitions and the topology of figures 3 and 4.

9. The four ages of life

An anaerobic phase in which photosynthetic non-sulphur bacteria (and before them extinct stem negibacteria) were the major primary producers for ecosystems. The major consumers with surviving descendants were heterotrophic chlorobacteria, and perhaps also Hadobacteria if they preceded the origin of photosystem II. Exclusively anaerobic life probably persisted for roughly a billion years (from approx. 3.5 Gyr ago, the consensus but controversial date for the origin of life, to just under approx. 2.5 Gyr ago, the best date for the origin of photosystem II and oxygenic photosynthesis (Kirschvink & Kopp 2008). Claims for an earlier origin approx. 2.78 Gyr ago have been invalidated by the discovery that the hydrocarbon hopanoid biomarkers on which they were based (anyway not specific for cyanobacteria Rashby et al. 2007) are not contemporaneous with the rocks whence they came (Rasmussen et al. 2008) they may be substantially younger (the same evidence invalidates claims using sterane biomarkers that eukaryotes are comparably old, always extremely discordant with the most conservative estimates based on morphological fossils of 800–850 Gyr (Cavalier-Smith 2002a) steranes are also not specific for eukaryotes). Though there have been claims for bacterial body fossils during this period, all are very nondescript (Schopf & Klein 1992) none is assignable to a particular phylum or subkingdom or even beyond reasonable question a genuine cellular fossil. Evidence for life is extremely indirect, mainly restricted to stromatolites (which could have been produced by filamentous Chlorobacteria or by stem bacteria now extinct) and isotopic signatures many of which may be genuinely biogenic but are prone to overoptimistic interpretations based on preconceptions and limited understanding of which aspects of presently known isotopic fractions can legitimately be extrapolated backwards into the Archaean, where we have no direct knowledge of which organisms were actually present. I call this the age of Eobacteria, though there is no direct evidence how far Chlorobacteria go back into this period or of when they replaced simpler stem bacteria that must once have existed.Though evidence for chlorobacteria being the most ancient cell type is good, I know none that can distinguish between their being sisters to all other organisms (as in figure 4) or a paraphyletic group ancestral to all other cells. Whichever is correct, if the tree is correctly rooted beside chlorobacteria as shown, or within them, they provide the best evidence we have for reconstructing the nature of the first cells. Aerobic life only evolved with the origin of oxygenic photosynthesis, which occurred at one of two points (figure 4): either immediately prior to the divergence of cyanobacteria and flagellate bacteria or somewhat earlier prior to the divergence of Hadobacteria.

The age of cyanobacteria (approx. 2.5–1.5 Gyr ago) in which cyanobacteria were the major primary producers and dominant morphological fossils. However, very extensive anaerobic habitats probably remained, especially in the deep ocean. In the later part of this period, there are convincing body fossils of diverse cyanobacteria, including complex filamentous forms, some with heterocysts for fixing nitrogen (Schopf & Klein 1992). Major innovations during this period were: the origins of eubacterial flagella enabling life to move from ancestral benthic microbial mats into the plankton the differential loss and modification of photosystem I or II to make three distinct phyla of anoxygenic phototrophs that could exploit anaerobic regions closed to cyanobacteria by acquiring novel antenna pigments enabling coexistence with and partial displacement of the more ancient chlorobacteria and internalization of flagella to form spirochaetes able to corkscrew through soft anaerobic sediments. Concomitantly, there was massive metabolic diversification yielding a huge diversity of chemotrophic and heterotrophic negibacteria (especially by modifying the dominant purple bacteria, Proteobacteria) that greatly affected biogeochemical cycles.

The age of slowly increasing morphological complexity and colonization of continental surfaces by both Cyanobacteria and Posibacteria (1.5–0.85 Gyr ago). In the past, some of the largest microfossils from this part of the middle Proterozoic have been attributed to eukaryotic algae more recently many have been instead assigned to the fungi or (more plausibly in my view) to a mixture of complex Cyanobacteria and of the Posibacteria that display the greatest morphological complexity: the actinomycete Actinobacteria (Cavalier-Smith 2006c). Possibly therefore Posibacteria originated about 1.5 Gyr ago. No fossils in this period can be assigned with confidence to any eukaryote phyla and none in my view can assuredly be identified as eukaryotes. Some have been thought to be stem eukaryotes of undefined affinities, but all identifications of fossils in this period (even my own) merit scepticism except for those that are almost indubitably filamentous cyanobacteria of various groups.

The age of eukaryotes and obvious macroorganisms (850–800 Myr ago to the present). Protozoa became the major predators on bacteria in water and wet earth typically brownish photophagotrophic and photosynthetic chromists conquered the oceans a green alga became a land plant 400 Myr ago, its descendants coating the continents where not too dry or cold with a green veneer providing homes and food for descendants of mobile animals (bilateria) that evolved 530 Myr ago via Cnidaria from marine sponges that fed on bacteria, like their choanoflagellate protozoan ancestors (figure 6). One choanoflagellate created sponges by evolving epithelia and connective tissue to allow more extensive filter feeding, and anisogamous sex to allow non-feeding ciliated larvae to grow large before settling onto rocks to feed. A distant choanozoan relative encased its filopodia in chitinous walls to evolve fungi that colonized soil as saprotrophs on dead plant material and symbionts and parasites of land plants. Archaebacterial sisters of eukaryotes colonized extreme habitats, one lineage evolving methanogenesis, changing climatic history by producing methane far faster than inorganic processes and triggering evolution of methanotrophs, mostly eubacteria (Cavalier-Smith 2006a) some methanogens invaded animal guts, evolving novel pseudomurein walls to evade digestion by host proteases.

Figure 5. The four ages of life. The six geological eras (black capitals) are demarcated especially by their fossils, which are absent in the Hadean, extremely sparse and problematic in the Archaean, numerous after about 2.2 Gy but all microscopic in the Proterozoic, and of every size and abundant in the Phanerozoic. In recognizing four ages of life (lower case colour on the right), I group the Late Proterozoic and Phanerozoic eras as the age of eukaryotes, because the origin of eukaryotic and archaebacterial cells that immediately followed the neomuran revolution is much more fundamental than the origin of bilaterian animals (around 550 Myr ago Martin et al. 2000) that arguably initiated the Cambrian explosion (approx. 535–525 Myr ago) at the base of the Phanerozoic. On this view, increased acritarch fossil complexity at the transition from mid- to late Proterozoic was directly caused by the origin of the eukaryote cell. The Archaean/Proterozoic boundary essentially corresponds with the origin of photosystem II and oxygenic photosynthesis, shortly before the divergence of cyanobacteria (which are holophyletic, ignoring their being chloroplast ancestors, and thus not directly ancestral to other photosynthetic glycobacteria figure 4). The early to mid-Proterozoic boundary is the most difficult to connect to a specific biological innovation. It may correspond with the origin of the posibacterial cell by a massive thickening of the murein wall and consequent loss of the OM, which may have stimulated the colonization of primitive cyanobacteria-dominated soils by Posibacteria (Cavalier-Smith 2006a) identification of the most complex mid-Proterozoic fossils as fungi (Butterfield 2005) is not compelling (earlier suggestions of eukaryotic algae were even less convincing). Possibly they are pseudosporangia and hyphae of Actinobacteria (Cavalier-Smith 2006a). The first convincing eukaryotic fossils are Melanocyrillium testate amoebae (Porter & Knoll 2000), though I do not accept their overconfident assignment to extant protozoan phyla (Porter et al. 2003) more likely they are an extinct group of early eukaryotes (Cavalier-Smith 2009a). Except for the final Vendian Period, bearing arguably stem animal fossils not confidently assignable to extant phyla, the Neoproterozoic was an era of only protists (unicellular eukaryotes prior to the origin of plastids, perhaps little over 600 Myr ago, probably mainly Eozoa (figure 6) and Amoebozoa) and bacteria phagotrophs diversified and underwent symbiogenesis to make various eukaryotic algae.

Figure 6. The eukaryote evolutionary tree, showing the messiness of real phylogeny. Compared with figure 1, the ancestral kingdoms Protozoa (all taxa inside the orange box) and Plantae are expanded to show their deepest branches and the reticulation caused by symbiogenetic cell enslavement. Apusozoa are gliding zooflagellates (Apusomonadida, Planomonadida Cavalier-Smith et al. 2008) deeply divergent from other main groups. The large red arrow indicates the enslavement of a phagocytosed red alga over 530 Myr ago by a biciliate protozoan to form the chimaeric common ancestor of kingdom Chromista. Previously, Alveolata (i.e. Ciliophora and Myzozoa) were treated as protozoa, but are now included within Chromista (Cavalier-Smith submitted b) Ciliophora and most Myzozoa (subphyla Dinozoa, Apicomplexa) have lost photosynthesis (though many heterotrophic Myzozoa retain colourless plastids for lipid synthesis). Likewise, Rhizaria (Cercozoa, Foraminifera, Radiozoa) and centrohelid Heliozoa, both formerly treated as Protozoa, appear to be major chromist lineages that independently lost the ancestral red algal chloroplast and are now placed within Chromista not Protozoa (Cavalier-Smith submitted b). One small lineage of dinoflagellates (Dinozoa) replaced its ancestral chloroplast symbiogenetically by another from an undigested eaten haptophyte chromist (Patron et al. 2006). Independently, another small dinoflagellate lineage replaced its plastid by one from a green alga (Viridiplantae dashed green arrow 1). Green algal chloroplasts were similarly independently implanted into Cercozoa (to make chlorarachnean algae arrow 2) and into Euglenozoa (to make euglenoid algae arrow 3). Euglenozoa, a phylum of ancestrally gliding zooflagellates (euglenoids kinetoplastids, e.g. Trypanosoma and Bodo postgaardiids and diplonemids), differ so greatly from all other eukaryotes, and retain primitive bacteria-like features of mitochondrial protein-targeting and nuclear DNA pre-replication implying that they are the earliest diverging eukaryotic branch (Cavalier-Smith submitted b). Excavates comprise three entirely heterotrophic phyla: the putatively ancestral largely aerobic phylum Loukozoa (jakobids, which retain the most bacteria-like mitochondrial DNA, and Malawimonas), the largely aerobic derived phylum Percolozoa, and the secondarily anaerobic phylum Metamonada (e.g. Giardia and Trichomonas) that converted its mitochondria into hydrogenosomes or mitosomes and lost their genomes. Similar anaerobic relics of mitochondria evolved independently in Fungi, Amoebozoa, Percolozoa, Euglenozoa and Chromista. Contrary to earlier ideas, there are no primitively amitochondrial or primitively non-ciliate eukaryotes earliest eukaryotes were aerobic flagellates, some of which evolved pseudopodia and became amoeboflagellates or eventually just amoebae. Animals and fungi both evolved from the same protozoan phylum, Choanozoa, but from different subgroups, being sisters of choanoflagellates and nucleariids, respectively (Shalchian-Tabrizi et al. 2008 Cavalier-Smith 2009a). Corticates and Eozoa are grouped as ‘bikonts’ formerly, the root of the eukaryote tree was postulated to be between unikonts and bikonts, not between Euglenozoa and excavates as shown here and justified in detail elsewhere (Cavalier-Smith submitted b)—a reassessment needing extensive testing.

The extremely complex origin of the eukaryotic cell initiated the modern world (phase 4) only after over three-quarters of the history of life was already over. This late origin of eukaryotes is attributable to the lateness of the immediately preceding neomuran revolution, during which bacterial secretion mechanisms and cell wall chemistry radically changed, allowing for the first time enough cell surface flexibility for evolution of phagocytosis of other cells. The inherent difficulty and improbability of the neomuran revolution, rather than the succeeding changes that made eukaryotes, probably accounts for the lateness of their origin and that of brainy life during the Cambrian explosion as a result of the origin of the anus and continuous flow processing of food (Cavalier-Smith 2006a).

It is no longer phylogenetically acceptable to assume that methanogenic archaebacteria existed in the Archaean age of anaerobic life and that their biogenic methane saved the Archaean world from global freezing. Either there was a now-extinct group of negibacteria that could make methane or, more likely, a mixture of carbon dioxide, water vapour and abiogenic methane were the major greenhouse gases maintaining climatic stability. Oxidative removal of abiogenic methane by the origin of oxygenic photosynthesis approximately 2.5 Gyr ago probably precipitated the Palaeoproterozoic global freezing approximately 2.3–2.4 Gyr ago (Kirschvink et al. 2000 Kopp et al. 2005 Kirschvink & Kopp 2008). Conversely, explosive production of methane by archaebacterial methanogenesis, significantly after neomura originated roughly 850 Myr ago, arguably destabilized climates by sudden runaway global warming and a reverberating intense cooling, inducing Neoproterozoic snowball Earth episodes (Cavalier-Smith 2006a).

The idea of Weismann and Wallace that asexual non-recombining organisms cannot evolve is wrong. Evolution in phases 1–3 was clonal: asexual cell lineages diverged without ever fusing. Some gene exchange occurred by viruses and in some groups by infectious plasmids or incidentally via food DNA (genetic transformation Redfield et al. 2006). But recombination was not fundamentally important for evolution it evolved primarily for DNA repair to stop harmful change. LGT was an incidental consequence of this effects were often neutral though sometimes of adaptive significance, as in the evolution of eubacterial thermophily, drug resistance, host range or acquisition of foreign enzymes. But progressive changes in basic cell structure and the initial evolution of each metabolic pathway probably depended largely on mutation and vertical inheritance. Sex probably originated relatively late during eukaryogenesis, as a consequence, not cause, of the preceding changes in cell structure (Cavalier-Smith 2002b). Recombination is probably more important for the preservation of complexity than for its origin.

10. The cambrian explosion and early eukaryote phylogeny

The Cambrian explosion of novel animal phyla was immediately preceded by and overlapped with a similar explosion of protozoan and eukaryote algal phyla. This close timing of protist and animal megadiversification is most simply interpreted as the natural biological outcome of the somewhat earlier origin of phagotrophy and the eukaryotic cell itself, before which neither animals nor the enslavement of cyanobacteria to form eukaryotic algae and belatedly land plants was possible (Cavalier-Smith 2006a). Figure 6 summarizes deep eukaryote phylogeny, showing that the animal and fungal kingdoms both evolved from choanozoan ancestors and that origins of the plant and chromist kingdoms lie in the other half of the protozoan tree. After the origin of the eukaryote cell, few major innovations in cell structure were needed before these four derived kingdoms could have evolved (see Cavalier-Smith (2009a) for details on early eukaryote body plans and Cavalier-Smith (submitted b) for deep eukaryotic phylogeny). Although eukaryotes originated at least by 800 Myr ago, the period 800–600 Myr ago was considerably occupied by roughly three successive near-global glaciations (snowball Earth), which surely would have retarded early protist diversification. It cannot be coincidental that the largest expansion of protist diversity in Earth history immediately followed these global glaciations. The pump was primed by the earlier origin of eukaryotes. Glacial melting did not initiate cellular innovation it just released the pent-up potential for innovation and rapid radiation that major new body plans themselves create. However, the symbiogenetic origin of chloroplasts may have taken place only about 600 Myr ago, immediately after the global snowball unfroze (most probably from 850 to 600 Myr ago the early eukaryotic photosynthesizers lived only by temporarily harbouring unintegrated cyanobacteria in their cells, as ‘pseudoalgae’ analogous to corals and green hydra, though eukaryotic algae might also have evolved earlier and failed to survive the freezing). Had archaebacteria never evolved and Neoproterozoic snowball Earth never occurred, the Cambrian explosion could have occurred 100 Myr earlier. But if the eubacterial cell wall necessarily prevented evolution of phagocytosis, phagocytosis could not have preceded the neomuran revolution and had to wait billions of years until that enabling change in wall chemistry.

11. Stasis, consTructional constraints and the rarity of mega-evolutionary innovation

The actual steps by which individuals come to differ from their parents are due to causes other than selection, and in consequence, evolution can only follow certain paths. These paths are determined by factors which we can only very dimly conjecture.

Variations are not, as Darwin thought, in every direction … Mutations only seem to occur along certain lines, which are very similar in closely related species, but differ in more distant species.

Contrary to what I implied above, purifying/stabilizing selection is not the sole cause of stasis. Constructional constraints that make some phenotypes much more readily mutable than others are often equally important. The extreme stability over 3.5 Gyr of the negibacterial body plan with two bounding membranes, compared with unimembrana with one, is not explicable by harmfulness of mutations changing it but by their extreme rarity. The OM arguably evolved and was lost only once in the history of life (Cavalier-Smith 1987a, 2006c) it is exceedingly difficult to see how any DNA mutation could eliminate the OM except by the mechanism proposed for the origin of unibacteria (Cavalier-Smith 1980, 2006c): murein hypertrophy preventing insertion of lipid and proteins synthesized elsewhere in the cell into it. Such a mechanism is unavailable to mitochondria or most plastids, which are therefore irretrievably encumbered with a double envelope, irrespective of whether they would in principle function better and more efficiently without them. It is unreasonable to argue that having two membranes around a plastid is adaptive or optimal, still less for the optimality of having four around them as most chromists do (figures 1 and 6) simply because of an accident in history impossible to reverse or substantially improve upon. There is no reason whatever to think that the basically different body plan of photosynthetic chromists compared with plants (i.e. with plastids inside a periplastid membrane) is functionally an improvement it is probably simply irreversible because no DNA mutation is possible that would remove three theoretically unnecessary membranes and relocate needed functions in just one. The complex lipid- and protein-insertion machinery is geared to retain the status quo and is permanently locked in complexity just as were the origins of the endomembrane system during the origin of eukaryotes, for which mutational reversal is inconceivable. The convergently evolved three membranes bounding dinoflagellate and euglenoid plastids are similarly frozen accidents (Cavalier-Smith 2003), like the specific details of the genetic code, and not adaptive.

Thus, progressive evolution is not inexorable, as Lamarck supposed, but has fits and starts, some especially significant for dividing the continuous tree of life into discrete taxa with radically different phenotypes durable over many hundreds of millions of years without radical evolutionary change. Lamarck imagined a polyphyletic origin of life, with inevitable steady upward progress he supposed that unicellular organisms such as bacteria simply originated much more recently than groups such as vertebrates and therefore had less time to evolve greater complexity. That view of steady change is wrong. Bacteria have been around far longer, but failed (except when one lineage became the first eukaryote) to evolve greater complexity despite mutations in every part of every gene in every generation for over three billion years, roughly a trillion generations—such is the power of constructional constraints and stabilizing selection to prevent radical evolutionary change. They enable ancestral (paraphyletic) groups to retain phenotypic coherence and validity as taxa, despite the occasional relatively rare origin from them of new body plans, themselves mostly stable for hundreds of millions of years. By my counting, fewer than 60 phyla evolved in the history of life (Cavalier-Smith 1998). Probably none and very few class-level body plans ever became extinct and few if any major adaptive zones were ever totally emptied by extinction throughout Earth history.

Yet the false Lamarckian view of a steady rate of evolution remains remarkably pervasive 150 years after Darwin wrote The origin, substituted the divergent tree model for linear progress, and argued that major new adaptive types could originate and radiate extremely rapidly compared with the generality of evolutionary change. Examples of touching faith in the uniformity of evolutionary rates include the false supposition that cryptomonads independently enslaved a red alga much more recently than other chromists, because they alone retain the red algal nucleus as a nucleomorph (Whatley et al. 1979) the false claim that rRNA is a molecular chronometer (Woese 1987) excessive respect for the myth of a biological sequence clock the idea that we can infer antiquity independently of direct fossil evidence from the degree of genetic or phenotypic change the idea that sister groups necessarily deserve equal rank (Hennig 1966) and the idea that older groups necessarily deserve higher ranks. Twenty-first-century biology deserves better than these pre-Darwinian hangovers. Taxonomic rank should reflect the magnitude of the phenotypic innovations that created the group's cenancestor, not cladistic or temporal properties of the tree, as Darwin, an excellent taxonomist, recognized. However, though noting the reality of stasis, Darwin overlooked the centrality of body-plan stasis in evolutionary explanations of the taxonomic hierarchy.

Thus, there can be an essential irreversibility of many innovations in body plan, enabling a minority of lineages to grow periodically more complex by successive steps (figures 1, 3, 4, 6). The eighteenth-century ladder of life was mistaken in its lack of branching, but not in representing genuine evolutionary progress. Lamarck was the first to realize that there is not a single ladder of life but several divergent or parallel ones, but unlike some later writers did not throw its progressive features out with the bathwater. As one of the very few systematists in the history of biology (a name he invented) to work successfully on the higher classification of both the animal and plant kingdoms, Lamarck saw an aspect of the big picture of evolution that Darwin and Wallace with their emphasis on adaptation and biogeography largely missed. This is the contrast that Lamarck drew between adaptive change through new habits and new environments and the inherent tendency of life to become more complex that is the dominant factor in evolving new body plans, which persist millions of years beyond any local selective forces that initiated them. Though (like both Darwins) Lamarck failed to understand that effects of changed habits on evolution were mediated by mutation and selection (Wallace (1889) and Weismann (1889) independently thus explained the evolutionary effects of ‘use and disuse’), he had a more balanced view than many of the interplay of internal and external factors in evolution and suffered unduly from misrepresentation of his actual views. As others like Whyte (1965) later emphasized, internal organismal factors in evolution must not be ignored. Wallace apparently never tried to explain the taxonomic hierarchy or published any tree, but took refuge in spiritualism and the idea of benevolent mind—helped by sundry subsidiary spirits—subtly diverting evolution away from its spontaneous tendencies towards usefulness for its crowning glory, civilized man (Wallace 1911) he rejected the pure mechanism of Maupertuis, Lamarck, Darwin and Haeckel as atheistic. Wallace (1911) thought that the origin of the eukaryotic cell required a designing mind a mechanistic explanation now exists (Cavalier-Smith 2009b). Increases in cellular and organismal complexity do not require a guiding mind, but are inevitable eventual consequences of life only being able to start very simply (for a model starting with only three genes in our last common ancestor, see Cavalier-Smith 2001). Once life began, radiation in every direction allowed by existing constructional constraints and continued viability must inevitably increase complexity in some lineages, irrespective of equally inevitable secondary simplifications in others how both occur is constrained not just by population genetics and ecology, but still more fundamentally by physical interactions and coevolution of different parts of the cell (Cavalier-Smith 2002a, 2006a, 2009b, in press), by developmental constraints in multicellular organisms (Raff 1996 Roux & Robinson-Rechavi 2008), and by the starting material available in each era from past phylogeny (phylogenetic constraints).

Historical accidents (e.g. which of several possibilities happened first) can become fixed as phylogenetic constraints. Thus, adaptations for phagotrophy almost certainly played a key role in initiating eukaryogenesis, but the endomembrane system, cytoskeleton and mitosis that evolved as a result of historical accidents and the inner logic of recovery from the associated disruptions (Cavalier-Smith 2009b) persist unchanged in plants, fungi and others that have long since given up phagotrophy simply because of constructional inertia and the irreversibility of complex evolution. Likewise, adaptedness to hyperthermophily probably favoured the origin of novel archaebacterial lipids, but played no role in their retention by secondary mesophiles, which was just constructional inertia coupled with the impossibility of re-evolving the old type or regaining them by LGT. The loss of the negibacterial OM may never have been directly selected at all, but was an indirect mechanistic consequence of murein hypertrophy that might itself have been an adaptation against desiccation (Cavalier-Smith 1980). Such constructional complications, what Darwin (1859) called ‘mysterious laws of the correlation of growth’—the sphere of cell and developmental biologists—are very important for evolutionary biology, yet outside the scope of the population genetics approach to evolution, which though illuminating is necessarily limited through sidestepping the specifics of actual phenotypes, particular phylogenies and unique historical accidents.

As always, Haldane (1932, pp. 104–105), the prime mover of modern evolutionary theory, was ahead of the pack in recognizing a role for constructional constraints in channelling large-scale evolution and in accepting that when ‘a successful evolutionary step rendered a new type of organism possible’, major subgroups arise relatively suddenly ‘in an orgy of variation’ and that subsequent evolution is ‘a slower affair’. Darwin (1859) said it as strongly. Of the ‘new synthesis’ authors only Simpson (1944), who coined the term ‘quantum evolution’ for the ultra-rapid origin of a new body plan, fully appreciated the extreme rapidity of mega-evolution, another neglected Simpsonian concept that I seek to revive. My life-time studies of microbial evolution fully confirm Simpson's conclusions from animal palaeontology and highlight the fundamental misinterpretations of the tree of life that arose from the contrasting false belief in uniformism throughout phylogenetic history (Cavalier-Smith 2006ac, 2009a,b, in press).

12. Need to intensify study of chlorobacteria

According to my recent analyses, Chlorobacteria are the most primitive extant cells (Cavalier-Smith 2006a,c). The misconception that Archaebacteria are extremely ancient early diverging cells especially significant for the origin of life (Woese & Fox 1977) has proved to be false (Cavalier-Smith 2006a,c). Widespread belief that it was true caused numerous fundamental misinterpretations of the tree of life and the dogmatism often associated with it has impeded more balanced understanding. However, faith in this fundamentally mistaken idea has also immensely stimulated research into archaebacteria for three decades, which has yielded innumerable valuable new discoveries and insights into microbiology. Moreover, as archaebacteria have turned out to be sisters of eukaryotes, the new facts were very important and beneficial for understanding their origin (Cavalier-Smith 1987a,b, 2002b, 2009b), though seeing archaebacteria as ancestral and ancient has been harmfully confusing and grossly misleading as to the nature of the last common ancestor of all life. Thus, intense recent archaebacterial research has been extremely productive and valuable, despite being totally irrelevant to and a distraction from understanding the origin of life. Better understanding of earliest evolution requires a comparable large-scale effort to elucidate the diversity, cell biology, and ecology of Chlorobacteria. If I am right about their deep phylogenetic position, this will greatly clarify the nature of the last common ancestor of all life. Even were I wrong, such research would hugely advance understanding of an important, highly divergent bacterial phylum probably the least understood of all 10 bacterial phyla that I currently recognize. Environmental DNA sequencing reveals numerous chlorobacterial lineages that have never been cultured. Only four genomes are sequenced (e.g. Seshadri et al. 2005 Wu et al. 2009) and the physiology and phenotypes of the vast majority of lineages are unknown. Chlorobacterial research is also important for biotechnology and bioremediation, as many (e.g. Dehalococcoides) anaerobically respire chlorinated hydrocarbons as food, playing a crucial role in their natural detoxification (Kittelmann & Friedrich 2008) might other novel metabolisms be revealed? Sceptics who wish to disprove my conclusions also should study chlorobacterial molecular and cell physiology to show how their cell envelopes work and see if they can explain how their apparently primitive properties might have evolved secondarily from other bacteria that I consider more advanced.

Membrane chemistry differs in the non-photosynthetic chlorobacterium Thermomicrobium from other negibacterial phyla by lacking glycerophospholipids (Wu et al. 2009) and having instead glycolipids based on long-chain diols (Pond et al. 1986 Wait et al. 1997), probably also present in the photosynthesic Chloroflexus (Woese 1987), and unusual glycosylated carotenoids (Wu et al. 2009) conceivably, these unusual lipids may stabilize chlorobacterial membranes in the absence of lipopolysaccharide or hopanoids. In addition to similar diol glycolipids, the hadobacterium Thermus possesses both phospholipids and glyceroglycolipids (Wait et al. 1997) this suggests that, if phospholipids and/or glycerolipids prove to be absent from all Chlorobacteria, one or both may have evolved after the divergence of hadobacteria and glycobacteria from them (figure 4). A phylogenetically broad survey of lipid chemistry and membrane organization (both the cytoplasmic and OM how greatly do they differ?) among Chlorobacteria would test this and be important for correctly deducing the nature of the membranes in the last common ancestor of all life contrary to widespread assumptions, such an ancestor might not have had any kind of phospholipid (whether the acyl ester phospholipids of non-chlorobacterial eubacteria or the isoprenoid ethers of archaebacteria) in its membranes it might instead have had acyl ester diol glycerolipids, only later replaced in most organisms by glycerophospholipids, with hadobacteria an intermediate stage possessing both. Many cherished assumptions about early cellular evolution might be overturned by more thorough and phylogenetically representative study of the molecular cell biology of Eobacteria, including the many still uncultured chlorobacterial lineages known only from environmental DNA sequencing.


DEVELOPMENTAL TERMS

Protostome: In protostomes (“first mouth”), the oral end of the animal develops from the first opening to form in early development (e.g., in molluscs, annelids, and arthropods).

Deuterostome: In deuterostomes (“second mouth”), the oral end develops from a second opening forming in early development (e.g., in echinoderms and chordates).

Mesoderm: The mesoderm is the middle layer of the three primary germ layers in the very early embryo, between the endoderm and ectoderm.

Trochophore larvae: This type of planktonic larva swims by the action of bands of cilia beating in synchrony.

Lecithotrophic larvae: Lecithotrophic (“yolk-eating”) larvae get their nutrition solely from yolk originally in the egg they commonly live in the water column for a short period of time (days to weeks).

Planktotrophic larvae: Planktotrophic (“plankton-eating”) larvae are capable of feeding and live in the water column for longer periods of time (weeks to months), increasing their dispersal capabilities.

Heterochrony: Heterochrony describes the evolutionary consequences of changes in developmental timing or rate. Paedomorphic taxa, as adults, appear similar to juveniles of their ancestors neotenic taxa decrease rate of development, whereas progenetic taxa truncate development. Peramorphic taxa delay maturation and extend their development beyond the adults of their ancestors.

Appreciation of the broader significance of brachiopods in metazoan evolution was triggered by the Field et al. (1988) study that attempted to reconstruct the molecular phylogeny of the animal kingdom by comparing sequences of nucleotides from small-subunit (18S) rRNA—at the time, a lofty but tremendously exciting goal. Field et al. (1988) concluded, on the basis of the inclusion of Lingula reevi in their study, that brachiopods were more closely related to molluscs (a protostome group) than to hemichordates and other deuterostomes. If robust, this molecular analysis would indicate that numerous significant developmental characters had evolved in parallel between the brachiopods and the deuterostomes (Eernisse et al. 1992, Luter & Bartolomaeus 1997, Peterson & Eernisse 2001), which was unsettling to many. Many researchers subsequently sequenced additional species, attempting to test the conclusions of Field and colleagues and establish an ever more robust and defensible phylogeny of all animals. These studies included at least one, sometimes two or three, brachiopod species, in part because of their mosaic of features, articulated so clearly by Hyman (Giribet et al. 2000, Paps et al. 2009, Sperling et al. 2011). From these and other studies, the Lophotrochozoa (Halanych et al. 1995) emerged, a clade that includes, among others, molluscs, annelids, bryozoans, phoronids, and brachiopods, deriving its name from morphological features of the lophophore and trochophore larvae.

Relationships among the lophotrochozoans have been difficult to establish (Giribet 2008), but until recently a consensus was beginning to emerge in which brachiopods and phoronids would form a clade more closely related either to molluscs (Mallatt & Winchell 2002, Paps et al. 2009, Luo et al. 2015) or to annelids (Dunn et al. 2008, Podsiadlowski et al. 2009), with bryozoans more distantly related, near the base of the lophotrochozoan clade (Nielsen 1995, 2002 Hejnol et al. 2009 Paps et al. 2009) (Figure 3a). More recent phylogenomic studies, however, have recovered a monophyletic Lophophorata (Nesnidal et al. 2013) (Figure 3b), which supports a hypothesis proposed initially by Emig (1984) on the basis of morphology. Relationships among phoronids and brachiopods remain contentious: Are they separate clades (Figure 4a,b) or internested clades (Figure 4c)? Cohen (2000) proposed the hypothesis that phoronids are brachiopods that have secondarily lost the bivalved shell, along with other morphological modifications. Despite the fact that this hypothesis nests one phylum inside another, which can be difficult for those with a static taxic view of the world to accept, this hypothesis is relatively easy to reconcile phylogenetically. It also has obvious implications for hypotheses about the evolution of the bivalved shell in brachiopods (Section 5.4). Later analyses have recovered the more traditional view that brachiopods and phoronids could be sister clades (Giribet et al. 2000, Sperling et al. 2011). Ongoing research (E.A. Sperling, personal communication) on the phylogenomics of brachiopods and phoronids utilizing next-generation sequencing techniques will hopefully resolve this disagreement definitively in the near future.

From the geological perspective, Conway Morris & Peel (1995) were the first to suggest that brachiopods might trace their origin to an unusual and poorly understood extinct group, the halkieriids, which possess multiple skeletal elements of unknown original mineralogy. However, Vinther & Nielsen (2005) concluded that halkieriids were likely to have been calcareous, and very likely to be more closely related to molluscs than to brachiopods. The study by Conway Morris & Peel (1995) triggered a host of other papers on a variety of rather poorly known Lower Cambrian phosphatic fossils referred to generally as tommotiids because of their first appearance in the Tommotian Stage of the Early Cambrian. One genus of tommotiid, Micrina, previously argued to be a halkieriid (Holmer et al. 2002), was claimed to represent a stem group brachiopod, largely because of microstructural features of the phosphatic sclerites (Williams & Holmer 2002, Skovsted et al. 2014). Several other Lower Cambrian fossils have also been considered as possible stem group brachiopods, including Mickwitzia (Skovsted & Holmer 2003), Tannuolina (Skovsted et al. 2014), Paterimitra (Larsson et al. 2014), and Heliomedusa (Zhang et al. 2009). The latter studies argue that the brachiopod ancestor closely resembled one of the many different Lower Cambrian fossils and possessed either a multielement phosphatic or agglutinated skeleton, or was soft-bodied (Balthasar & Butterfield 2009).

The term stem group has a specific meaning. It refers to a paraphyletic group basal to a crown clade, within a total clade (see sidebar, Phylogenetic Terms). In order to establish the boundaries of a stem group, a crown clade and a total clade must first be established. Yet neither had been established before the proliferation of papers that asserted, without phylogenetic analysis, putative stem groups or stem fossils (Skovsted et al. 2008). Most speculation on stem groups was untested (Skovsted et al. 2009, 2011). A more explicit phylogenetic analysis of many of these putative brachiopod stem groups (Carlson & Cohen 2009) suggests a range of hypotheses that are all equally plausible given the limited evidence in hand if anything, these analyses point to a possible stem-linguliform relationship (S.J. Carlson, in preparation). Later studies (Murdock et al. 2012, 2014) recommended that a robust phylogenetic analysis was needed to test, with data, the various stem group hypotheses. Coupled with the establishment of phylogenetic definitions of Brachiopoda and Pan-Brachiopoda (Carlson & Cohen 2016) (Figure 2), which define the brachiopod crown and total clades, more such analyses will enable the many stem group hypotheses to be tested rigorously.


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Vol 342, Issue 6164
13 December 2013

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