The Cambrian Conundrum: Early Divergence and Later Ecological Success in the Early History of Animals

Major animal clades evolved tens of millions of years before the widespread appearance of animal fossils. Diverse bilaterian clades emerged apparently within a few million years during the early Cambrian, and various environmental, developmental, and ecological causes have been proposed to explain this abrupt appearance. A compilation of the patterns of fossil and molecular diversification, comparative developmental data, and information on ecological feeding strategies indicate that the major animal clades diverged many tens of millions of years before their first appearance in the fossil record, demonstrating a macroevolutionary lag between the establishment of their developmental toolkits during the Cryogenian [(850 to 635 million years ago (Ma)], and the later ecological success of metazoans during the Ediacaran (635 to 541 Ma) and Cambrian (541 to 488 Ma) periods. We argue that this diversification involved new forms of developmental regulation, as well as innovations in networks of ecological interaction within the context of permissive environmental circumstances.

[1]  D. Venton Paleobiology , 2013, Proceedings of the National Academy of Sciences.

[2]  D. Erwin,et al.  The Cambrian Explosion: The Construction of Animal Biodiversity. , 2013 .

[3]  P. Cárdenas,et al.  No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera , 2012, Hydrobiologia.

[4]  Yan Liu,et al.  A Potent and Broad Neutralizing Antibody Recognizes and Penetrates the HIV Glycan Shield , 2011, Science.

[5]  Auinash Kalsotra,et al.  Functional consequences of developmentally regulated alternative splicing , 2011, Nature Reviews Genetics.

[6]  G. Edgecombe,et al.  MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda , 2011, Proceedings of the National Academy of Sciences.

[7]  S. Bengtson,et al.  Chronology of early Cambrian biomineralization , 2011, Geological Magazine.

[8]  T. Iliffe,et al.  Global Biodiversity and Phylogenetic Evaluation of Remipedia (Crustacea) , 2011, PloS one.

[9]  K. Peterson,et al.  Molecular paleobiological insights into the origin of the Brachiopoda , 2011, Evolution & development.

[10]  J. Grotzinger,et al.  Enigmatic origin of the largest-known carbon isotope excursion in Earth's history , 2011 .

[11]  A. Knoll The Multiple Origins of Complex Multicellularity , 2011 .

[12]  J. Zalasiewicz,et al.  An Early Cambrian Hemichordate Zooid , 2011, Current Biology.

[13]  H. Philippe,et al.  Resolving Difficult Phylogenetic Questions: Why More Sequences Are Not Enough , 2011, PLoS biology.

[14]  B Franz Lang,et al.  Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. , 2011, Molecular biology and evolution.

[15]  G. Shields-Zhou,et al.  The case for a Neoproterozoic Oxygenation Event: Geochemical evidence and biological consequences , 2011 .

[16]  R. Copley,et al.  Acoelomorph flatworms are deuterostomes related to Xenoturbella , 2011, Nature.

[17]  G. Edgecombe,et al.  A congruent solution to arthropod phylogeny: phylogenomics, microRNAs and morphology support monophyletic Mandibulata , 2011, Proceedings of the Royal Society B: Biological Sciences.

[18]  K. Peterson,et al.  Rangeomorphs, Thectardis (Porifera?) and dissolved organic carbon in the Ediacaran oceans , 2011, Geobiology.

[19]  A. Maloof,et al.  The earliest Cambrian record of animals and ocean geochemical change , 2010 .

[20]  D. Erwin,et al.  Possible animal-body fossils in pre-Marinoan limestones from South Australia , 2010 .

[21]  Todd H. Oakley,et al.  The Amphimedon queenslandica genome and the evolution of animal complexity , 2010, Nature.

[22]  A. Maloof,et al.  Constraints on early Cambrian carbon cycling from the duration of the Nemakit-Daldynian–Tommotian boundary δ13C shift, Morocco , 2010 .

[23]  Robert S. Sansom,et al.  Soft-part anatomy of the Early Cambrian bivalved arthropods Kunyangella and Kunmingella: significance for the phylogenetic relationships of Bradoriida , 2010, Proceedings of the Royal Society B: Biological Sciences.

[24]  George C. Ebers,et al.  The natural history of multiple sclerosis, a geographically based study 10: relapses and long-term disability , 2010, Brain : a journal of neurology.

[25]  Jonathan B. Losos,et al.  Adaptive Radiation, Ecological Opportunity, and Evolutionary Determinism , 2010, The American Naturalist.

[26]  J. Keppie,et al.  Cambrian origin of all skeletalized metazoan phyla—Discovery of Earth's oldest bryozoans (Upper Cambrian, southern Mexico) , 2010 .

[27]  S. Zamora Middle Cambrian echinoderms from north Spain show echinoderms diversified earlier in Gondwana , 2010 .

[28]  J. Vinther,et al.  Ordovician faunas of Burgess Shale type , 2010, Nature.

[29]  Martin R. Smith,et al.  Primitive soft-bodied cephalopods from the Cambrian , 2010, Nature.

[30]  B. Morgenstern,et al.  Improved Phylogenomic Taxon Sampling Noticeably Affects Nonbilaterian Relationships , 2010, Molecular biology and evolution.

[31]  J. Mallatt,et al.  Nearly complete rRNA genes assembled from across the metazoan animals: effects of more taxa, a structure-based alignment, and paired-sites evolutionary models on phylogeny reconstruction. , 2010, Molecular phylogenetics and evolution.

[32]  D. Shu,et al.  Tentaculate Fossils from the Cambrian of Canada (British Columbia) and China (Yunnan) Interpreted as Primitive Deuterostomes , 2010, PloS one.

[33]  A. Daley,et al.  A Possible Anomalocaridid from the Cambrian Sirius Passet Lagerstätte, North Greenland , 2010 .

[34]  J. S. Peel A Corset-Like Fossil from the Cambrian Sirius Passet Lagerstätte of North Greenland and Its Implications for Cycloneuralian Evolution , 2010 .

[35]  J. Vinther,et al.  A placozoan affinity for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes , 2010, Evolution & development.

[36]  G. Edgecombe Arthropod phylogeny: an overview from the perspectives of morphology, molecular data and the fossil record. , 2010, Arthropod structure & development.

[37]  S. Morris,et al.  New Palaeoscolecidan Worms from the Lower Cambrian: Sirius Passet, Latham Shale and Kinzers Shale , 2010 .

[38]  D. McIlroy,et al.  First evidence for locomotion in the Ediacara biota from the 565 Ma Mistaken Point Formation, Newfoundland , 2010 .

[39]  K. Peterson,et al.  Where's the glass? Biomarkers, molecular clocks, and microRNAs suggest a 200‐Myr missing Precambrian fossil record of siliceous sponge spicules , 2010, Geobiology.

[40]  A. Ivantsov New reconstruction of Kimberella, problematic Vendian metazoan , 2009 .

[41]  J. W. Valentine,et al.  THE IMPORTANCE OF PREADAPTED GENOMES IN THE ORIGIN OF THE ANIMAL BODYPLANS AND THE CAMBRIAN EXPLOSION , 2009, Evolution; international journal of organic evolution.

[42]  E. Davidson,et al.  Evolutionary innovation and stability in animal gene networks. , 2009, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[43]  Davide Pisani,et al.  Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. , 2009, Molecular biology and evolution.

[44]  I. Rahman,et al.  The oldest cinctan carpoid (stem-group Echinodermata), and the evolution of the water vascular system , 2009 .

[45]  J. Paterson,et al.  The Tommotiid Camenella reticulosa from the Early Cambrian of South Australia: Morphology, Scleritome Reconstruction, and Phylogeny , 2009 .

[46]  Artem V. Kouchinsky,et al.  The lower cambrian fossil anabaritids: Affinities, occurrences and systematics , 2009 .

[47]  D. Erwin Early origin of the bilaterian developmental toolkit , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[48]  M. McPeek,et al.  MicroRNAs and metazoan macroevolution: insights into canalization, complexity, and the Cambrian explosion , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[49]  Corinne Da Silva,et al.  Phylogenomics Revives Traditional Views on Deep Animal Relationships , 2009, Current Biology.

[50]  A. Knoll,et al.  Large spinose microfossils in Ediacaran rocks as resting stages of early animals , 2009, Proceedings of the National Academy of Sciences.

[51]  Daniel J. Condon,et al.  Fossil steroids record the appearance of Demospongiae during the Cryogenian period , 2009, Nature.

[52]  L. Holmer,et al.  THE ENIGMATIC EARLY CAMBRIAN SALANYGOLINA– A STEM GROUP OF RHYNCHONELLIFORM CHILEATE BRACHIOPODS? , 2009 .

[53]  S. McLoughlin,et al.  Early Jurassic annelid cocoons from eastern Australia , 2008 .

[54]  D. Erwin Macroevolution of ecosystem engineering, niche construction and diversity. , 2008, Trends in ecology & evolution.

[55]  M. Martindale,et al.  Acoel development supports a simple planula-like urbilaterian , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[56]  J. Cotton,et al.  The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[57]  T. Maniatis,et al.  Multilevel Regulation of Gene Expression by MicroRNAs , 2008, Science.

[58]  A. Anbar,et al.  Tracing the stepwise oxygenation of the Proterozoic ocean , 2008, Nature.

[59]  L. Holmer,et al.  The scleritome of Eccentrotheca from the Lower Cambrian of South Australia: Lophophorate affinities and implications for tommotiid phylogeny , 2008 .

[60]  J. Vinther,et al.  Machaeridians are Palaeozoic armoured annelids , 2008, Nature.

[61]  S. Xiao,et al.  The Avalon Explosion: Evolution of Ediacara Morphospace , 2008, Science.

[62]  H. Hofmann,et al.  Ediacaran Biota on Bonavista Peninsula, Newfoundland, Canada , 2008, Journal of Paleontology.

[63]  D. Bryant,et al.  A general comparison of relaxed molecular clock models. , 2007, Molecular biology and evolution.

[64]  P. Allen,et al.  Geochronologic constraints on the chronostratigraphic framework of the Neoproterozoic Huqf Supergroup, Sultanate of Oman , 2007, American Journal of Science.

[65]  H. Mutvei,et al.  LATE CAMBRIAN PLECTRONOCERID NAUTILOIDS AND THEIR ROLE IN CEPHALOPOD EVOLUTION , 2007 .

[66]  A. Collins,et al.  Exceptionally Preserved Jellyfishes from the Middle Cambrian , 2007, PloS one.

[67]  Maoyan Zhu,et al.  Diverse pelagic predators from the Chengjiang Lagerstätte and the establishment of modern-style pelagic ecosystems in the early Cambrian , 2007 .

[68]  L. Babcock,et al.  Cambrian chronostratigraphy: Current state and future plans , 2007 .

[69]  M. Steiner,et al.  Early Cambrian metazoan fossil record of South China: Generic diversity and radiation patterns , 2007 .

[70]  J. Sigwart,et al.  Deep molluscan phylogeny: synthesis of palaeontological and neontological data , 2007, Proceedings of the Royal Society B: Biological Sciences.

[71]  Xi-guang Zhang,et al.  An epipodite-bearing crown-group crustacean from the Lower Cambrian , 2007, Nature.

[72]  Nicholas H. Putnam,et al.  Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization , 2007, Science.

[73]  S. Jensen,et al.  A critical reappraisal of the fossil record of the bilaterian phyla. , 2007 .

[74]  D. Canfield,et al.  Late-Neoproterozoic Deep-Ocean Oxygenation and the Rise of Animal Life , 2007, Science.

[75]  D. Siveter,et al.  THE SYSTEMATICS AND PHYLOGENETIC RELATIONSHIPS OF VETULICOLIANS , 2007 .

[76]  J. Grotzinger,et al.  Oxidation of the Ediacaran Ocean , 2006, Nature.

[77]  M. Benton,et al.  Paleontological evidence to date the tree of life. , 2006, Molecular biology and evolution.

[78]  Marco Stampanoni,et al.  Cellular and Subcellular Structure of Neoproterozoic Animal Embryos , 2006, Science.

[79]  Maoyan Zhu,et al.  Advances in Cambrian stratigraphy and paleontology: Integrating correlation techniques, paleobiology, taphonomy and paleoenvironmental reconstruction , 2006 .

[80]  J. Mullikin,et al.  The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: evidence from the starlet sea anemone, Nematostella vectensis , 2006, Genome Biology.

[81]  C. Schander,et al.  A soft-bodied mollusc with radula from the Middle Cambrian Burgess Shale , 2006, Nature.

[82]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[83]  Justin P. Wright,et al.  The Concept of Organisms as Ecosystem Engineers Ten Years On: Progress, Limitations, and Challenges , 2006 .

[84]  E. Davidson,et al.  Gene Regulatory Networks and the Evolution of Animal Body Plans , 2006, Science.

[85]  N. Trewin,et al.  A HEXAPOD FROM THE EARLY DEVONIAN WINDYFIELD CHERT, RHYNIE, SCOTLAND , 2005 .

[86]  刘金明,et al.  IL-13受体α2降低血吸虫病肉芽肿的炎症反应并延长宿主存活时间[英]/Mentink-Kane MM,Cheever AW,Thompson RW,et al//Proc Natl Acad Sci U S A , 2005 .

[87]  Jean‐Bernard Caron Banffia constricta, a putative vetulicolid from the Middle Cambrian Burgess Shale , 2005, Transactions of the Royal Society of Edinburgh: Earth Sciences.

[88]  G. Narbonne THE EDIACARA BIOTA: Neoproterozoic Origin of Animals and Their Ecosystems , 2005 .

[89]  S. Jensen,et al.  Trace fossil preservation and the early evolution of animals , 2005 .

[90]  D. Shu,et al.  A new arthropod from the Chengjiang Lagerstätte, Early Cambrian, southern China , 2005 .

[91]  Kenneth M. Halanych,et al.  The New View of Animal Phylogeny , 2004 .

[92]  S. Thrush,et al.  Bioturbators enhance ecosystem function through complex biogeochemical interactions , 2004, Nature.

[93]  J. Baguñá,et al.  The dawn of bilaterian animals: the case of acoelomorph flatworms , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[94]  X. Hou,et al.  Evidence for a single median fin‐fold and tail in the Lower Cambrian vertebrate, Haikouichthys ercaicunensis , 2004, Journal of evolutionary biology.

[95]  Diying Huang,et al.  Early Cambrian sipunculan worms from southwest China , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[96]  G. Narbonne Modular Construction of Early Ediacaran Complex Life Forms , 2004, Science.

[97]  E. Davidson,et al.  Small Bilaterian Fossils from 40 to 55 Million Years Before the Cambrian , 2004, Science.

[98]  J. Bergström,et al.  THE LOWER CAMBRIAN CRUSTACEAN PECTOCARIS FROM THE CHENGJIANG BIOTA, YUNNAN, CHINA , 2004, Journal of Paleontology.

[99]  Mark A McPeek,et al.  Estimating metazoan divergence times with a molecular clock. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[100]  S. Porter Closing the Phosphatization Window: Testing for the Influence of Taphonomic Megabias on the Pattern of Small Shelly Fossil Decline , 2004 .

[101]  D. Waloszek,et al.  A new 'great-appendage' arthropod from the Lower Cambrian of China and homology of chelicerate chelicerae and raptorial antero-ventral appendages , 2004 .

[102]  D. Grazhdankin Patterns of distribution in the Ediacaran biotas: facies versus biogeography and evolution , 2004, Paleobiology.

[103]  M. Sutton,et al.  Computer reconstruction and analysis of the vermiform mollusc Acaenoplax hayae from the Herefordshire Lagerstätte (Silurian, England), and implications for molluscan phylogeny , 2004 .

[104]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[105]  Xiu-Qiang Wang,et al.  The first tunicate from the Early Cambrian of South China , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[106]  J. Grotzinger,et al.  Extinction of Cloudina and Namacalathus at the Precambrian-Cambrian boundary in Oman , 2003 .

[107]  B. Waggoner The Ediacaran Biotas in Space and Time1 , 2003, Integrative and comparative biology.

[108]  S. Bengtson Origins and Early Evolution of Predation , 2002 .

[109]  D. Waloszek,et al.  A Larval Sea Spider (Arthropoda: Pycnogonida) from the Upper Cambrian ‘orsten’ of Sweden, and the Phylogenetic Position of Pycnogonids , 2002 .

[110]  Yuan-long Zhao,et al.  Revision of the Cambrian discoidal animals Stellostomites eumorphus and Pararotadiscus guizhouensis from South China , 2002 .

[111]  H. Dartnall,et al.  Fossil Rotifers and the Early Colonization of an Antarctic Lake , 2001, Quaternary Research.

[112]  S. Carroll,et al.  Early animal evolution: emerging views from comparative biology and geology. , 1999, Science.

[113]  J. W. Valentine,et al.  Fossils, molecules and embryos: new perspectives on the Cambrian explosion. , 1999, Development.

[114]  A. Knoll,et al.  Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite , 1998, Nature.

[115]  J. Lawton,et al.  POSITIVE AND NEGATIVE EFFECTS OF ORGANISMS AS PHYSICAL ECOSYSTEM ENGINEERS , 1997 .

[116]  N. Butterfield Plankton ecology and the Proterozoic-Phanerozoic transition , 1997, Paleobiology.

[117]  S. Morris,et al.  A Pikaia-like chordate from the Lower Cambrian of China , 1996, Nature.

[118]  G. Shields,et al.  Integrated chemo- and biostratigraphic calibration of early animal evolution: Neoproterozoic–early Cambrian of southwest Mongolia , 1996, Geological Magazine.

[119]  A. Mccarthy Development , 1996, Current Opinion in Neurobiology.

[120]  K. Müller,et al.  'Orsten' type phosphatized soft-integument preservation and a new record from the Middle Cambrian Kuonamka Formation in Siberia , 1995 .

[121]  D. Walossek The Upper CambrianRehbachiella, its larval development, morphology and significance for the phylogeny of Branchiopoda and Crustacea , 1995, Hydrobiologia.

[122]  K. Müller,et al.  An exceptionally preserved parasitic arthropod, Heymonsicambria taylori n.sp. (Arthropoda incertae sedis: Pentastomida), from Cambrian – Ordovician boundary beds of Newfoundland, Canada , 1994 .

[123]  E. Landing Precambrian-Cambrian boundary global stratotype ratified and a new perspective of Cambrian time , 1994 .

[124]  G. Poinar,et al.  Fossil habrotrochid rotifers in Dominican amber , 1993, Experientia.

[125]  S. Bengtson,et al.  Predatorial Borings in Late Precambrian Mineralized Exoskeletons , 1992, Science.

[126]  J. Todd,et al.  The first fossil entoproct , 1992, Naturwissenschaften.

[127]  A. Seilacher Vendobionta and Psammocorallia: lost constructions of Precambrian evolution , 1992, Journal of the Geological Society.

[128]  K. Müller,et al.  Upper Cambrian stem-lineage crustaceans and their bearing upon the monophyletic origin of Crustacea and the position of Agnostus , 1990 .

[129]  G. Narbonne,et al.  The Placentian Series: appearance of the oldest skeletalized faunas in southeastern Newfoundland , 1989, Journal of Paleontology.

[130]  A. Seilacher Vendozoa: Organismic construction in the Proterozoic biosphere , 1989 .

[131]  J. W. Valentine,et al.  A COMPARATIVE STUDY OF DIVERSIFICATION EVENTS: THE EARLY PALEOZOIC VERSUS THE MESOZOIC , 1987, Evolution; international journal of organic evolution.

[132]  Jon Marks,et al.  Development as an evolutionary process: Edited by Rudolf A. Raff & Elizabeth C. Raff (1987) New York: Alan R. Liss, Inc. xiv and 329 pp. ISBN 0-8451-2207-X. $58.00 , 1987 .

[133]  B. Runnegar A molecular‐clock date for the origin of the animal phyla , 1982 .

[134]  Douglas H. Jones,et al.  Echiura from the Pennsylvanian Essex Fauna of northern Illinois , 1977 .

[135]  J. Warn Presumed myzostomid infestation of an Ordovician crinoid , 1974 .

[136]  F. Schram Pseudocoelomates and a nemertine from the Illinois Pennsylvanian , 1973 .

[137]  H. Pflug Systematik der jung-präkambrischen PetalonamaePflug 1970 , 1972 .

[138]  S. Goldhor Ecology , 1964, The Yale Journal of Biology and Medicine.

[139]  A. Gray,et al.  I. THE ORIGIN OF SPECIES BY MEANS OF NATURAL SELECTION , 1963 .

[140]  Robert Blair Vocci Geology , 1882, Nature.

[141]  James D. Schiffbauer,et al.  Quantifying the evolution of early life , 2011 .

[142]  T. Lowenstein,et al.  Microbial communities in fluid inclusions and long-term survival in halite , 2011 .

[143]  Philip C J Donoghue,et al.  The impact of the representation of fossil calibrations on Bayesian estimation of species divergence times. , 2010, Systematic biology.

[144]  G. Richards,et al.  The dawn of developmental signaling in the metazoa. , 2009, Cold Spring Harbor symposia on quantitative biology.

[145]  E. Davidson,et al.  An integrated view of precambrian eumetazoan evolution. , 2009, Cold Spring Harbor symposia on quantitative biology.

[146]  S. Xiao,et al.  On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota. , 2009, Trends in ecology & evolution.

[147]  P. Vickers-Rich,et al.  The Rise and Fall of the Ediacaran Biota , 2007 .

[148]  S. Charbonnier,et al.  The Early Cambrian origin of thylacocephalan arthropods , 2006 .

[149]  F. Maytag Evolution , 1996, Arch. Mus. Informatics.

[150]  G. Poinar,et al.  Earliest fossil nematode (Mermithidae) in cretaceous Lebanese amber , 1994 .

[151]  B. Ratcliff,et al.  Development as an Evolutionary Process , 1987, The Yale Journal of Biology and Medicine.

[152]  B. Runnegar Oxygen requirements, biology and phylogenetic significance of the late Precambrian worm Dickinsonia, and the evolution of the burrowing habit , 1982 .

[153]  Nicolas Lartillot,et al.  PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating , 2009, Bioinform..

[154]  Lethaia , 2022 .