Evolutionary Biology Origin and Early Evolution of Animals
by
Kevin J. Peterson
  • LAST REVIEWED: 19 May 2017
  • LAST MODIFIED: 13 January 2014
  • DOI: 10.1093/obo/9780199941728-0043

Introduction

Coming at the end of one of the most intensive glaciation periods in Earth history (glaciers at sea level on the equator!), the explosive rise of animals 530 million years ago is one of the few major events in the history of life that combines the evolution of novel developmental regulatory circuitry with the emergence of unique environmental circumstances. This “Cambrian explosion” is truly a remarkable event in the history of life, as the Earth’s biota went from an essentially static system billions of years in existence to the one we enjoy today, a dynamic and awesomely complex system that forever changed the Earth’s biota, and ultimately the Earth itself. Part of the intrigue with the Cambrian explosion is that numerous phyla with very distinct body plans (whether arthropod, annelid, mollusk, echinoderm, or chordate) arrive on the scene in a geological blink of the eye, with little or no warning of what is to come in rocks that predate this interval of time. The abruptness of the transition between the “Precambrian” to the Cambrian was apparent early on with the publication of Murchison’s The Silurian System (1839), and is still apparent today. Indeed, the abruptness of the explosion has only gotten more pronounced since Murchison’s time as more and more of the Earth’s geological record has been explored, and accurate and precise dates have been placed on many of these outcrops. The books and papers in this article highlight the multifarious nature of the origin and early evolution of animals, ranging from morphology, to phylogeny, to paleontology, to developmental biology, and even to geochemistry and molecular biology.

The Cambrian Explosion

As with most things in ecology and evolution, the first statement of the problem that the origin of animals had for modern evolutionary theory can be found in Darwin 1859. Since that time, though numerous “precambrian” forms were described, they were virtually all debunked in Cloud 1968, making the starkness of the Cambrian explosion very real. Runnegar 1982 in many ways defined the essence of the problem that the Cambrian explosion represents, and concluded, based on early molecular clock dates, that the Cambrian explosion likely represents the first appearance of fossils. In contrast, Budd and Jensen 2000 argued that bilaterians were not likely older than about 555 Ma, and thus the Cambrian explosion records the evolution of animals themselves and not just the first appearance of animal fossils. Gould 1989 also saw the Cambrian explosion as an evolutionary event. Erwin, et al. 2011, using a molecular clock, substantiated Runnegar’s general thesis by showing that the origin of bilaterian animals was nearly 200 million years before the Cambrian explosion itself. Nonetheless the explosion is still very real in terms of the ecological revolution that takes place (Erwin and Valentine 2013), a revolution that some, for example Knoll 2003, see as driven by the advent of relatively higher oxygen levels.

  • Budd, G. E., and S. Jensen. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biological Reviews of the Cambridge Philosophical Society 75:253–295.

    DOI: 10.1017/S000632310000548XSave Citation »Export Citation »E-mail Citation »

    Here, Budd and Jensen argue that in essence the Cambrian explosion simply reflects the origin of bilaterian animals themselves, but that the origin of the “body plans” of most phyla evolved later in geological time. Further, they argue that because the last common ancestor of bilaterians possessed coelom(s), the trace fossil record then constrains the age of this clade to younger than 555 Ma.

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    • Cloud, P. E. J. 1968. Pre-metazoan evolution and the origins of the Metazoa. In Evolution and environment. Edited by E. T. Drake, 1–72. New Haven, CT: Yale Univ. Press.

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      Preston Cloud, by rejecting numerous instances of purported Precambrian metazoan fossils, defined the problem of the Cambrian explosion by showing that authentic metazoan remains seemed restricted to Phanerozoic rocks.

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      • Darwin, C. 1859. On the origin of species. London: John Murray.

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        In chapter 9 (pp. 279–311) Darwin considers the known fossil record. He goes on to detail why the fossil record is likely incomplete, not preserving the ancestors of these animals. Then, using this insight, he addresses the problem of the Cambrian explosion (p. 306) and suggests that the ancestors of Cambrian animals swarmed the Precambrian seas but simply had not (yet) been found. Republished by Harvard Univ. Press, Cambridge, MA, 1964.

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        • Erwin, D. H., M. LaFlamme, S. M. Tweedt, E. A. Sperling, D. Pisani, and K. J. Peterson. 2011. The Cambrian conundrum: Early divergence and later ecological success in the early history of animals. Science 334:1091–1097.

          DOI: 10.1126/science.1206375Save Citation »Export Citation »E-mail Citation »

          Erwin, et al. present the latest molecular clock estimates for animal diversification and the newest compendium of the known fossil record calibrated to the current geochronological record. These authors suggest that because the origin of bilaterian metazoans predates the Cambrian explosion by tens of millions of years, the explosion must largely be the result of novel ecological interactions within permissive environmental circumstances.

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          • Erwin, D. H., and J. W. Valentine. 2013. The Cambrian explosion: The construction of animal biodiversity. Greenwood Village, CO: Roberts.

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            An outstanding treatment of the multifarious suite of problems and questions that constitute the research avenue that is the Cambrian explosion. For each of the sections in this article, the interested reader should also consult the specific chapter for a synthetic, up-to-date, and highly readable treatment.

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            • Gould, S. J. 1989. Wonderful life. New York and London: W. W. Norton.

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              Gould argues that the Cambrian was a special time in animal evolutionary history in that body plans were highly plastic, but quickly settled into relatively few major design themes, what we today call “phyla.” Further, Gould tackles the theme of “contingency,” such that if the tape of Earth’s history were rewound (the source of the title of the book), a different set of winners might populate the world’s oceans.

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              • Knoll, A. H. 2003. Life on a young planet. Princeton, NJ, and Oxford: Princeton Univ. Press.

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                Andy Knoll, one of the leading researchers on the Cambrian explosion and the evolution of life, places the Cambrian explosion in the context of Earth history and highlights many of the critical features about the explosion. A highly entertaining and informative read.

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                • Runnegar, B. 1982. The Cambrian explosion: Animals or fossils? Journal of the Geological Society of Australia 29:395–411.

                  DOI: 10.1080/00167618208729222Save Citation »Export Citation »E-mail Citation »

                  A masterly treatment of the metazoan fossil record: Runnegar defined the problem of the Cambrian explosion for the modern era and suggested that a sharp rise in the level of atmospheric oxygen played a crucial role in the appearance of animals.

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                  Metazoan Morphology and Phylogenetic Interrelationships

                  The pattern of metazoan interrelationships is particularly important as it sheds light on the acquisition of characters that come to almost “define” metazoan clades, in particular phyla and the higher-level groups like Bilateria, the intra- and inter-phylogenetic relationships of which are presented in Cracraft and Donoghue 2004. In particular, the evolution of coeloms is key, as coeloms (see Ruppert 1991) are found only in larger organisms, animals that are capable of leaving evidence of their existence in the form of trace fossils (see in particular Budd and Jensen 2000, cited under the Cambrian Explosion). The books Ax 1996, Brusca and Brusca 2002, The Microscopic Anatomy of Invertebrates series (Harrison and Ruppert 1991–1999), and Schmidt-Rhaesa 2007 present the interested reader with detailed discussions of metazoan anatomy, whereas Nielsen 2012 presents these morphological insights within a phylogenetic and highly personal context, and Valentine 2004 discusses animal morphology in light both the anatomical and the evolutionary record.

                  • Ax, P. 1996. Multicellular animals: A new approach to the phylogenetic order in nature. Berlin: Springer.

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                    A three-volume series that addresses the metazoan tree using morphological data in a precise cladistic framework.

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                    • Brusca, R. C., and G. J. Brusca. 2002. Invertebrates. Sunderland, MA: Sinauer.

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                      A highly readable text book on invertebrates.

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                      • Cracraft, J., and M. J. Donoghue. 2004. Assembling the tree of life. Oxford: Oxford Univ. Press.

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                        A collection of papers detailing what was known of life’s phylogeny as of 2004, paying particular attention to the metazoan tree of life.

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                        • Harrison, F. W., and E. E. Ruppert. 1991–1999. Microscopic anatomy of invertebrates. 15 vols. New York: Wiley-Liss.

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                          This series of books is the most detailed examination of the anatomy of invertebrates ever published.

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                          • Nielsen, C. 2012. Animal evolution: Interrelationships of the living phyla. 3d ed. Oxford: Oxford Univ. Press.

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                            An outstanding treatment of metazoan phylogeny in light of morphological data in particular, written from a highly personal perspective.

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                            • Ruppert, E. E. 1991. Introduction to the aschelminth phyla: A consideration of mesoderm, body cavities, and cuticle. In Microscopic anatomy of invertebrates. Vol. 4. Edited by F. W. Harrison and E. E. Ruppert, 1–17. New York: Wiley-Liss.

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                              The single best treatment of coeloms in relation to animal phylogeny and evolution.

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                              • Schmidt-Rhaesa, A. 2007. The evolution of organ systems. Oxford: Oxford Univ. Press.

                                DOI: 10.1093/acprof:oso/9780198566687.001.0001Save Citation »Export Citation »E-mail Citation »

                                A survey of the animal kingdom organ system by organ system by one of the most knowledgeable invertebrate zoologists in the world. An unusual but highly informative treatment of animal morphology and evolution.

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                                • Valentine, J. W. 2004. On the origin of phyla. Chicago and London: Univ. of Chicago Press.

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                                  A magisterial treatment of the morphology, fossil record, phylogeny, and evolution of the animal phyla.

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                                  Molecular Phylogenetics and Phylogenomics

                                  Starting with Field, et al. 1988, addressing the phylogenetic interrelationships among animals has largely become the domain of molecular systematics. Although Peterson and Eernisse 2001 showed that numerous clades recognized on the basis of morphology were confirmed with molecular data, some real surprises were in store, including the protostome affinity of brachiopods and other lophophorates (Halanych, et al. 1995), the grouping of nematodes with arthropods (Aguinaldo, et al. 1997), and the deuterostome affinity of acoel flatworms (Philippe, et al. 2011a), which is a highly contentious conclusion (Edgecombe, et al. 2011). The position of ctenophores (Dunn, et al. 2008) continues to be contentious as well (Philippe, et al. 2011b).

                                  • Aguinaldo, A. M. A., J. M. Turbeville, L. S. Linford, et al. 1997. Evidence for a clade of nematodes, arthropods and other molting animals. Nature 387:489–493.

                                    DOI: 10.1038/387489a0Save Citation »Export Citation »E-mail Citation »

                                    A seminal paper in the history of metazoan phylogenetics. The second of two papers from Lake and colleagues that reorganized the protostome side of the animal tree. Here, they erect the clade Ecdysozoa, which includes the arthropods, nematodes, and priapulids, plus their near relatives.

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                                    • Dunn, C. W., A. Hejnol, D. Q. Matus, et al. 2008. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 397:707–710.

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                                      Using a large phylogenomic data set, these authors recognized the standard division of bilaterians into three large clades, but also had some surprising results including the basal position of ctenophores below sponges on the animal tree of life.

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                                      • Edgecombe, G. D., G. Giribet, C. W. Dunn, et al. 2011. Higher-level metazoan relationships: Recent progress and remaining questions. Organisms, Diversity & Evolution 11:151–172.

                                        DOI: 10.1007/s13127-011-0044-4Save Citation »Export Citation »E-mail Citation »

                                        A recent review of the latest data on metazoan interrelationships especially in light of the torrent of data stemming from the phylogenomic revolution in molecular systematics.

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                                        • Field, K. G., G. J. Olsen, D. J. Lane, et al. 1988. Molecular phylogeny of the animal kingdom. Science 239:748–753.

                                          DOI: 10.1126/science.3277277Save Citation »Export Citation »E-mail Citation »

                                          The first study that attacked the problem of metazoan interrelationships from a molecular perspective.

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                                          • Halanych, K. M., J. D. Bacheller, A. M. A. Aguinaldo, S. M. Liva, D. M. Hillis, and J. A. Lake. 1995. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267:1641–1643.

                                            DOI: 10.1126/science.7886451Save Citation »Export Citation »E-mail Citation »

                                            The first of two papers from Jim Lake and colleagues that reorganized the protostome side of the bilaterian tree.

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                                            • Peterson, K. J., and D. J. Eernisse. 2001. Animal phylogeny and the ancestry of bilaterians: Inferences from morphology and 18S rDNA gene sequences. Evolution & Development 3:170–205.

                                              DOI: 10.1046/j.1525-142x.2001.003003170.xSave Citation »Export Citation »E-mail Citation »

                                              Peterson and Eernisse attack the problem of animal interrelationships from both a morphological and molecular perspective, highlighting areas of the tree that in accord, and discussing areas of the tree where there is discordance between the two data sets.

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                                              • Philippe, H., H. Brinkmann, R. R. Copley, et al. 2011a. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470:255–258.

                                                DOI: 10.1038/nature09676Save Citation »Export Citation »E-mail Citation »

                                                Using data from phylogenomics, mitochondrial sequences, and microRNAs, Philippe, et al. cogently argue that acoel flatworms, rather than representing a basal bilaterian group, are instead allied to the deuterostomes, likely the echinoderms and hemichordates.

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                                                • Philippe, H., H. Brinkmann, D. Lavrov, et al. 2011b. Resolving difficult phylogenetic questions: Why more sequences are not enough. PLoS Biology 9:e1000602.

                                                  DOI: 10.1371/journal.pbio.1000602Save Citation »Export Citation »E-mail Citation »

                                                  These authors pay particular attention to the base of the animal tree, the mono- versus paraphyly of sponges, the position of ctenophores, and the position of placozoans.

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                                                  Geochronology of the Neoproterozoic and Cambrian

                                                  As famously quipped by the eminent geologist Paul Hoffman, “No dates, no rates!” and thus in order to understand the dynamics of the Cambrian explosion, and ultimately its cause(s), an accurate and precise time scale needs to be developed. Amthor, et al. 2003; Bowring, et al. 1993; Condon, et al. 2005; Grotzinger, et al. 1995; Landing 1994; Landing, et al. 2000; and Martin, et al. 2000 are the key papers dating this critical time in Earth history, and Walker, et al. 2013 is the latest review of the geologic time scale. For a detailed discussion of the latest divisions of the Cambrian, see CHAPTER 2 (pp. 13–28) of Erwin and Valentine 2013 (cited under the Cambrian Explosion).

                                                  • Amthor, J. E., J. P. Grotzinger, S. Schröder, et al. 2003. Extinction of Cloudina and Namacalathus at the Precambrian-Cambrian boundary in Oman. Geology 31:431–434.

                                                    DOI: 10.1130/0091-7613(2003)031%3C0431:EOCANA%3E2.0.CO;2Save Citation »Export Citation »E-mail Citation »

                                                    The Precambrian-Cambrian boundary is precisely dated by these authors at 542.6 ± 0.3 Ma.

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                                                    • Bowring, S. A., J. P. Grotzinger, C. E. Isachsen, A. H. Knoll, S. M. Pelechaty, and P. Kolosov. 1993. Calibrating rates of early Cambrian evolution. Science 261:1293–1298.

                                                      DOI: 10.1126/science.11539488Save Citation »Export Citation »E-mail Citation »

                                                      The first paper that obtained accurate and precise geochronological constraints on the absolute age and rate of the Cambrian explosion.

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                                                      • Condon, D., M. Zhu, S. Bowring, W. Wang, A. Yang, and Y. Jin. 2005. U-Pb ages from the Neoproterozoic Doushantuo Formation, China. Science 308:95–98.

                                                        DOI: 10.1126/science.1107765Save Citation »Export Citation »E-mail Citation »

                                                        These authors date the beginning of the Ediacaran period to 635 Ma.

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                                                        • Grotzinger, J. P., S. A. Bowring, B. Z. Saylor, and A. J. Kaufman. 1995. Biostratigraphic and geochronologic constraints on early animal evolution. Science 270:598–604.

                                                          DOI: 10.1126/science.270.5236.598Save Citation »Export Citation »E-mail Citation »

                                                          Grotzinger, et al. document that most Ediacaran animals are no older than 549 Ma and some are as young as 543 Ma, essentially coincident with the Precambrian-Cambrian boundary. Further, in Namibia, the Precambrian-Cambrian boundary is younger than 543.3 and older than 539.4 Ma.

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                                                          • Landing, E. 1994. Precambrian-Cambrian boundary global stratotype ratified and a new perspective of Cambrian time. Geology 22:179–182.

                                                            DOI: 10.1130/0091-7613(1994)022%3C0179:PCBGSR%3E2.3.CO;2Save Citation »Export Citation »E-mail Citation »

                                                            Review of the Precambrian-Cambrian boundary, the stratotype, and its correlation to other sections. Makes the point that the early Cambrian radiation was a two-stage process with uppermost Precambrian trace producers replaced with Phanerozoic-aspect assemblages, and a subsequent appearance of diverse skeletalized metazoans.

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                                                            • Landing, E., S. A. Bowring, K. L. Davidek, A. W. A. Rushton, R. A. Fortey, and A. P. Wibledon. 2000. Cambrian-Ordovician boundary age and duration of the lowest Ordovician Tremadoc series based on U-Pb zircon dates from Avalonian Wales. Geological Magazine 137:485–494.

                                                              DOI: 10.1017/S0016756800004507Save Citation »Export Citation »E-mail Citation »

                                                              These authors date the Cambrian-Ordovician boundary at 489 Ma.

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                                                              • Martin, M. W., D. V. Grazhdankin, S. A. Bowring, D. A. D. Evans, M. A. Fedonkin, and J. L. Kirschvink. 2000. Age of Neoproterozoic bilaterian body and trace fossils, White Sea, Russia: Implications for metazoan evolution. Science 288:841–845.

                                                                DOI: 10.1126/science.288.5467.841Save Citation »Export Citation »E-mail Citation »

                                                                These authors date the age of Kimberella-containing deposits to 555 Ma.

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                                                                • Walker, J. D., J. W. Geissman, S. A. Bowring, and L. E. Babcock. 2013. The Geological Society of America geologic time scale. GSA Bulletin 125:259–272.

                                                                  DOI: 10.1130/B30712.1Save Citation »Export Citation »E-mail Citation »

                                                                  The geological time scale as of 2013.

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                                                                  The Macroscopic Body- and Trace-Fossil Record of the Ediacaran and Cambrian

                                                                  The proverbial “nuts and bolts” of the Cambrian explosion—so to speak—is the macrofossil record of the late Precambrian and the Cambrian. Long recognized by the first appearance of skeletonized forms—in particular trilobites—this explosive event is also seen in the trace fossil record, as first realized by Seilacher 1956 and further discussed in Bottjer, et al. 2000 and Jensen 2003, demonstrating that the event is more than just the advent of skeletons. When trace fossils first evolved is slightly contentious, but new research suggests that the oldest traces are older than 585 million years (Pecoits, et al. 2012). Briggs, et al. 1994 and Xian-guang, et al. 2004 offer book-length treatments of the two most famous Cambrian fossil deposits, the Burgess Shale and the Chengjiang Biota, respectively. Van Roy, et al. 2010 show that these animals, although largely the domain of the Cambrian, were also present in the Ordovician.

                                                                  • Bottjer, D. J., J. W. Hagadorn, and S. Q. Dornbos. 2000. The Cambrian substrate revolution. GSA Today 10:1–7.

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                                                                    These authors document the trace fossil record across the Precambrian-Cambrian boundary, and highlight the impact these trace-makers had on the world’s substrates. They argue that the appearance of macroscopic burrowers caused the demise of the microbial mats that so extensively covered benthic sediments during the Ediacaran.

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                                                                    • Briggs, D. E. G., D. H. Erwin, and F. J. Collier. 1994. The fossils of the Burgess Shale. Washington, DC, and London: Smithsonian Institution.

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                                                                      Book-length treatment of the famous Burgess Shale fossils placed into the context of the Cambrian radiation.

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                                                                      • Jensen, S. 2003. The Proterozoic and earliest Cambrian trace fossil record: Patterns, problems and perspectives. Integrative and Comparative Biology 43:219–228.

                                                                        DOI: 10.1093/icb/43.1.219Save Citation »Export Citation »E-mail Citation »

                                                                        An excellent review of the trace fossil record of the Precambrian-Cambrian transition.

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                                                                        • Pecoits, E., K. O. Konhauser, N. R. Aubet, et al. 2012. Bilaterian burrows and grazing behavior at >585 million years ago. Science 336:1693–1696.

                                                                          DOI: 10.1126/science.1216295Save Citation »Export Citation »E-mail Citation »

                                                                          If confirmed, these trace fossils would constitute the oldest occurrence of bilaterian trace fossils.

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                                                                          • Seilacher, A. 1956. Der Beginn des Kambriums als biologische Wende. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 103:155–180.

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                                                                            The original paper that shows that the trace fossil record supports a Cambrian explosion event as well, independent of the body fossil record. Indeed, it is the trace fossil record that is so informative, as it is separate from the confounding issues related to biomineralization and the evolution of skeletons.

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                                                                            • Van Roy, P., P. J. Orr, J. P. Botting, et al. 2010. Ordovician faunas of Burgess Shale type. Nature 465:215–218.

                                                                              DOI: 10.1038/nature09038Save Citation »Export Citation »E-mail Citation »

                                                                              These authors demonstrate Burgess Shale taxa in Early Ordovician rocks, suggesting that the disappearance of Burgess Shale taxa at the end of the Cambrian is due not to extinction, but instead to the near absence of suitable preservation.

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                                                                              • Xian-guang, H., R. J. Aldridge, J. Bergström, D. J. Siveter, and F. Xiang-Hong. 2004. The Cambrian fossils of Chengjiang, China: The flowering of early animal life. Malden, MA: Blackwell.

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                                                                                Book-length treatment of the famous Chengjiang Fossil Biota from the Early Cambrian of South China.

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                                                                                The Timing of Metazoan Diversification

                                                                                As Runnegar 1982 was the first to point out, testing the completeness of the known fossil record demands an independent proxy, and as reviewed by Smith and Peterson 2002, the development of the molecular “clock” provided exactly that, despite ultimately relying on the accuracy of the known fossil record (Benton, et al. 2009). Although numerous studies suggested that the origin and diversification of animals occurred nearly a billion years ago (see for example Wray, et al. 1996), the latest studies are more congruent with the known fossil record (Peterson and Butterfield 2005; Peterson, et al. 2008) and as Parfrey, et al. 2011 show simply part of a larger eukaryotic radiation.

                                                                                • Benton, M. J., P. C. J. Donoghue, and R. J. Asher. 2009. Calibrating and constraining molecular clocks. In The timetree of life. Edited by S. B. Hedges and S. Kumar, 35–86. Oxford: Oxford Univ. Press.

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                                                                                  An extensive discussion of the calibration of molecular clocks and a detailed discussion of specific metazoan calibration nodes for molecular clock studies

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                                                                                  • Parfrey, L. W., D. J. G. Lahr, A. H. Knoll, and L. A. Katz. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proceedings of the National Academy of Sciences USA 108:13624–13629.

                                                                                    DOI: 10.1073/pnas.1110633108Save Citation »Export Citation »E-mail Citation »

                                                                                    This paper places the metazoan diversification within the broader context of eukaryotic evolution.

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                                                                                    • Peterson, K. J., and N. J. Butterfield. 2005. Origin of the Eumetazoa: Testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proceedings of the National Academy of Sciences USA 102:9547–9552.

                                                                                      DOI: 10.1073/pnas.0503660102Save Citation »Export Citation »E-mail Citation »

                                                                                      Peterson and Butterfield argue that the appearance of predators in the fossil record is discernable by the appearance of anti-predatory structures, in this case spines in marine algae called acritarchs, which corresponds in time to when macroscopic but unmineralized grazers first appeared according to the molecular clock.

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                                                                                      • Peterson, K. J., J. A. Cotton, J. G. Gehling, and D. Pisani. 2008. The Ediacaran emergence of bilaterians: Congruence between the genetic and geologic fossil records. Philosophical Transactions of the Royal Society B: Biological Sciences 363:1435–1443.

                                                                                        DOI: 10.1098/rstb.2007.2233Save Citation »Export Citation »E-mail Citation »

                                                                                        These authors pay particular attention to the geologic and genetic fossil records, finding them largely concordant with one another, in stark contrast to many earlier molecular clock studies.

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                                                                                        • Runnegar, B. 1982. A molecular-clock date for the origin of the animal phyla. Lethaia 15:199–205.

                                                                                          DOI: 10.1111/j.1502-3931.1982.tb00645.xSave Citation »Export Citation »E-mail Citation »

                                                                                          The first molecular clock analysis specifically testing the adequacy of the geologic fossil record.

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                                                                                          • Smith, A. B., and K. J. Peterson. 2002. Dating the time of origin of major clades: Molecular clocks and the fossil record. Annual Review of Earth and Planetary Sciences 30:65–88.

                                                                                            DOI: 10.1146/annurev.earth.30.091201.140057Save Citation »Export Citation »E-mail Citation »

                                                                                            A review on the methodology and application of molecular clocks, with particular attention paid to the discordance between the geologic and genetic fossil records, specifically the origin of birds and mammals, and the origin of the animal phyla.

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                                                                                            • Wray, G. A., J. S. Levinton, and L. H. Shapiro. 1996. Molecular evidence for deep Precambrian divergences among metazoan phyla. Science 274:568–573.

                                                                                              DOI: 10.1126/science.274.5287.568Save Citation »Export Citation »E-mail Citation »

                                                                                              A seminal study. Although their estimates for metazoan divergences are now widely regarded as too deep in geological time, this was the study that reinvigorated the particulars of how to use molecules to estimate animal divergence times in the Precambrian.

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                                                                                              The Ediacaran Period and the Ediacara Macrobiota

                                                                                              The newest addition to the geological time scale, the Ediacaran period, is now properly defined (Knoll, et al. 2004) and long known to contain a curious assemblage of organisms, as detailed in Fedonkin, et al. 2007. This “Ediacara biota” has continually defied easy classification among the Recent biota (see, in particular, Seilacher 1989), but the latest surveys have suggested that it constitutes a polyphyletic assemblage of organisms, a few of which might be related to living animals including Kimberella (Fedonkin and Waggoner 1997). Of particular interest to current workers is the specific biology of these organisms, irrespective of taxonomic placement, especially as discussed in LaFlamme, et al. 2009; LaFlamme, et al. 2013; and Sperling, et al. 2010; how these organisms fed; and, as detailed in Narbonne 2005, the underlying ecological organization of these biotas.

                                                                                              • Fedonkin, M. A., J. G. Gehling, K. Grey, G. M. Narbonne, and P. Vickers-Rich. 2007. The rise of animals: Evolution and diversification of the kingdom Animalia. Baltimore: Johns Hopkins Univ. Press.

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                                                                                                A book-length treatment of the Ediacaran including its biota by the leading researchers on these organisms and this time period in Earth’s history.

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                                                                                                • Fedonkin, M. A., and B. M. Waggoner. 1997. The late Precambrian fossil Kimberella is a mollusc-like bilaterian organism. Nature 388:868–871.

                                                                                                  DOI: 10.1038/42242Save Citation »Export Citation »E-mail Citation »

                                                                                                  Virtually the only Ediacaran organism broadly accepted as a bilaterian metazoan.

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                                                                                                  • Knoll, A. H., M. R. Walter, G. M. Narbonne, and N. Christie-Blick. 2004. A new period for the geologic time scale. Science 305:621–622.

                                                                                                    DOI: 10.1126/science.1098803Save Citation »Export Citation »E-mail Citation »

                                                                                                    These authors announce the creation of the Ediacaran Period.

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                                                                                                    • LaFlamme, M., S. A. F. Darroch, S. M. Tweedt, K. J. Peterson, and D. H. Erwin. 2013. The end of the Ediacara biota: Extinction, biotic replacement, or Cheshire Cat? Gondwana Research 23:558–573.

                                                                                                      DOI: 10.1016/j.gr.2012.11.004Save Citation »Export Citation »E-mail Citation »

                                                                                                      These authors classify the Ediacara biota into thirteen groups, the majority of which are hypothesized to be monophyletic (see also Erwin, et al. 2011, cited under the Cambrian Explosion). This paper also addresses the extinction of the Ediacara biota in relation to the Cambrian explosion, and suggests that the demise of the biota was likely due to the indirect ecological impact metazoans had upon the Ediacarans.

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                                                                                                      • LaFlamme, M., S. Xiao, and M. Kowalewski. 2009. Osmotrophy in modular Ediacara organisms. Proceedings of the National Academy of Sciences USA 106:14438–14443.

                                                                                                        DOI: 10.1073/pnas.0904836106Save Citation »Export Citation »E-mail Citation »

                                                                                                        LaFlamme, et al. show that because of their high surface-to-volume relationship the primary feeding strategy of at least some Ediacaran organisms was likely osmotrophy, the feeding of dissolved organic matter directly via osmosis. This, as well as the observation that Ediacaran sponges might have fed in a similar manner (Sperling, et al. 2010), might have important implications for the oxygenation of the world’s deep oceans.

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                                                                                                        • Narbonne, G. M. 2005. The Ediacara biota: Neoproterozoic origin of animals and their ecosystems. Annual Review of Earth and Planetary Sciences 33:421–442.

                                                                                                          DOI: 10.1146/annurev.earth.33.092203.122519Save Citation »Export Citation »E-mail Citation »

                                                                                                          An outstanding review of the Ediacara biota paying particular attention to the ecology of the assemblages.

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                                                                                                          • Seilacher, A. 1989. Vendozoa: Organismic construction in the Proterozoic biosphere. Lethaia 22:229–239.

                                                                                                            DOI: 10.1111/j.1502-3931.1989.tb01332.xSave Citation »Export Citation »E-mail Citation »

                                                                                                            A must-read for anyone interested in the biology and phylogenetic affinities of Ediacara organisms. Although Seilacher argues that they constitute an extinct “kingdom”-level clade, most modern workers would argue that they are clearly a polyphyletic assemblage of a variety of different clades (see LaFlamme, et al. 2013). Nonetheless, this is the key paper that made the field rethink what it thought it knew about the late Precambrian macrobiota.

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                                                                                                            • Sperling, E. A., K. J. Peterson, and M. LaFlamme. 2010. Rangeomorphs, Thectardis (Porifera?) and dissolved organic carbon in the Ediacaran ocean. Geobiology 9:2–33.

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                                                                                                              These authors hypothesize that the enigmatic cone-shaped organism Thectardis is allied with modern sponges; if correct, this would suggest that the paleoecology of the Mistaken Point biota was dominated by sponges and rangeomorphs, organisms that are either known or hypothesized to feed in large part on dissolved organic carbon (DOC). If correct, then this provides a “draw-down” mechanism for labile DOC from the water to the seafloor.

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                                                                                                              • Xiao, S., and M. LaFlamme. 2009. On the eve of animal radiation: Phylogeny, ecology and evolution of the Ediacara biota. Trends in Ecology and Evolution 24:31–40.

                                                                                                                DOI: 10.1016/j.tree.2008.07.015Save Citation »Export Citation »E-mail Citation »

                                                                                                                Insightful reviews of the biota paying particular attention to the ecology of the assemblages.

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                                                                                                                Biomineralization and the Origin and Evolution of Animal Skeletons

                                                                                                                The Cambrian explosion was long recognized solely from the skeletal record of animals (Bengtson 1994), and indeed the earliest skeletonized forms appear right before the beginning of the Cambrian (Grotzinger, et al. 2000), complete with evidence of predatory bore holes (Bengtson and Zhao 1992). As documented by Kouchinsky, et al. 2012, skeletons appear quickly and seemingly quixotically during the Cambrian, but in fact the appearance of the types of animal skeletons appears to be related to seawater chemistry (Porter 2007), and indeed the authors of Peters and Gaines 2012 see major geological events playing a key role in the advent of animal skeletons. Nonetheless, why skeletons are so obviously absent from the Ediacaran and even the Cryogenian remains mysterious, and as Sperling, et al. 2010 documents, some types of animal skeletons should have been quite common during the late Precambrian.

                                                                                                                • Bengtson, S. 1994. The advent of animal skeletons. In Early life on Earth. Edited by S. Bengtson, 412–425. Nobel Symposium No. 84. New York: Columbia Univ. Press.

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                                                                                                                  An outstanding review on the evolution of skeletons.

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                                                                                                                  • Bengtson, S., and Y. Zhao. 1992. Predatorial borings in late Precambrian mineralized exoskeletons. Science 257:367–369.

                                                                                                                    DOI: 10.1126/science.257.5068.367Save Citation »Export Citation »E-mail Citation »

                                                                                                                    Reports the earliest occurrence of evidence of predation in one of the earliest known skeletal forms, consistent with the idea that skeletons evolved, at least in part, as defense against carnivory.

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                                                                                                                    • Grotzinger, J. P., W. A. Watters, and A. H. Knoll. 2000. Calcified metazoans in thrombolite-stromatolite reefs of the terminal Proterozoic Nama Group, Namibia. Paleobiology 26:334–359.

                                                                                                                      DOI: 10.1666/0094-8373(2000)026%3C0334:CMITSR%3E2.0.CO;2Save Citation »Export Citation »E-mail Citation »

                                                                                                                      The authors report on some of the oldest unequivocal animal skeletons.

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                                                                                                                      • Kouchinsky, A., S. Bengtson, B. Runnegar, C. Skovsted, M. Steiner, and M. Vendrasco. 2012. Chronology of early Cambrian biomineralization. Geological Magazine 149:221–251.

                                                                                                                        DOI: 10.1017/S0016756811000720Save Citation »Export Citation »E-mail Citation »

                                                                                                                        An outstanding review. These authors compile data on the first appearances of animals with mineralized skeletons with respect to the latest summarized herein with references to an improved carbon isotope stratigraphy and radiometric dating.

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                                                                                                                        • Peters, S. E., and R. R. Gaines. 2012. Formation of the “Great Unconformity” as a trigger for the Cambrian explosion. Nature 484:363–366.

                                                                                                                          DOI: 10.1038/nature10969Save Citation »Export Citation »E-mail Citation »

                                                                                                                          Peters and Gaines suggest that the “Great Unconformity”—a gap in the geological record between often Precambrian basement rock and Cambrian-aged deposits—caused, in part, the Cambrian explosion by affecting seawater chemistry, allowing for the utilization of calcium for the construction of mineralized skeletons.

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                                                                                                                          • Porter, S. M. 2007. Seawater chemistry and early carbonate biomineralization. Science 316:1302.

                                                                                                                            DOI: 10.1126/science.1137284Save Citation »Export Citation »E-mail Citation »

                                                                                                                            Porter relates the acquisition of major skeleton types and the choice of mineral used to the ambient seawater chemistry, such that skeletons that are made of aragonite evolved at the time when aragonite was precipitated, whereas skeletons that are made of calcite evolved at the time when calcite was precipitated.

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                                                                                                                            • Sperling, E. A., J. M. Robinson, D. Pisani, and K. J. Peterson. 2010. Where’s the glass? Biomarkers, molecular clocks, and microRNAs suggest a 200-Myr missing Precambrian fossil record of siliceous-sponge spicules. Geobiology 8:24–36.

                                                                                                                              DOI: 10.1111/j.1472-4669.2009.00225.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                              A molecular paleobiological analysis that suggests that sponge spicules must have evolved well before they appeared in the fossil record in the earliest Cambrian, highlighting the potential taphonomic issues surrounding the origin of animals and their skeletons.

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                                                                                                                              Geochemistry, Biology, and the Oxygenation of the World’s Oceans

                                                                                                                              The role oxygen plays in diversification is undeniable, as animals require oxygen for respiration and production of many essential proteins, including collagen. However, the exact role oxygen plays in this story is highly controversial. Some authors see oxygen as a primary driver of animal evolution (see in particular Knoll 2003, cited under the Cambrian Explosion, as well as Canfield, et al. 2006; Fike, et al. 2006; McFadden, et al. 2008), whereas others, including the authors of Butterfield 2009 and Erwin and Valentine 2013 (cited under the Cambrian Explosion), see oxygenation of the world’s oceans as likely a consequence of animal activities rather than a cause, specifically the pumping of water by sponges and the burrowing (and hence mixing) activities of worms; and Logan, et al. 1995 presents the linkage of the pelagos with the benthos via zooplankton. Maloof, et al. 2010 and Sahoo, et al. 2012 detail the pattern very precisely, and Sperling, et al. 2013 details what is likely the true importance of oxygen on animal evolution.

                                                                                                                              • Butterfield, N. J. 2009. Oxygen, animals and oceanic ventilation: An alternative view. Geobiology 7:1–7.

                                                                                                                                DOI: 10.1111/j.1472-4669.2009.00188.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                Butterfield cogently argues that the exploration of the pelagos by zooplankton starting in the early Cambrian linked the pelagic and benthic ecosystems, thus affecting the nature of the carbon cycle and ultimately the oxygenation of the world’s oceans. Further, he makes the argument that the geochemical perturbations that characterize the Neoproterozoic-Paleozoic transition might be more accurately interpreted a consequences rather than the cause of metazoan evolution.

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                                                                                                                                • Canfield, D. E., S. W. Poulton, and G. M. Narbonne. 2006. Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315:92–95.

                                                                                                                                  DOI: 10.1126/science.1135013Save Citation »Export Citation »E-mail Citation »

                                                                                                                                  These authors document a correlation between the advent of oxic waters and the first occurrence of macroscopic life soon after the Gaskiers glaciation event, and that these oxic waters allowed for the eventual appearance of bilaterians.

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                                                                                                                                  • Fike, D. A., J. P. Grotzinger, L. M. Pratt, and R. E. Summons. 2006. Oxidation of the Ediacaran ocean. Nature 444:744–747.

                                                                                                                                    DOI: 10.1038/nature05345Save Citation »Export Citation »E-mail Citation »

                                                                                                                                    Using high-resolution carbon isotope and sulfur isotope records from Oman that cover most of the Ediacaran period, these authors document that the ocean became increasingly oxygenated after the end of the Marinoan glaciation.

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                                                                                                                                    • Logan, Graham A., J. M. Hayes, G. B. Hieshima, and R. E. Summons. 1995. Terminal Proterozoic reorganization of biogeochemical cycles. Nature 376:53–56.

                                                                                                                                      DOI: 10.1038/376053a0Save Citation »Export Citation »E-mail Citation »

                                                                                                                                      A highly influential paper. Using distinctive carbon isotopic signatures, these authors identify an extended microbial reworking of primary productivity (phytoplankton) within the water column of Proterozoic-aged oceans, whereas in the Phanerozoic the introduction of zooplankton and—importantly—their fecal pellets resulted in the vertical export of carbon from the water to the sediment, effectively oxygenating the benthos.

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                                                                                                                                      • Maloof, A. C., S. M. Porter, J. L. Moore, et al. 2010. The earliest Cambrian record of animals and ocean geochemical change. GSA Bulletin 122:1731–1177.

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                                                                                                                                        An excellent review focusing on the geochemical record of the late Neoproterozoic–to–Cambrian transition, and the concomitant biological record. In particular, these authors present a new absolute timeline for first appearances of skeletal animals and for changes in the carbon, strontium, and redox chemistry of the ocean during the early Cambrian.

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                                                                                                                                        • McFadden, K. A., J. Huang, X. Chu, et al. 2008. Pulsed oxidation and biological evolution in the Ediacaran Doushantuo Formation. Proceedings of the National Academy of Sciences USA 105:3197–3202.

                                                                                                                                          DOI: 10.1073/pnas.0708336105Save Citation »Export Citation »E-mail Citation »

                                                                                                                                          These authors argue that the distribution of early Ediacaran eukaryotes likely tracked redox conditions, and that only after 551 Ma did evolution of oxygen-requiring taxa reach global distribution.

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                                                                                                                                          • Sahoo, S. K., N. J. Planavsky, B. Kendall, et al. 2012. Ocean oxygenation in the wake of the Marinoan glaciation. Nature 489:546–549.

                                                                                                                                            DOI: 10.1038/nature11445Save Citation »Export Citation »E-mail Citation »

                                                                                                                                            Sahoo, et al. report on redox-sensitive proxies from the Doushantuo formation of South China that suggest an early Ediacaran oxygenation event immediately in the aftermath of the Marinoan glaciation.

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                                                                                                                                            • Sperling, E. A., C. A. Frieder, A. V. Raman, P. R. Girguis, L. A. Levin, and A. H. Knoll. 2013. Oxygen, ecology, and the Cambrian radiation of animals. Proceedings of the National Academy of Sciences USA 110:13446–13451.

                                                                                                                                              DOI: 10.1073/pnas.1312778110Save Citation »Export Citation »E-mail Citation »

                                                                                                                                              Sperling, et al. demonstrate that low oxygen is linked to low proportions of carnivores in modern oceanic settings, whereas higher oxygen levels allow for more complex food webs.

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                                                                                                                                              Putative Metazoan Microfossil Record

                                                                                                                                              The Doushantuo Formation is famous for its presence of what appear to be fossils recording the earliest stages of embryonic development (Xiao, et al. 1998). However, more recent investigations into the ontogenetic process of this as-of-yet-undescribed organism suggest that whatever what was the final product of this embryonic trajectory was not descended from the last common ancestor of all living animals, and might instead be allied with protistians near the fungal-metazoan split (Hagadorn, et al. 2006; Huldtgren, et al. 2011). In addition to these unambiguous embryo fossils, a series of high-profile papers from J. Y. Chen and colleagues (Chen, et al. 2000; Chen, et al. 2004; Chen, et al. 2006) have recorded the highly contentious occurrences of metazoan embryos and larvae in the Doushantuo Formation of South China. However, careful studies, in particular Cunningham, et al. 2012, have concluded based on a careful reexamination of the fossils that the structures used to designate a bilaterian affinity are late diagenetic artifacts, and thus there are no convincing records of bilaterians in the Doushantuo microfossil assemblage.

                                                                                                                                              • Chen, J.-Y., D. J. Bottjer, E. H. Davidson, et al. 2006. Phosphatized polar lobe-forming embryos from the Precambrian of Southwest China. Science 312:1644–1646.

                                                                                                                                                DOI: 10.1126/science.1125964Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                Chen, et al. describe what they believe to be polar lobes in some Doshantuo embryos, suggesting then a spiralian affinity for these embryos.

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                                                                                                                                                • Chen, J.-Y., D. J. Bottjer, P. Oliveri, et al. 2004. Small bilaterian fossils from 40 to 55 million years before the Cambrian. Science 305:218–222.

                                                                                                                                                  DOI: 10.1126/science.1099213Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                  Chen, et al. describe Vernanimalcula, which they reconstruct as a bilaterian with paired coeloms and sense organs.

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                                                                                                                                                  • Chen, J., P. Oliveri, C.-W. Li, et al. 2000. Precambrian animal diversity: Putative phosphatized embryos from the Doushantuo Formation of China. Proceedings of the National Academy of Sciences USA 97:4457–4462.

                                                                                                                                                    DOI: 10.1073/pnas.97.9.4457Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                    Using serial sectioning, these authors argue for the occurrence of a variety of bilaterian forms contained within the Doshantuo deposits.

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                                                                                                                                                    • Cunningham, J. A., G.-W. Thomas, S. Bengtson, et al. 2012. Distinguishing geology from biology in the Ediacaran Doushantuo biota relaxes constraints on the timing of the origin of bilaterians. Proceedings of the Royal Society B: Biological Sciences 279:2369–2376.

                                                                                                                                                      DOI: 10.1098/rspb.2011.2280Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                      These authors demonstrate that the key structures used to identify Doushantuo bilaterians by Chen, et al. can be dismissed as late diagenetic artifacts.

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                                                                                                                                                      • Hagadorn, J. W., S. Xiao, P. C. J. Donoghue, et al. 2006. Cellular and subcellular structure of Neoproterozoic animal embryos. Science 314:291–294.

                                                                                                                                                        DOI: 10.1126/science.1133129Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                        Using scanning electron microscopy and X-ray computed tomography, these authors make the important observation that these embryos exhibit no evidence of epithelial organization, even in embryos composed of 1,000 cells. Thus, because gastrulation is a key embryonic character present among all living animals, these embryos probably lie outside of the metazoan “crown group.”

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                                                                                                                                                        • Huldtgren, T., J. A. Cunningham, C. Yin, et al. 2011. Fossilized nuclei and germination structures identify Ediacaran “animal embryos” as encysting protists. Science 334:1696–1699.

                                                                                                                                                          DOI: 10.1126/science.1209537Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                          Huldtgren, et al. conclude that based on the pattern of cleavage apparent in these fossils, these fossils are not the remains of metazoans or even embryos. Instead, they likely represent dispersal “spores” made by organisms that lie outside of the crown group Metazoa.

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                                                                                                                                                          • Xiao, S., Y. Zhang, and A. H. Knoll. 1998. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391:553–558.

                                                                                                                                                            DOI: 10.1038/35318Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                            Xiao, et al. document what they believe to be cleavage-stage embryos of bilaterians tens of millions of years before they make their first macroscopic appearance in the rock record.

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                                                                                                                                                            Disparity, Development, and Morphological Evolution

                                                                                                                                                            The appearance of metazoan fossils in the late Precambrian obviously necessitated that the developmental mechanisms necessary in order to build an animal had to already have been in place. Nonetheless, the specific role development plays in the Cambrian explosion, specifically with regard to the question of animal body plans (Davidson and Erwin 2006), their diversity (termed “disparity”) (Briggs, et al. 1992; Erwin 2007), and subsequent stability over the ensuing 500 million years (Erwin, et al. 1987; Valentine 1995), is an active and vibrant research area. Indeed, the study Webster 2007, on morphological variation in trilobites, has been linked to the gains of a new type of genetic regulator called microRNAs by Peterson, et al. 2009.

                                                                                                                                                            • Briggs, Derek E. G., Richard A. Fortey, and Mathew A. Wills. 1992. Morphological disparity in the Cambrian. Science 256:1670–1673.

                                                                                                                                                              DOI: 10.1126/science.256.5064.1670Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                              These authors show that the amount of measured disparity among recent arthropods is similar to that of the Burgess Shale, ostensibly refuting Gould’s thesis that disparity was highest in the Cambrian.

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                                                                                                                                                              • Davidson, E. H., and D. H. Erwin. 2006. Gene regulatory networks and the evolution of animal body plans. Science 311:796–800.

                                                                                                                                                                DOI: 10.1126/science.1113832Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                These authors explore the role gene regulatory networks have on the evolution of animal body plans.

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                                                                                                                                                                • Erwin, D. H. 2007. Disparity: Morphological pattern and developmental context. Palaeontology 50:57–73.

                                                                                                                                                                  DOI: 10.1111/j.1475-4983.2006.00614.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                  Probably the best review on the subject of disparity in the context of animal evolution.

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                                                                                                                                                                  • Erwin, D. H., J. W. Valentine, and J. J. J. Sepkoski. 1987. A comparative study of diversification events: The early Paleozoic versus the Mesozoic. Evolution 41:1177–1186.

                                                                                                                                                                    DOI: 10.2307/2409086Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                    A classic paper showing that the origins of most animal phyla occurred early in the evolutionary history of animals, whereas lower levels arise continually throughout geological time. This temporal asymmetry of higher taxon (e.g., phylum) originations versus lower taxonomic levels (e.g., orders) is one of the key problems understanding the uniqueness of the Cambrian explosion.

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                                                                                                                                                                    • Fortey, R. A., D. E. G. Briggs, and M. A. Wills. 1996. The Cambrian evolutionary “explosion”: Decoupling cladogenesis from morphological disparity. Biological Journal of the Linnean Society 57:13–33.

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                                                                                                                                                                      Fortey and colleagues suggest that the Cambrian explosion represents the independent increase in body size coupled with the advent of skeletons in numerous different animal clades. This paper provides an interesting contrast with Budd and Jensen 2000, cited under the Cambrian Explosion.

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                                                                                                                                                                      • Peterson, K. J., M. R. Dietrich, and M. A. McPeek. 2009. MicroRNAs and metazoan macroevolution: Insights into canalization, complexity, and the Cambrian explosion. Bioessays 31:736–747.

                                                                                                                                                                        DOI: 10.1002/bies.200900033Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                        These authors suggested that the continual acquisition of group of genes called microRNAs—genes that code for small non-coding RNAs—might explain Webster’s observation regarding the temporal asymmetry of developmental plasticity in trilobites (and other animals). Further, because of the role microRNAs might play in the evolution of new cell types, microRNAs might also be instrumental in the evolution of complexity as well.

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                                                                                                                                                                        • Valentine, J. W. 1995. Why no new phyla after the Cambrian? Genome and ecospace hypotheses revisited. Palaios 10:190–194.

                                                                                                                                                                          DOI: 10.2307/3515182Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                          Valentine addresses the potential mechanistic underpinnings of why the origins of phyla seem to be restricted to a certain interval of geologic time.

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                                                                                                                                                                          • Webster, M. 2007. A Cambrian peak in morphological variation within trilobite species. Science 317:499–502.

                                                                                                                                                                            DOI: 10.1126/science.1142964Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                            An important paper that demonstrates that trilobite morphology varied at higher levels in the Cambrian than it did at younger times, consistent with the idea that development gets “canalized” or constrained during evolution, making phenotypic outcomes more predictable and less variable.

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                                                                                                                                                                            The Metazoan Genome

                                                                                                                                                                            With the sequencing of the human genome, it was quickly realized that the evolutionary history of metazoans was also written in the DNA of every living animal, and sequencing the genomes of key taxa would shed insight into their early evolutionary history. Although numerous genomes have now been sequenced, the papers below detail this molecular record in some of these key taxa including the sponge Amphimedon (Srivastava, et al. 2010), the placozoan Tricoplax (Srivastava, et al. 2008), the cnidarians Nematostella (Putnam, et al. 2007) and Hydra (Chapman, et al. 2010), the lancelet Branchiostoma (Putnam, et al. 2008), the echinoderm Strongylocentrotus (the Sea Urchin Genome Sequencing Consortium), and three lophotrochozoan protostomes (the mollusk Lottia and the annelids Capitella and Helobdella, Simakov, et al. 2013), in relation to a near non-metazoan relative, the choanoflagellate Monosiga (King, et al. 2008).

                                                                                                                                                                            • Chapman, J. A., E. F. Kirkness, O. Simakov, et al. 2010. The dynamic genome of Hydra. Nature 464:592–596.

                                                                                                                                                                              DOI: 10.1038/nature08830Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                              The genome sequence of the hydrozoan Hydra magnipapillata, an important animal for studies in animal regeneration.

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                                                                                                                                                                              • King, N., M. J. Westobrook, S. L. Young, et al. 2008. The genome of the choanoflagellate Monisiga brevicollis and the origin of metazoans. Nature 451:783–788.

                                                                                                                                                                                DOI: 10.1038/nature06617Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                Monosiga is a member of the choanoflagellates, the group of protists most closely related to animals, so comparing the gene content and structure of animals in relation to Monosiga is informative about the early evolution of the animal genome. In particular, this study demonstrates the paucity of transcription factors and signaling molecules absent in the choanoflagellate genome but present in animal genomes.

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                                                                                                                                                                                • Putnam, N. H., T. Butts, D. E. K. Ferrier, et al. 2008. The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064–1071.

                                                                                                                                                                                  DOI: 10.1038/nature06967Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                  Putnam and colleagues reconstruct the gene complement and genomic organization of the last common chordate ancestor, as well as describe the two genome-wide duplications and subsequent reorganizations that characterize the vertebrate genome.

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                                                                                                                                                                                  • Putnam, N. H., M. Srivastava, U. Hellsten, et al. 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–94.

                                                                                                                                                                                    DOI: 10.1126/science.1139158Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                    A fascinating paper that shows the underlying genomic complexity of “simple” animals like the cnidarian Nematostella vectensis, whose genome shows more similarity with vertebrates than many other invertebrate genomes like fruit flies or nematode worms.

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                                                                                                                                                                                    • The Sea Urchin Genome Sequencing Consortium. 2006. The genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941–952.

                                                                                                                                                                                      DOI: 10.1126/science.1133609Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                      The genome sequence of the sea urchin, an important deuterostome model system.

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                                                                                                                                                                                      • Simakov, O., F. Marletaz, S. J. Cho, et al. 2013. Insights into bilaterian evolution from three spiralian genomes. Nature 493:526–531.

                                                                                                                                                                                        DOI: 10.1038/nature11696Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                        The genome sequences of the mollusk Lottia gigantea and two annelids, the polychaete Capitella teleta and the leech Helobdella robusta. Interestingly, these genomes are more similar to the sequenced deuterostome genomes and even to the basal metazoan genomes than they are to the other protostome “model-system” genomes like the fruit fly Drosophila melanogaster and the nematode worm Caenorhabditis elegans.

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                                                                                                                                                                                        • Srivastava, M., E. Begovic, J. Chapman, et al. 2008. The Trichoplax genome and the nature of placozoans. Nature 454:955–960.

                                                                                                                                                                                          DOI: 10.1038/nature07191Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                          These authors show that even the simplest animals like the placozoan Tricoplax have remarkably complex genomes.

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                                                                                                                                                                                          • Srivastava, M., O. Simakov, J. Chapman, et al. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726.

                                                                                                                                                                                            DOI: 10.1038/nature09201Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                            A remarkable paper that shows how an underlying complex genome does not lead in any obvious manner to complex morphology, as sponges are some of the simplest animals, but yet the genome of this one sponge is remarkably similar to other animal genomes in content, structure, and organization.

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                                                                                                                                                                                            Ecological Diversification across the Precambrian and Cambrian Boundary

                                                                                                                                                                                            As initially envisioned by Stanley 1973, the Cambrian explosion can be thought of as the evolution of marine ecology (Zhuravlev and Riding 2001), driven largely by the evolution of predation (i.e., animals eating other animals; see for example Bengtson 2004), which established multi-tiered and recursive food webs (Dunne, et al. 2008) and the invasion of novel ecological space (Bambach, et al. 2007), including both the pelgaos (Hu, et al. 2007; Vannier, et al. 2007) and the benthos (Dzik 2005), and ultimately drove adaptations like skeletons that result from interorganismal interactions.

                                                                                                                                                                                            • Bambach, R. K., A. M. Bush, and D. H. Erwin. 2007. Autecology and the filling of ecospace: Key metazoan radiations. Palaeontology 50:1–22.

                                                                                                                                                                                              DOI: 10.1111/j.1475-4983.2006.00611.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                              A fascinating paper that documents the growth in ecological structure across the Precambrian-Cambrian boundary including the appearance of predators, deep burrowers, and pelagic forms.

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                                                                                                                                                                                              • Bengtson, S. 2004. Origins and early evolution of predation. Paleontological Society Papers 8:289–317.

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                                                                                                                                                                                                An outstanding review on predation and its impact on early animal evolution.

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                                                                                                                                                                                                • Dunne, J. A., R. J. Williams, N. D. Martinez, R. A. Wood, and D. H. Erwin. 2008. Compilation and network analyses of Cambrian food webs. PLoS Biology 6:693–708.

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                                                                                                                                                                                                  These authors document that the architecture of Cambrian food webs were remarkably similar to modern marine food webs, despite the changes in the constituent taxa over the subsequent 500 million years, and thus much of the marine ecosystem complexity characterizing the modern fauna was in place by the late Early Cambrian independent of the species that actually constitute the webs at any given time.

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                                                                                                                                                                                                  • Dzik, J. 2005. Behavioral and anatomical unity of the earliest burrowing animals and the cause of the “Cambrian explosion.” Paleobiology 31:503–521.

                                                                                                                                                                                                    DOI: 10.1666/0094-8373(2005)031[0503:BAAUOT]2.0.CO;2Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                    Dzik suggests that like skeletons, burrowing represents a strategy that evolved in response to predation.

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                                                                                                                                                                                                    • Hu, S., M. Steiner, M. Zhu, et al. 2007. Diverse pelagic predators from the Chengjiang Lagerstätte and the establishment of modern-style pelagic ecosystems in the early Cambrian. Palaeogeography, Palaeoclimatology, Palaeoecology 254:307–316.

                                                                                                                                                                                                      DOI: 10.1016/j.palaeo.2007.03.044Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                      Hu, et al. review the fossil record of pelagic metazoans found in the Chengjiang deposits and highlight the fact that there was a complex trophic system containing possibly up to four trophic levels.

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                                                                                                                                                                                                      • Stanley, S. M. 1973. An ecological theory for the sudden origin of multicellular life in the late Precambrian. Proceedings of the National Academy of Sciences USA 70:1486–1489.

                                                                                                                                                                                                        DOI: 10.1073/pnas.70.5.1486Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                        This classic paper by Steve Stanley argues that the invention of marine ecology essentially caused the Cambrian explosion. For modern treatments of the role predators had in influencing the tempo and mode of animal evolution, see in particular the papers by Butterfield in the Macroevolutionary Transition from the Precambrian to the Phanerozoic.

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                                                                                                                                                                                                        • Vannier, J., M. Steiner, E. Renvoisé, S.-X. Hu, and J.-P. Casanova. 2007. Early Cambrian origin of modern food webs: Evidence from predator arrow worms. Proceedings of the Royal Society B: Biological Sciences 274:627–633.

                                                                                                                                                                                                          DOI: 10.1098/rspb.2006.3761Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                          These authors document the occurrence of chaetognaths in early Cambrian deposits and the importance of this discovery in light of the construction of modern food webs.

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                                                                                                                                                                                                          • Zhuravlev, A. Y., and R. Riding, eds. 2001. The ecology of the Cambrian radiation. New York: Columbia Univ. Press.

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                                                                                                                                                                                                            An edited volume containing numerous papers on various aspects of the ecology of the Cambrian explosion.

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                                                                                                                                                                                                            The Macroevolutionary Transition from the Precambrian to the Phanerozoic

                                                                                                                                                                                                            In a series of insightful papers, Nick Butterfield, in Butterfield 1997, Butterfield 2007, and Butterfield 2010, has detailed the macroevolution and macroecology associated with the Precambrian-Cambrian transition. In essence, the evolutionary and ecological “rules” changed with the appearance of animals, as animals and only animals can drive morphological arms races and thus change the tempo of evolution. These are “must-reads” for anyone interested in the Cambrian explosion and what it means for our understanding of the history of life.

                                                                                                                                                                                                            • Butterfield, N. J. 1997. Plankton ecology and the Proterozoic-Phanerozoic transition. Paleobiology 23:247–262.

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                                                                                                                                                                                                              Arguably the most perspicacious treatment of the Cambrian explosion. Butterfield argues that the evolution of the mesozooplankton was a key step in the eventual Cambrian explosion, as mesozooplankton is the key ecological link between phytoplankton and the larger macrozooplankton and nekton that characterizes the Phanerozoic.

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                                                                                                                                                                                                              • Butterfield, N. J. 2007. Macroevolution and macroecology through deep time. Palaeontology 50:41–55.

                                                                                                                                                                                                                DOI: 10.1111/j.1475-4983.2006.00613.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                A review of Butterfield’s ideas where he documents the importance of the Ediacaran Period as the geological time in Earth history when the “rules” of evolution changed.

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                                                                                                                                                                                                                • Butterfield, N. J. 2010. Animals and the invention of the Phanerozoic Earth system. Trends in Ecology and Evolution 26:81–87.

                                                                                                                                                                                                                  DOI: 10.1016/j.tree.2010.11.012Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                  A highly readable review of Butterfield’s ideas and insights.

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                                                                                                                                                                                                                  The Ordovician Radiation

                                                                                                                                                                                                                  Although the Cambrian explosion is “over” by end of the early Cambrian, significant ecological innovations continue to occur, not least the continued exploration of the planktonic and nektonic realm by animals, and the origins of benthic suspension feeders. This primarily occurs in the late Cambrian into the Early Ordovician, and Droser and Finnegan 2003; Servais, et al. 2008; Servais, et al. 2010; and Webby, et al. 2004 expertly detail these profound ecological advancements.

                                                                                                                                                                                                                  • Droser, M. L., and S. Finnegan. 2003. The Ordovician radiation: A follow-up to the Cambrian explosion? Integrative and Comparative Biology 43:178–118.

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                                                                                                                                                                                                                    Droser and Finnegan focus in particular on the diversity-level dynamics of the Ordovician radiation and address the interesting question of whether Ordovician radiation is an extension of the Cambrian explosion or instead is a unique evolutionary event.

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                                                                                                                                                                                                                    • Servais, T., O. Lehnert, J. Li, et al. 2008. The Ordovician Biodiversification: Revolution in the oceanic trophic chain. Lethaia 41:99–109.

                                                                                                                                                                                                                      DOI: 10.1111/j.1502-3931.2008.00115.xSave Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                      This review pays particular attention to the ecological ramifications that occurred in the world’s pelagic realm in relation to the benthic biota.

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                                                                                                                                                                                                                      • Servais, T., A. W. Owen, D. A. T. Harper, B. Kröger, and A. Munnecke. 2010. The Great Ordovician Biodiversification Event (GOBE): The palaeoecological dimension. Palaeogeography, Palaeoclimatology, Palaeoecology 294:99–119.

                                                                                                                                                                                                                        DOI: 10.1016/j.palaeo.2010.05.031Save Citation »Export Citation »E-mail Citation »

                                                                                                                                                                                                                        An outstanding review of the Ordovician radiation that places the profound ecological changes that occurred during this interval in the context of Earth history.

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                                                                                                                                                                                                                        • Webby, B. D., F. Paris, M. L. Droser, and I. G. Percival. 2004. The Great Ordovician Biodiversification Event. New York: Columbia Univ. Press.

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                                                                                                                                                                                                                          A book-length treatment of the Ordovician radiation.

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