19. Rokas and Carroll, “Bushes in the Tree of Life,” 1899–1904.
20. Rokas and Carroll, “Bushes in the Tree of Life,” 1899–1904 (internal citations omitted).
21. Rokas and Carroll, “Bushes in the Tree of Life,” 1899–1904 (internal citations omitted).
22. Rokas and Carroll, “Bushes in the Tree of Life,” 1899–1904.
23. Rokas, Krüger, and Carroll, “Animal Evolution and the Molecular Signature of Radiations Compressed in Time,” 1935.
24. Zuckerkandl and Pauling, “Evolutionary Divergence and Convergence in Proteins,” 101.
25. Zuckerkandl and Pauling, “Evolutionary Divergence and Convergence in Proteins,” 101.
26. Theobald, “29+ Evidences for Macroevolution.”
27. Hyman, The Invertebrates, vol. 1: Protozoa Through Ctenophora.
28. Holton and Pisani, “Deep Genomic-Scale Analyses of the Metazoa Reject Coelomata.”
29. Aguinaldo et al., “Evidence for a Clade of Nematodes, Arthropods and Other Moulting Animals.” See also Telford et al., “The Evolution of the Ecdysozoa”; Halanych and Passamaneck, “A Brief Review of Metazoan Phylogeny and Future Prospects in Hox-Research”; and Mallatt, Garey, and Shultz, “Ecdysozoan Phylogeny and Bayesian Inference.”
30. Aguinaldo et al., “Evidence for a Clade of Nematodes, Arthropods and Other Moulting Animals.” See also Halanych, “The New View of Animal Phylogeny.”
31. Telford et al., “The Evolution of the Ecdysozoa.”
32. Aguinaldo et al., “Evidence for a Clade of Nematodes, Arthropods and Other Moulting Animals,” 492.
33. In 2004, for instance, researcher Yuri Wolf and his colleagues at the National Center for Biotechnology Information (NCBI) published a phylogeny based on molecular data (500 sets of proteins as well as insertion/deletion patterns in similar proteins) supporting the earlier Coelomata hypothesis. Wolf’s team concluded, “All of these approaches supported the coelomate clade and showed concordance between evolution of protein sequences and higher-level evolutionary events” (“Coelomata and Not Ecdysozoa,” 29). Another NCBI study, by Jie Zheng and colleagues published in 2007, analyzed conserved intron positions in the genomes of various animals; it supported the Coelomata clade and rejected Ecdysozoa (introns are sections of the genome that do not encode information for building proteins and occur in the genome between the regions, called exons, that do code for proteins; “Support for the Coelomata Clade of Animals from a Rigorous Analysis of the Pattern of Intron Conservation”).
34. In 2008, for example, Scott Roy (who also works at the NCBI) and Manuel Irimia (at the University of Barcelona) argued that the intron data actually supported the Ecdysozoa hypothesis (“Rare Genomic Characters Do Not Support Coelomata”).
35. Holton and Pisani, “Deep Genomic-Scale Analyses of the Metazoa Reject Coelomata.”
36. In this tree, now generally known as the Ecdysozoa hypothesis, the bilaterians are divided first into the protostomes and deuterostomes. the protostomes (or Protostomia) are then further subdivided into two distinct groups: (1) the Lophotrochozoa (so called because of two distinctive anatomical characters, a ciliated larva [trochophore] and a ciliated feeding structure [lophophore]) and (2) the Ecdysozoa (the molting animals).
37. Maley and Marshall, “The Coming of Age of Molecular Systematics,” 505.
38. As Maley and Marshall conclude, “Different representative species, in this case brine shrimp or tarantula for the arthropods, yield wildly different inferred relationships among phyla” (“The Coming of Age of Molecular Systematics,” 505).
39. According to Valentine, Jablonski, and Erwin, “Molecular evidence has produced a new view of metazoan phylogeny, prompting new analyses of morphological, ultrastructural and developmental characters” (“Fossils, Molecules and Embryos,” 854).
40. See Nielsen, Animal Evolution, 82.
41. Rokas et al., “Conflicting Phylogenetic Signals at the Base of the Metazoan Tree”; Halanych, “The New View of Animal Phylogeny”; Borchiellini et al., “Sponge Paraphyly and the Origin of Metazoa.”
42. Rokas et al., “Conflicting Phylogenetic Signals at the Base of the Metazoan Tree”; Halanych, “The New View of Animal Phylogeny.”
43. Gura, “Bones, Molecules … or Both?” 230. A 2004 paper in the Annual Review of Ecology and Systematics puts it this way: “Molecular tools have profoundly rearranged our understanding of metazoan phylogeny.” (Halanych, “The New View of Animal Phylogeny,” 229.)
44. Dávalos et al., “Understanding Phylogenetic Incongruence: Lessons from Phyllostomid Bats,” 993.
45. One might object here that building phylogenetic trees among the higher taxonomic groups, such as the animal phyla, is an inherently tricky business—but that phylogenetic trees describing lower taxonomic groups, such as those within the phyla, show consistency among different kinds of evidence. Of course, strictly speaking, even if there was evidence of a single coherent tree connecting groups within a phylum, it would do nothing to establish ancestors of the phyla themselves, but instead only members of the smaller groups within specific phyla. Nevertheless, even among lower taxa the primary literature on phylogenetic inference challenges the treelike picture of animal history.
Consider the crustacea, for instance, a large group within the phylum Arthropoda. The crustacea include such familiar creatures as shrimp and lobsters. (Darwin himself published his major technical work in biology on the classification of barnacles, a group [Cirripedia] within the crustacea.) Given the claims of Dawkins, Coyne, and Atkins, we might have expected that evolutionary biologists would have long ago established a single univocal evolutionary history for a well-studied group such as the crustacea, and that molecular data would by now only be confirming what biologists have known all along. But note, instead, that Ronald Jenner, a zoologist and expert on crustacea at the British Museum of Natural History, describes crustacean phylogeny as “essentially unresolved.” As he explains the situation, “Conflict is rife, irrespective of whether one compares different morphological studies, molecular studies, or both” (“Higher-Level Crustacean Phylogeny,” 143). The area of study remains “intensely contentious,” he continues, and “published studies show very few points of consensus, even if one constrains the comparison to just the most comprehensive and careful analyses” (151).
Other studies of different classes of organisms within the arthropod phyla introduce further uncertainty. Insects provide another important example of such incongruity. Based on anatomical evidence, systematists have long held that insects are most closely related to the group that contains centipedes and millipedes (called the myriapod group). Nevertheless, molecular studies by F. Nardi and colleagues indicate that insects are more closely related to crustaceans. Similarly, the same molecular study suggested that some wingless insects are more closely related to crustaceans than they are to other insects, though anatomical studies indicate the opposite for obvious reasons. This led the authors of the paper to conclude that insects (hexapods) are not monophyletic—a view never anticipated by most evolutionary biologists. Because of incongruities between molecular and morphology-based trees, the Nardi team offered a puzzled observation: “Although this tree shows many interesting outcomes, it also contains some evidently untenable relationships, which nevertheless have strong statistical support” (“Hexapod Origins,” 1887). But see Delsuc et al., “Comment on ‘Hexapod Origins: Monophyletic or Paraphyletic?’ ” 1482d; Nardi et al., “Response to Comment on ‘Hexapod Origins: Monophyletic or Paraphyletic?’” 1482e.
Studies of vertebrates, a subphylum of another phylum, the chordates, have revealed similar contradictory phylogenetic relationships. For example, a recent paper on bat phylogenetics, noted that “For more than a decade, evolutionary relationships among members of the New World bat family Phyllostomidae inferred from morphological and molecular data have been in conflict.” The authors “ruled out paralogy, lateral gene transfer, and poor taxon sampling and outgroup choices among the
processes leading to incongruent gene trees in phyllostomid bats.” The authors further note that “differential rates of change and evolutionary mechanisms driving those rates produce incongruent phylogenies. Incongruence among phylogenies estimated from different sets of characters is pervasive. Phylogenetic conflict has become a more acute problem with the advent of genome-scale data sets. These large data sets have confirmed that phylogenetic conflict is common, and frequently the norm rather than the exception.” Dávalos et al., “Understanding phylogenetic incongruence: lessons from phyllostomid bats,” 991–1024 (internal citations omitted). See also Patterson et al., “Congruence Between Molecular and Morphological Phylogenies,” 153–88.
46. Schwartz and Maresca, “Do Molecular Clocks Run at All?” 357.
47. James Valentine, for example, disputes the reality of the coelom as a shared characteristic that defines a group, as advocates of the Coelomata hypothesis contended. As Valentine notes, the “assumption of the monophyly of coelomic spaces” was one of the “major principles used to relate the phyla.” In his view, however, the coelom evolved multiple times independently and thus cannot be used as a homologous character defining a monophyletic group. He argues, instead, that “coeloms are polyphyletic. Few characters are simpler than fluid-filled cavities, and it is not difficult to visualize them as evolving many times for a number of purposes” (On the Origin of Phyla, 500).
48. Figure 6.2 derived from: Figure 1 of Edgecombe et al., “Higher-Level Metazoan Relationships: Recent Progress and Remaining Questions.”
49. For further discussion of the central position of germ cells in evolution, see Ewen-Campen, Schwager, and Extavour, “The Molecular Machinery of Germ Line Specification.” As they explain: “Sexually reproducing animals must ensure that one particularly important cell type is determined: the germ cells. These cells will be the sole progenitors of eggs and sperm in the sexually mature adult, and as such, their correct specification during embryonic development is critical for reproductive success and species survival” (3).
50. As is the case with mutations affecting other major organismal features, there is a remarkable absence of examples of successful (i.e., stably transmitted) mutations that significantly modify PGC formation in any animal group. Searching the experimental literature of the model systems in developmental biology, such as fruit flies (Drosophila), mice (Mus), and nematodes (C. elegans), reveals instead many loss-of-function or loss-of-structure examples, including total absence of egg cells (oocytes) in fruit flies (Lehmann, “Germ-Plasm Formation and Germ-Cell Determination in Drosophila”), germ-cell reduction and sterility in mice (Pellas et al., “Germ-Cell Deficient [gcd], an Insertional Mutation Manifested as Infertility in Transgenic Mice”), and oocyte elimination with consequent sterility in hermaphroditic nematodes (Kodoyianni, Maine, and Kimble, “Molecular Basis of Loss-of-Function Mutations in the glp–1 Gene of Caenorhabditis elegans”). See also Youngren, “The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours,” 360–64. Such examples of deleterious or catastrophic mutations could be multiplied indefinitely from these and other model systems.
51. Andrew Johnson, associate professor and reader in genetics at the University of Nottingham, and several coauthors frame the point this way: “Germ cell development acting as a constraint on embryonic morphogenesis is at first difficult to accept. However, the retention of a pool of PGCs, which will later produce gametes, is a fundamental constraint on any sexually reproducing organism, because the inability to pass inherited traits to subsequent generations will terminate an individual’s lineage. Therefore, changes in developmental processes that endanger the maintenance of PGCs will not be retained” (“Evolution of Predetermined Germ Cells in Vertebrate Embryos: Implications for Macroevolution,” 425, emphasis added).
52. Extavour, “Evolution of the Bilaterian Germ Line,” 774. See Fig. 6.4.
53. Extavour, “Gray Anatomy,” 420. Instead, she postulates that “convergent evolution has resulted in many different morphological, and possibly molecular genetic, solutions to the various problems posed by sexual reproduction.”
54. Willmer and Holland, “Modern Approaches to Metazoan Relationships,” 691, emphasis in original.
55. Willmer and Holland, “Modern Approaches to Metazoan Relationships,” 690.
56. Brusca and Brusca, Invertebrates, 120; 2nd ed., 115.
57. Jenner, “Evolution of Animal Body Plans,” 209.
58. In addition to convergent evolution, evolutionary biologists have offered a whole host of explanations to account for the many instances where shared anatomical and molecular similarity is not explicable by reference to vertical descent from a common ancestor, including: differing rates of evolution (resulting from positive selection or purifying selection), long branch attraction, rapid evolution, whole genome-fusion, coalescent (e.g., incomplete lineage sorting), DNA contamination, and horizontal gene transfer.
Horizontal gene transfer (HGT) occurs when organisms (usually prokaryotes such as bacteria) transfer genes to neighboring individuals. This mechanism provides a plausible explanation for some phylogenetic incongruence in prokaryotes, although some mission-critical housekeeping genes are thought to resist HGT. The mechanisms by which HGT occurs are well characterized, and include transformation (incorporation of free DNA from the environment into a recipient cell), transduction (transfer of DNA from one cell to another by a bacterial virus called a bacteriophage), and conjugation (transfer of DNA by direct cell-to-cell contact via a pilus). Horizontal gene transfer is less plausible however, in eukaryotes, where it occurs much less frequently and potential mechanisms are far less well characterized, although it is thought to occur in some rare cases between eukaryotes and prokaryotes, though more rarely, if at all, between different animals. [See Doolittle, “Phylogenetic Classification and the Universal Tree,” 2124–28; Hall, “Contribution of Horizontal Gene Transfer to the Evolution of Saccharomyces cerevisiae,” 1102–15; Kondo, “Genome Fragment of Wolbachia Endosymbiont Transferred to X Chromosome of Host Insect,” 14280–85.]
Another proposed explanation of phylogenetic conflict is called long-branch attraction, an artifact of the phylogenetic algorithms, that results in preferentially grouping together related lineages that diverged quickly, and then evolved separately over long periods of time. [Bergsten, “A Review of Long-Branch Attraction,” 163–93.]
Another proposed cause of incongruity is a phenomenon called incomplete lineage sorting. This occurs when a lineage splits and then rapidly splits again to yield three daughter species. This second split takes place before the process of sorting is complete (i.e., the process by which a daughter species gradually acquires its own unique set of genetic variants). This event is followed by the loss of a random variant by genetic drift, and this may cause two species to group together which otherwise would not. This process only accounts for phylogenetic incongruity between closely related species, however.
While some of these explanations may be plausible in some cases, they remain what they are: attempts to explain how two similar genes or traits could have arisen without those genes or traits having been inherited from a common ancestor. Thus in each case they provide counter-examples to the premise upon which all phylogenetic reconstruction is based—namely that similarity is an indicator of common ancestry.
Chapter 7: Punk Eek!
1. Lecture Notes, Paul Nelson, University of Pittsburgh, 9-28-83.
2. Gould and Eldredge, “Punctuated Equilibrium: The Tempo and Mode of Evolution Reconsidered,” 147.
3. Gould and Eldredge, “Punctuated Equilibrium: The Tempo and Mode of Evolution Reconsidered,” 115.
4. Eldredge, The Pattern of Evolution, 21.
5. Sepkoski, “ ‘Radical’ or ‘Conservative’? The Origin and Early Reception of Punctuated Equilibrium,” 301–25. Gould and Eldredge continued to jointly offered papers elaborating and refining the theory of punctuated equilibrium until 1993. See Gould and Eldredge, “Punct
uated Equilibrium Comes of Age,” 223–27.
6. As the U.S. National Academy of Sciences explained, punctuated equilibrium sought to account for the absence of transitional intermediates by showing that “changes in populations might occur too rapidly to leave many transitional fossils” (Teaching About Evolution and the Nature of Science, 57).
7. Though Gould and Eldredge formulated punctuated equilibrium several years before studies of the molecular evidence discussed in Chapter 6, their theory could also help explain the conflicting phylogenetic histories discussed there as well. As Rokas, Krüger, and Carroll would later argue (“Animal Evolution and the Molecular Signature of Radiations Compressed in Time”), if the evolutionary process acts quickly enough, leaving little time for differences to accumulate in key molecular markers, then biologists should expect phylogenetic studies to generate conflicting trees.
8. Sepkoski, “ ‘Radical’ or ‘Conservative’?” 304.
9. Gould and Eldredge, “Punctuated Equilibrium Comes of Age”; Theobald, “Punctuated Equilibrium” (“Punctuated equilibrium immediately lit a scientific controversy that has smoldered ever since”); Bell, “Gould’s Most Cherished Concept” (“Whether or not you agree with Gould that punctuated equilibrium has become the conventional wisdom, it certainly has led to a healthy debate concerning the sufficiency of neo-Darwinian theory to explain macroevolution, the analysis of biostratigraphic sequences, and the increased incorporation of paleontological data into evolutionary theory”); Dawkins, The Blind Watchmaker, 240–41; Dennett, Darwin’s Dangerous Idea, 282–99; Ridley, “The Evolution Revolution”; Gould, “Evolution: Explosion, Not Ascent”; Boffey, “100 Years after Darwin’s Death, His Theory Still Evolves”; Gleick, “The Pace of Evolution”; Maynard Smith, “Darwinism Stays Unpunctured”; Levinton, “Punctuated Equilibrium”; Schopf, Hoffman, and Gould, “Punctuated Equilibrium and the Fossil Record”; Lewin, “Punctuated Equilibrium Is Now Old Hat” (noting that “the tenor of the debate” over punctuated equilibrium “at times has been strident”); Levinton, “Bryozoan Morphological and Genetic Correspondence”; Lemen and Freeman, “A Test of Macroevolutionary Problems with Neontological Data”; Charlesworth, Lande, and Slatkin, “A Neo-Darwinian Commentary on Macroevolution”; Douglas and Avise, “Speciation Rates and Morphological Divergence in Fishes.”
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