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Animal Evolution: Genomes, Fossils, and Trees

Animal Evolution: Genomes, Fossils, and Trees One of the central and longest standing puzzles in systematic biology has been the interrelationships of the major higher taxa of animals. Pre-Darwinian biologists like Linnaeus, Lamarck, Geoffroy, and Cuvier all wrestled with the problem; and since the days of Darwin, a legion of the best comparative anatomists and embryologists, from Thomas Henry Huxley to Ernst Haeckel to Libby Hyman, have proposed phylogenies based on morphological and embryological characters. Yet, biologists could reach no consensus based solely on this evidence. Until recently, most books presented the problem as unresolved. Huge numbers of morphological and embryological characters were available and were analyzed many times by different phylogenetic methods, but a consensus solution eluded scientists for over a century. Another approach to the problem came from molecular biology, which developed to its present mature state only in the past two decades. As the editors of the review book point out, the first attempt to decipher metazoan phylogeny using molecular data was the small subunit rRNA sequence analysis of Field et al. (1988), published just 22 years ago. Molecular studies soon became more and more frequent as advances in technology made them easier and more reliable, and soon there were entire journals focused on topics like molecular evolution. The decade of 2000–2010 saw most of these studies converging on similar answers from many different molecular systems, and consensus starting to emerge. This progress has been marked by several new books, including Minelli's (2009) textbook (reviewed in this journal by Giribet 2009), and the book reviewed here. Unlike Minelli's textbook, the book of Telford and Littlewood, Animal Evolution: Genomes, Fossils, and Trees, is an edited symposium volume, originating from a Royal Society Discussion Meeting entitled “The Evolution of Animals—A Linnaean Tercentenary Celebration” in June 2007. Many of the contributions were first published in Philosophical Transactions of the Royal Society B: Biological Sciences (vol. 363, number 1496). As such, this volume benefits from the inclusion of many of the leading workers in the field. It also suffers in that the topics range widely, the coverage of themes is uneven, and there is not an overarching synthesis, as a single-authored textbook can have. Unlike many books on this topic, the Telford and Littlewood book includes chapters not only by molecular biologists, but also by paleontologists, embryologists, and morphologists. For scientists interested in the cutting edge of metazoan phylogeny research, this volume is indispensable. Nearly all the chapters are short and succinct, well illustrated (with a color section in the middle of the book for images that required color), and provide a valuable entrée into the detailed literature of their respective topics. Most are written at an accessible level that biologists and paleontologists should be able to understand, and are contributed by some of the leading scientists in each area of expertise. The volume begins with a chapter by paleontologist Graham Budd, summarizing the latest evidence and arguments around the “Cambrian explosion” and what might have triggered the appearance of multicellular skeletonized fossils. The second chapter by Peterson and others is authored by a mix of both paleontologists and molecular biologists (Peterson has expertise in both areas) summarizing their recent arguments that resolve the conundrum that molecular clock data suggest metazoan roots are much older than the fossil record suggests. The third chapter by Nichols and others looks at the recent evidence placing choanoflagellates as the sister group of metazoans, and the implications for the homeobox genes that support this hypothesis, and the changes needed to turn choanoflagellates into colonial sponges. In their chapter, “The mouth, the anus, and the blastopore—open questions about questionable openings,” Hejnol and Martindale dissect the old embryological arguments about the homologies of mouth, anus, and blastopores. They suggest that the evolution of anal openings was evolved several times independently. As such, the origins of these openings are not simple embryological homologs that could be used to support the monophyly of animals whose mouth or anus seemed to develop from the blastopore or from another part of the blastula. The second part of the book focuses on the evolution of the Bilateria, beginning with a chapter by legendary developmental biologist Rudolf Raff, who summarizes the status of embryological evidence in the light of the new molecular phylogenies of bilaterians. Giribet and others look at the evidence that supports the spiralian branch of the protostomes (i.e., the trochozoan clade of mollusks, annelids, lophophorates, and nemerteans, plus the platyozoan clade of flatworms and other acoelomate worms). Arendt and others describe how centralized nervous systems evolved within the Bilateria. Telford and others dissect the relationships of the (now well-supported) clade of Ecdysozoa, the“molting animals” united by their possession of a chitinous exoskeleton that must be molted during growth. The Ecdysozoan includes arthropods, velvet worms, priapulids and kinorhynchs, and the nematodes. Smith and Swalla look at deuterostome (echinoderms, hemichordates, and chordates) phylogeny, utilizing evidence from both the fossil record and the latest molecular data. Lowe discusses how the molecular genetics of the hemichordate Saccoglossus gives insights into deuterostome development. Despite the big differences in morphology between an acorn worm and a chordate, the degree of conservation of gene expression in both groups is remarkable. The final section of the book examines a miscellany of topics of both paleontological and molecular nature. Jenner and Littlewood discuss the issue with problematic taxa, both mysterious and poorly preserved fossils as well as living organisms whose phylogenetic placement is obscure. Lartillot and Philippe summarize the evidence for how phylogenetic methods analyzing the relationships of bilaterians have improved, using better models of molecular evolution. Boore and Fuerstenberg make the argument that characters at the level of entire genomes, not just linear sequences of nucleotides, have an important role to play in phylogenetic analysis. Copley discusses the problem of making the link between genomic and phenotypic complexity, and how the problem needs to be understood in the context of interacting components. Sperling and Peterson make the case that microRNAs may be the best molecular sequences for phylogenetic analysis because they are added over time, rarely change their primary sequence, rarely are secondarily lost, and appear to be nearly free of homoplasies. Peel summarizes the evolution of novelty in insects, focusing on developmental gene networks, as exemplified by insects that undergo complete metamorphosis. Beldade and Saenko discuss the implications of conserved developmental processes and their role in the evolution of novel traits in embryos and adults. Finally, the editors contribute a summary chapter, which nicely synthesizes most of the recent research (including the chapters in this book), describing it as a “four-dimensional puzzle.” In this chapter, they point out the successes that have been achieved, the remaining problem areas for future research, and the perspectives that have been gained over the past two decades. Most importantly, this is one of the few books or symposia that truly represent a synthesis of paleontological, embryological, morphological, and molecular data. Too often, we hear only one side of the story, with no consideration of conflicting data from other fields. This problem is particularly acute in the area of vertebrate phylogeny (not covered in this book, a significant oversight), which has seen a pattern of noncooperation between paleontologists/morphologists and molecular biologists. In particular, the molecular biologists have unilaterally declared that they have solved the long-standing problems of mammalian phylogeny, without seeking much or any input from mammalian paleontologists, despite efforts by mammalian paleontologists such as Malcolm McKenna and Michael Novacek in the 1980s and 1990s to reach out to them. Today, their phylogenies and taxa such as “Laurasiatheria” and “Euarchontoglires” are routinely accepted by outsiders, even though there is no support from any anatomical or nonmolecular evidence, and most mammalian paleontologists have not adopted this classification scheme. Combined with single-author textbooks like Minelli (2009), this volume is extremely useful for those who want to find out the latest ideas, or catch up in an area of research that moves more rapidly than most of us can keep up with. The past decade was truly one of remarkable progress solving centuries-old problems. Volumes such as this are valuable milestones and summaries of that progress, even as more studies are published that push the boundaries of our understanding of metazoan phylogeny even further. References Field KG , Olsen GJ , Lane DJ , Giovannoni SJ , Ghiselin MT , Raff EC . Molecular phylogeny of the animal kingdom , Science , 1988 , vol. 239 (pg. 748 - 753 ) Google Scholar Crossref Search ADS PubMed WorldCat Giribet G . Review of Perspectives in animal phylogeny and evolution , Syst. Biol. , 2009 , vol. 58 (pg. 159 - 160 ) Google Scholar Crossref Search ADS WorldCat Minelli A . , Perspectives in animal phylogeny and evolution. , 2009 Oxford Oxford University Press Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC © The Author(s) 2010. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: [email protected] http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Systematic Biology Oxford University Press

Animal Evolution: Genomes, Fossils, and Trees

Prothero, Donald, R.
Systematic Biology , Volume 59 (6) – Dec 1, 2010
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Publisher
Oxford University Press
Copyright
© The Author(s) 2010. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: [email protected]
ISSN
1063-5157
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1076-836X
DOI
10.1093/sysbio/syq033
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Abstract

One of the central and longest standing puzzles in systematic biology has been the interrelationships of the major higher taxa of animals. Pre-Darwinian biologists like Linnaeus, Lamarck, Geoffroy, and Cuvier all wrestled with the problem; and since the days of Darwin, a legion of the best comparative anatomists and embryologists, from Thomas Henry Huxley to Ernst Haeckel to Libby Hyman, have proposed phylogenies based on morphological and embryological characters. Yet, biologists could reach no consensus based solely on this evidence. Until recently, most books presented the problem as unresolved. Huge numbers of morphological and embryological characters were available and were analyzed many times by different phylogenetic methods, but a consensus solution eluded scientists for over a century. Another approach to the problem came from molecular biology, which developed to its present mature state only in the past two decades. As the editors of the review book point out, the first attempt to decipher metazoan phylogeny using molecular data was the small subunit rRNA sequence analysis of Field et al. (1988), published just 22 years ago. Molecular studies soon became more and more frequent as advances in technology made them easier and more reliable, and soon there were entire journals focused on topics like molecular evolution. The decade of 2000–2010 saw most of these studies converging on similar answers from many different molecular systems, and consensus starting to emerge. This progress has been marked by several new books, including Minelli's (2009) textbook (reviewed in this journal by Giribet 2009), and the book reviewed here. Unlike Minelli's textbook, the book of Telford and Littlewood, Animal Evolution: Genomes, Fossils, and Trees, is an edited symposium volume, originating from a Royal Society Discussion Meeting entitled “The Evolution of Animals—A Linnaean Tercentenary Celebration” in June 2007. Many of the contributions were first published in Philosophical Transactions of the Royal Society B: Biological Sciences (vol. 363, number 1496). As such, this volume benefits from the inclusion of many of the leading workers in the field. It also suffers in that the topics range widely, the coverage of themes is uneven, and there is not an overarching synthesis, as a single-authored textbook can have. Unlike many books on this topic, the Telford and Littlewood book includes chapters not only by molecular biologists, but also by paleontologists, embryologists, and morphologists. For scientists interested in the cutting edge of metazoan phylogeny research, this volume is indispensable. Nearly all the chapters are short and succinct, well illustrated (with a color section in the middle of the book for images that required color), and provide a valuable entrée into the detailed literature of their respective topics. Most are written at an accessible level that biologists and paleontologists should be able to understand, and are contributed by some of the leading scientists in each area of expertise. The volume begins with a chapter by paleontologist Graham Budd, summarizing the latest evidence and arguments around the “Cambrian explosion” and what might have triggered the appearance of multicellular skeletonized fossils. The second chapter by Peterson and others is authored by a mix of both paleontologists and molecular biologists (Peterson has expertise in both areas) summarizing their recent arguments that resolve the conundrum that molecular clock data suggest metazoan roots are much older than the fossil record suggests. The third chapter by Nichols and others looks at the recent evidence placing choanoflagellates as the sister group of metazoans, and the implications for the homeobox genes that support this hypothesis, and the changes needed to turn choanoflagellates into colonial sponges. In their chapter, “The mouth, the anus, and the blastopore—open questions about questionable openings,” Hejnol and Martindale dissect the old embryological arguments about the homologies of mouth, anus, and blastopores. They suggest that the evolution of anal openings was evolved several times independently. As such, the origins of these openings are not simple embryological homologs that could be used to support the monophyly of animals whose mouth or anus seemed to develop from the blastopore or from another part of the blastula. The second part of the book focuses on the evolution of the Bilateria, beginning with a chapter by legendary developmental biologist Rudolf Raff, who summarizes the status of embryological evidence in the light of the new molecular phylogenies of bilaterians. Giribet and others look at the evidence that supports the spiralian branch of the protostomes (i.e., the trochozoan clade of mollusks, annelids, lophophorates, and nemerteans, plus the platyozoan clade of flatworms and other acoelomate worms). Arendt and others describe how centralized nervous systems evolved within the Bilateria. Telford and others dissect the relationships of the (now well-supported) clade of Ecdysozoa, the“molting animals” united by their possession of a chitinous exoskeleton that must be molted during growth. The Ecdysozoan includes arthropods, velvet worms, priapulids and kinorhynchs, and the nematodes. Smith and Swalla look at deuterostome (echinoderms, hemichordates, and chordates) phylogeny, utilizing evidence from both the fossil record and the latest molecular data. Lowe discusses how the molecular genetics of the hemichordate Saccoglossus gives insights into deuterostome development. Despite the big differences in morphology between an acorn worm and a chordate, the degree of conservation of gene expression in both groups is remarkable. The final section of the book examines a miscellany of topics of both paleontological and molecular nature. Jenner and Littlewood discuss the issue with problematic taxa, both mysterious and poorly preserved fossils as well as living organisms whose phylogenetic placement is obscure. Lartillot and Philippe summarize the evidence for how phylogenetic methods analyzing the relationships of bilaterians have improved, using better models of molecular evolution. Boore and Fuerstenberg make the argument that characters at the level of entire genomes, not just linear sequences of nucleotides, have an important role to play in phylogenetic analysis. Copley discusses the problem of making the link between genomic and phenotypic complexity, and how the problem needs to be understood in the context of interacting components. Sperling and Peterson make the case that microRNAs may be the best molecular sequences for phylogenetic analysis because they are added over time, rarely change their primary sequence, rarely are secondarily lost, and appear to be nearly free of homoplasies. Peel summarizes the evolution of novelty in insects, focusing on developmental gene networks, as exemplified by insects that undergo complete metamorphosis. Beldade and Saenko discuss the implications of conserved developmental processes and their role in the evolution of novel traits in embryos and adults. Finally, the editors contribute a summary chapter, which nicely synthesizes most of the recent research (including the chapters in this book), describing it as a “four-dimensional puzzle.” In this chapter, they point out the successes that have been achieved, the remaining problem areas for future research, and the perspectives that have been gained over the past two decades. Most importantly, this is one of the few books or symposia that truly represent a synthesis of paleontological, embryological, morphological, and molecular data. Too often, we hear only one side of the story, with no consideration of conflicting data from other fields. This problem is particularly acute in the area of vertebrate phylogeny (not covered in this book, a significant oversight), which has seen a pattern of noncooperation between paleontologists/morphologists and molecular biologists. In particular, the molecular biologists have unilaterally declared that they have solved the long-standing problems of mammalian phylogeny, without seeking much or any input from mammalian paleontologists, despite efforts by mammalian paleontologists such as Malcolm McKenna and Michael Novacek in the 1980s and 1990s to reach out to them. Today, their phylogenies and taxa such as “Laurasiatheria” and “Euarchontoglires” are routinely accepted by outsiders, even though there is no support from any anatomical or nonmolecular evidence, and most mammalian paleontologists have not adopted this classification scheme. Combined with single-author textbooks like Minelli (2009), this volume is extremely useful for those who want to find out the latest ideas, or catch up in an area of research that moves more rapidly than most of us can keep up with. The past decade was truly one of remarkable progress solving centuries-old problems. Volumes such as this are valuable milestones and summaries of that progress, even as more studies are published that push the boundaries of our understanding of metazoan phylogeny even further. References Field KG , Olsen GJ , Lane DJ , Giovannoni SJ , Ghiselin MT , Raff EC . Molecular phylogeny of the animal kingdom , Science , 1988 , vol. 239 (pg. 748 - 753 ) Google Scholar Crossref Search ADS PubMed WorldCat Giribet G . Review of Perspectives in animal phylogeny and evolution , Syst. Biol. , 2009 , vol. 58 (pg. 159 - 160 ) Google Scholar Crossref Search ADS WorldCat Minelli A . , Perspectives in animal phylogeny and evolution. , 2009 Oxford Oxford University Press Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC © The Author(s) 2010. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: [email protected]

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Systematic Biology – Oxford University Press

Published: Dec 1, 2010

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