The Cambrian Conundrum: Early Divergence and Later Ecological Success in the Early History of Animals
Abstract
Diverse bilaterian clades emerged apparently within a few million years during the early Cambrian, and various environmental, developmental, and ecological causes have been proposed to explain this abrupt appearance. A compilation of the patterns of fossil and molecular diversification, comparative developmental data, and information on ecological feeding strategies indicate that the major animal clades diverged many tens of millions of years before their first appearance in the fossil record, demonstrating a macroevolutionary lag between the establishment of their developmental toolkits during the Cryogenian [(850 to 635 million years ago (Ma)], and the later ecological success of metazoans during the Ediacaran (635 to 541 Ma) and Cambrian (541 to 488 Ma) periods. We argue that this diversification involved new forms of developmental regulation, as well as innovations in networks of ecological interaction within the context of permissive environmental circumstances.
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1
C. Darwin, On the Origin of Species by means of Natural Selection (John Murray, London, 1859).
2
Knoll A. H., Carroll S. B., Early animal evolution: Emerging views from comparative biology and geology. Science 284, 2129 (1999).
3
Valentine J. W., Jablonski D., Erwin D. H., Fossils, molecules and embryos: New perspectives on the Cambrian explosion. Development 126, 851 (1999).
4
Bowring S. A., et al., Geochronologic constraints of the chronostratigraphic framework of the Neoproterozoic Huqf Supergroup, Sultanate of Oman. Am. J. Sci. 307, 1097 (2007).
5
Landing E., Precambrian-Cambrian boundary global stratotype ratified and a new perspective of Cambrian time. Geology 22, 179 (1994).
6
S. Jensen, M. L. Droser, J. G. Gehling, in Neoproterozoic Geobiology and Paleobiology, S. Xiao, A. J. Kaufman, Eds. (Springer, Berlin, 2006), pp. 115–157.
7
Maloof A. C., et al., The earliest Cambrian record of animals and ocean geochemical change. Geol. Soc. Am. Bull. 122, 1731 (2010).
8
Kouchinsky A., et al., Chronology of early Cambrian biomineralization. Geol. Mag. 1 (2011).
9
Porter S. M., Closing the phosphotization window: Testing for the influence of taphonomic megabias on the pattern of small shelly fossil decline. Palaios 19, 178 (2004).
10
Erwin D. H., Valentine J. W., Sepkoski J. J., A comparative study of diversification events: The early Paleozoic versus the Mesozoic. Evolution 41, 1177 (1987).
11
Budd G. E., Jensen S., A critical reappraisal of the fossil record of the bilaterian phyla. Biol. Rev. Camb. Philos. Soc. 75, 253 (2000).
12
Runnegar B., A molecular-clock date for the origin of the animal phyla. Lethaia 15, 199 (1982).
13
Peterson K. J., et al., Estimating metazoan divergence times with a molecular clock. Proc. Natl. Acad. Sci. U.S.A. 101, 6536 (2004).
14
Peterson K. J., Cotton J. A., Gehling J. G., Pisani D., The Ediacaran emergence of bilaterians: Congruence between the genetic and the geological fossil records. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 1435 (2008).
15
Philippe H., et al., Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706 (2009).
16
Halanych K. M., The new view of animal phylogeny. Annu. Rev. Ecol. Syst. 35, 229 (2004).
17
Sperling E. A., Peterson K. J., Pisani D., Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Mol. Biol. Evol. 26, 2261 (2009).
18
Baguñà J., Riutort M., The dawn of bilaterian animals: The case of acoelomorph flatworms. Bioessays 26, 1046 (2004).
19
Hejnol A., Martindale M. Q., Acoel development supports a simple planula-like urbilaterian. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 1493 (2008).
20
Philippe H., et al., Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470, 255 (2011).
21
Love G. D., et al., Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457, 718 (2009).
22
Maloof A. C., et al., Probable animal body-fossils from pre-Marinoan limestones, South Australia. Nat. Geosci. 3, 653 (2010).
23
Putnam N. H., et al., Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86 (2007).
24
Knoll A. H., The multiple origins of complex multicellularity. Annu. Rev. Earth Planet. Sci. 39, 217 (2011).
25
Xiao S. H., Zhang Y., Knoll A. H., Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391, 553 (1998).
26
Chen J. Y., et al., Small bilaterian fossils from 40 to 55 million years before the cambrian. Science 305, 218 (2004).
27
Cohen P. A., Knoll A. H., Kodner R. B., Large spinose microfossils in Ediacaran rocks as resting stages of early animals. Proc. Natl. Acad. Sci. U.S.A. 106, 6519 (2009).
28
Hagadorn J. W., et al., Cellular and subcellular structure of neoproterozoic animal embryos. Science 314, 291 (2006).
29
Xiao S. H., Laflamme M., On the eve of animal radiation: Phylogeny, ecology and evolution of the Ediacara biota. Trends Ecol. Evol. 24, 31 (2009).
30
Seilacher A., Vendozoa: Organismic construction in the Proterozoic biosphere. Lethaia 22, 229 (1989).
31
Gehling J. G., The case for Ediacaran fossil roots to the metazoan tree. Mem. Geol. Soc. India 20, 181 (1991).
32
Waggoner B. M., The ediacaran biotas in space and time. Integr. Comp. Biol. 43, 104 (2003).
33
Narbonne G. M., Modular construction of early Ediacaran complex life forms. Science 305, 1141 (2004).
34
Sperling E. A., Peterson K. J., Laflamme M., Rangeomorphs, Thectardis (Porifera?) and dissolved organic carbon in the Ediacaran oceans. Geobiology 9, 24 (2011).
35
A. M. Bush, R. K. Bambach, D. H. Erwin, in Quantifying the Evolution of Early Life, M. Laflamme, J. D. Schiffbauer, S. Q. Dornbos, Eds. (Springer Science, 2011), pp. 111–133.
36
Bengtson S., Zhao Y., Predatorial borings in late Precambrian mineralized exoskeletons. Science 257, 367 (1992).
37
Amthor J. E., et al., Extinction of Cloudina and Namacalathus at the Precambrian-Cambrian boundary in Oman. Geology 31, 431 (2003).
38
Narbonne G. M., The Ediacara Biota: Neoproterozoic origin of animals and their ecosystems. Annu. Rev. Earth Planet. Sci. 33, 421 (2005).
39
Ivantsov A. Y., New reconstruction of Kimberella, problematic Vendian metazoan. Paleontol. J. 43, 601 (2009).
40
M. A. Fedonkin, A. Simonetta, A. Y. Ivantsov, in The Rise and Fall of the Ediacaran Biota, P. Vickers-Rich, P. Komarower, Eds. (Geological Society, London, 2007), pp. 157–179.
41
Sperling E. A., Vinther J., A placozoan affinity for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes. Evol. Dev. 12, 201 (2010).
42
Liu A. G., McIlroy D., Brasier M. D., First evidence for locomotion in the Ediacara biota from the 565 Ma Mistaken Point Formation, Newfoundland. Geology 38, 123 (2010).
43
Jensen S., Droser M. L., Gehling J. G., Trace fossil preservation and the early evolution of animals. Palaeogeogr. Palaeoclimatol. Palaeoecol. 220, 19 (2005).
44
J. W. Valentine, D. H. Erwin, in Development as an Evolutionary Process, R. A. Raff, Ed. (Liss, New York, 1987).
45
Grotzinger J. P., Fike D. A., Fischer W. W., Enigmatic origin of the largest-known carbon isotope excursion in Earth’s history. Nat. Geosci. 4, 285 (2011).
46
Shields-Zhou G., Och L., The case for a Neoproterozoic oxygenation event: Geochemical evidence and biological consequences. GSA Today 21, 4 (2011).
47
Fike D. A., Grotzinger J. P., Pratt L. M., Summons R. E., Oxidation of the Ediacaran ocean. Nature 444, 744 (2006).
48
Scott C., et al., Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452, 456 (2008).
49
Canfield D. E., Poulton S. W., Narbonne G. M., Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315, 92 (2007).
50
Runnegar B., Oxygen requirements, biology and phylogenetic significance of the late Precambrian worm Dickinsonia, and the evolution of burrowing habitat. Alcheringa 6, 223 (1982).
51
Erwin D. H., Early origin of the bilaterian developmental toolkit. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 2253 (2009).
52
Sebé-Pedrós A., de Mendoza A., Lang B. F., Degnan B. M., Ruiz-Trillo I., Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol. Biol. Evol. 28, 1241 (2011).
53
Richards G. S., Degnan B. M., The dawn of developmental signaling in the metazoa. Cold Spring Harb. Symp. Quant. Biol. 74, 81 (2009).
54
Srivastava M., et al., The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720 (2010).
55
Ryan J. F., et al., The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: Evidence from the starlet sea anemone, Nematostella vetensis. Genome Biol. 7, R64 (2006).
56
Davidson E. H., Erwin D. H., Gene regulatory networks and the evolution of animal body plans. Science 311, 796 (2006).
57
Davidson E. H., Erwin D. H., An integrated view of precambrian eumetazoan evolution. Cold Spring Harb. Symp. Quant. Biol. 74, 65 (2009).
58
Davidson E. H., Erwin D. H., Evolutionary innovation and stability in animal gene networks. J. Exp. Zool. B (Mol. Dev. Evol.) 314B, 182 (2010).
59
Makeyev E. V., Maniatis T., Multilevel regulation of gene expression by microRNAs. Science 319, 1789 (2008).
60
Peterson K. J., Dietrich M. R., McPeek M. A., MicroRNAs and metazoan macroevolution: Insights into canalization, complexity, and the Cambrian explosion. Bioessays 31, 736 (2009).
61
Marshall C. R., Valentine J. W., The importance of preadapted genomes in the origin of the animal bodyplans and the Cambrian explosion. Evolution 64, 1189 (2010).
62
Kalsotra A., Cooper T. A., Functional consequences of developmentally regulated alternative splicing. Nat. Rev. Genet. 12, 715 (2011).
63
D. H. Erwin, J. W. Valentine, The Cambrian Explosion: The Construction of Animal Biodiversity (Roberts, Greenwood, CO, 2012).
64
Butterfield N. J., Plankton ecology and the Proterozoic-Phanerozoic transition. Paleobiology 23, 247 (1997).
65
Losos J. B., Adaptive radiation, ecological opportunity, and evolutionary determinism. American Society of Naturalists E. O. Wilson award address. Am. Nat. 175, 623 (2010).
66
Jones C. G., Lawton J. H., Shachak M., Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78, 1946 (1997).
67
Wright J. P., Jones C. G., The concept of organisms as ecosystem engineers ten years on: Progress, limitations, and challenges. Bioscience 56, 203 (2006).
68
Erwin D. H., Macroevolution of ecosystem engineering, niche construction and diversity. Trends Ecol. Evol. 23, 304 (2008).
69
Lohrer A. M., Thrush S. F., Gibbs M. M., Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431, 1092 (2004).
70
Bengtson S., Origins and early evolution of predation. Paleontol. Soc. Pap. 8, 289 (2002).
71
Rota-Stabelli O., et al., A congruent solution to arthropod phylogeny: Phylogenomics, microRNAs and morphology support monophyletic Mandibulata. Proc. R. Soc. B 278, 298 (2011).
72
Campbell L. I., et al., MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda. Proc. Natl. Acad. Sci. U.S.A. 108, 15920 (2011).
73
Szaniawski H., New evidence for the protoconodont origin of chaetognaths. Acta Palaeontol. Pol. 47, 409 (2002).
74
J. J. Sepkoski Jr., A Compendium of Fossil Marine Animal Families (Milwaukee Public Museum Contributions in Biology and Geology, ed. 2, 1992), vol. 83, pp. 1–156.
75
Sepkoski J. J., A compendium of fossil marine animal genera. Bull. Am. Paleontol. 363, 1 (2002).
76
Li G. X., et al., Early Cambrian metazoan fossil record of South China: Generic diversity and radiation patterns. Palaeogeogr. Palaeoclimatol. Palaeoecol. 254, 229 (2007).
77
Babcock L. E., Peng S. C., Cambrian chronostratigraphy: Current state and future plans. Palaeogeogr. Palaeoclimatol. Palaeoecol. 254, 62 (2007).
78
Zhu M. Y., Babcock L. E., Peng S. C., Advances in Cambrian stratigraphy and paleontology: Integrating correlation techniques, paleobiology, taphonomy and paleoenvironmental reconstruction. Paleoworld 15, 217 (2006).
79
Edgecombe G. D., Arthropod phylogeny: an overview from the perspectives of morphology, molecular data and the fossil record. Arthropod Struct. Dev. 39, 74 (2010).
80
Sperling E. A., Pisani D., Peterson K. J., Molecular paleobiological insights into the origin of the Brachiopoda. Evol. Dev. 13, 290 (2011).
81
Mallatt J., Craig C. W., Yoder M. J., Nearly complete rRNA genes assembled from across the metazoan animals: Effects of more taxa, a structure-based alignment, and paired-sites evolutionary models on phylogeny reconstruction. Mol. Phylogenet. Evol. 55, 1 (2010).
82
E. A. Sperling, D. Pisani, K. J. Peterson, in The Rise and Fall of the Ediacaran Biota, P. Vickers-Rich, P. Komarower, Eds. (Geological Society, London, Special Publications, 2007), vol. 286, pp. 355–368.
83
Ronquist F., Huelsenbeck J. P., MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572 (2003).
85
Philippe H., et al., Resolving difficult phylogenetic questions: Why more sequences are not enough. PLoS Biol. 9, e1000602 (2011).
86
Sperling E. A., Robinson J. M., Pisani D., Peterson K. J., Where’s the glass? Biomarkers, molecular clocks, and microRNAs suggest a 200-Myr missing Precambrian fossil record of siliceous sponge spicules. Geobiology 8, 24 (2010).
87
Pick K. S., et al., Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol. Biol. Evol. 27, 1983 (2010).
88
Lartillot N., Lepage T., Blanquart S., PhyloBayes 3: A Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25, 2286 (2009).
89
Lepage T., Bryant D., Philippe H., Lartillot N., A general comparison of relaxed molecular clock models. Mol. Biol. Evol. 24, 2669 (2007).
90
Drummond A. J., Ho S. Y. W., Phillips M. J., Rambaut A., Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88 (2006).
91
Inoue J., Donoghue P. C., Yang Z., The impact of the representation of fossil calibrations on Bayesian estimation of species divergence times. Syst. Biol. 59, 74 (2010).
92
Seilacher A., Vendobionta and Psammocorallia: Lost constructions of Precambrian evolution. J. Geol. Soc. London 149, 607 (1992).
93
Laflamme M., Narbonne G. M., Ediacaran Fronds. Palaeogeogr. Palaeoclimatol. Palaeoecol. 258, 162 (2008).
94
M. A. Fedonkin et al., The Rise of Animals: Evolution and Diversification of the Kingdom Animalia (John Hopkins Press, Baltimore, 2007).
95
Shen B., Dong L., Xiao S., Kowalewski M., The Avalon explosion: Evolution of Ediacara morphospace. Science 319, 81 (2008).
96
Hofmann H. J., O’Brien S. J., King A. F., Ediacaran biota on Bonavista Peninsula, Newfoundland, Canada. J. Paleontol. 82, 1 (2008).
97
Grazhdankin D. V., Patterns of distribution in the Ediacaran biotas: Facies versus biogeography and evolution. Paleobiology 30, 203 (2004).
98
R. Richter, Die ältesten Fossilien Sud-Afrikas. Senckenberg lethaea 36, 243 (1955).
99
Pflug H. D., Systematik der jung-präikambrischen Petalonamae. Paläontologische Zeitschrift 46, 56 (1970).
100
M. F. Glaessner, in W. A. Berggren et al., Introduction, Fossilization (taphonomy) Biogeography and Biostratigraphy, Part A of R. C. Moore, Ed., Treatise on Invertebrate Paleontology (Geological Society of America, New York, and University of Kansas, Lawrence, 1979).
101
M. A. Fedonkin, in The Vendian System, vol. 1., Paleontology, B. S. Sokolov, A. B. Iwanowski, Eds. (Springer, New York, 1990), pp. 7–120, 132–137.
102
J. Reitner, G. Worheide, in Systema Porifera: A Guide to the Classification of Sponges, J. N. A. Hooper, R. W. M. Van Soest, Eds. (Kluwer Academic/Plenum, New York, 2002), pp. 52–68.
103
Reitner J., Coralline spongien: Der versuch einer phylogenetisch-taxonomischen analyse. Berl. Geowiss. Abh. Reihe E (Paläobiol.) 1, 1 (1992).
104
Kouchinsky A., Bengtson S., Feng W., Kutygin R., Val’kov A., The Lower Cambrian fossil anabaritids: Affinities, ocurrences and systematics. J. Syst. Palaeontology 7, 241 (2009).
105
Cartwright P., et al., Exceptionally preserved jellyfishes from the Middle Cambrian. PLoS ONE 2, e1121 (2007).
106
Swadling K., Dartnall H. J. G., Gibson J. A. E., Saulnier-Talbot É., Vincent W. F., Fossil rotifers and the early colonization of an Antarctic lake. Quat. Res. 55, 380 (2001).
107
Waggoner B. M., Poinar G. O., Fossil habrotrochid rotifers in Dominican amber. Cell. Mol. Life Sci. 49, 354 (1993).
108
Todd J. A., Taylor P. D., The first fossil entoproct. Naturwissenschaften 79, 311 (1992).
109
Landing E., Myrow P. M., Benus A. P., Narbonne G. M., The Placentian series: Appearance of the oldest skeletalized faunas in southeastern Newfoundland. J. Paleontol. 63, 739 (1989).
110
Skovsted C. B., Brock G. A., Paterson J. R., Holmer L. E., Budd G. E., The scleritome of Eccentrotheca from the Lower Cambrian of South Australia: Lophophorate affinities and implications for tommotid phylogeny. Geology 36, 171 (2008).
111
Skovsted C. B., Balthasar U., Brock G. A., Paterson J. R., The tommotiid Camenella reticulosa from the early Cambrian of South Australia: Morphology, scleritome reconstruction, and phylogeny. Acta Palaeontol. Pol. 54, 525 (2009).
112
L. E. Holmer, L. E. Popov, in Treatise on Invertebrate Paleontology, Part H, Brachiopoda, Revised, A. Williams, S. J. Carlson, C. H. C. Brunton, Eds. (Geological Society of America, Univ. of Kansas, Boulder, Lawrence, 2007), pp. 2580–2590.
113
Holmer L. E., Stolk S. P., Skovsted C. B., Balthasar U., Popov L., The enigmatic Early Cambrian Salanygolina–a stem group of rhynchonelliform chileate brachiopods? Palaeontology 52, 1 (2009).
114
Landing E., English A., Keppie J. D., Cambrian origin of all skeletonized metazoan phyla–discovery of Earth's oldest bryozoans (Upper Cambrian, southern Mexico). Geology 38, 547 (2010).
115
Caron J. B., Scheltema A., Schander C., Rudkin D., A soft-bodied mollusc with radula from the Middle Cambrian Burgess Shale. Nature 442, 159 (2006).
116
Sigwart J. D., Sutton M. D., Deep molluscan phylogeny: Synthesis of palaeontological and neontological data. Philos. Trans. R. Soc. Lond. B Biol. Sci. 274, 2413 (2007).
117
Sutton M. D., Briggs D. E. G., Siveter D. J., Siveter D. J., Computer reconstruction and analysis of the vermiform mollusc Acaenoplax hayae from the Herefordshire Lagerstätte (Silurian, England), and implications for molluscan phylogeny. Palaeontology 47, 293 (2004).
118
Smith M. R., Caron J. B., Primitive soft-bodied cephalopods from the Cambrian. Nature 465, 469 (2010).
119
Mutvei H., Zhang Y.-B., Dunca E., Late Cambrian plectronocerid nautiloids and their role in cephalopod evolution. Palaeontology 50, 1327 (2007).
120
Missarzhevsky V. V., The oldest skeletal fossils and stratigraphy of the Precambrian-Cambrian boundary beds. Trans. Geol. Inst. Russ. Acad. Sci. 443, 1 (1989).
121
Brasier M. D., Shields G., Kuleshov V. N., Zhegallo E. A., Integrated chemo- and biostratigraphic calibration of early animal evolution: Neoproterozoic-early Cambrian of southwest Mongolia. Geol. Mag. 133, 445 (1996).
122
Huang D.-Y., Chen J.-Y., Vannier J., Saiz Salinas J. I., Early Cambrian sipunculan worms from southwest China. Philos. Trans. R. Soc. Lond. B Biol. Sci. 271, 1671 (2004).
123
Vinther J., Van Roy P., Briggs D. E. G., Machaeridians are Palaeozoic armoured annelids. Nature 451, 185 (2008).
124
Conway Morris S., Peel J. S., New palaeoscolecidan worms from the Lower Cambrian: Sirius Passet, Latham Shale and Kinzers Shale. Acta Palaeontol. Pol. 55, 141 (2010).
125
Jones D., Thompson I., Echiura from the Pennsylvanian Essex Fauna of northern Illinois. Lethaia 10, 317 (1977).
126
Warn J., Presumed Myzostomid infestation of an Ordovician crinoid. J. Paleontol. 48, 506 (1974).
127
M. A. Wills, in The Fossil Record 2, M. J. Benton, Ed. (Chapman and Hall, London, 1993), chap. 15, p. 271.
128
Jansson I.-M., McLoughlin S., Vadja V., Early Jurassic annelid cocoons from eastern Australia. Alcheringa 32, 285 (2008).
129
Schram F. D., Pseudocoelomates and a nemertine from the Illinois Pennsylvanian. J. Paleontol. 47, 985 (1973).
130
Peel J. S., A corset-like fossil from the Cambrian Sirius Passet Lagerstatte of North Greenland and its implications for cycloneuralian evolution. J. Paleontol. 84, 332 (2010).
131
Poinar G. O., Acra A., Acra F., Earliest fossil nematode (Mermithidae) in Cretaceous Lebanese amber. Fundam. Appl. Nematol. 17, 475 (1994).
132
Chen J.-Y., Zhou G.-Q., Biology of the Chengjiang fauna. Bull. Nat. Mus. Nat. Sci. 10, 11 (1997).
133
Müller K. J., Walossek D., Zakharov A., 'Orsten' type phosphatized softintegument preservation and a new record from the Middle Cambrian Kuonamka Formation in Siberia. N. Jb. Geol. Palaeontol. Abh. 191, 101 (1995).
134
R. Bertolani, D. Grimaldi, in Studies on Fossils in Amber, with Particular Reference to the Cretaceous of New Jersey, D. Grimaldi, Ed. (Backhuys, Leiden, 2000), pp. 103–110.
135
Hou X. G., Bergstrom J., Arthropods of the Lower Cambrian Chengjiang fauna, Southwest China. Fossils Strata 45, 116 (1997).
136
Daley A. C., Peel J. S., A possible anomalocaridid from the Cambrian Sirius Passet Lagerstatte, North Greenland. J. Paleontol. 84, 352 (2010).
137
Zhang X. L., Shu D. G., A new arthropod from the Chengjiang lagerstatte, Early Cambrian, southern China. Alcheringa 29, 185 (2005).
138
J. A. Dunlop, P. A. Selden, in Arthropod Relationships, Systematics Association Special Volume 55, R. A. Fortey, R. Thomas, Eds. (Chapman and Hall, London, 1998), pp. 221–235.
139
Waloszek D., Dunlop J. A., A larval sea spider (Arthropoda: Pycnogonida) from the Upper Cambrian 'Orsten' of Sweden, and the phylogenetic position of pycnogonids. Palaeontology 45, 421 (2002).
140
Chen J., Waloszek D., Maas A., A new 'great appendage' arthropod from the Lower Cambrian of China and homology of chelicerate chelicerae and raptorial antero-ventral appendages. Lethaia 37, 3 (2004).
141
Van Roy P., et al., Ordovician faunas of Burgess Shale type. Nature 465, 215 (2010).
142
Hu S., et al., Diverse pelagic predators from the Chengjiang Lagerstatte and the establishment of modern-style pelagic ecosystems in the early Cambrian. Palaeogeogr. Palaeoclimatol. Palaeoecol. 254, 307 (2007).
143
Vannier J., et al., The Early Cambrian origin of the thylacocephalan arthropods. Acta Palaeontol. Pol. 51, 201 (2006).
144
Hou X. G., et al., Soft-part anatomy of the Early Cambrian bivalved arthropods Kunyangella and Kunmingella: Significance for the phylogenetic relationships of Bradoriida. Philos. Trans. R. Soc. Lond. B Biol. Sci. 277, 1835 (2010).
145
Waloszek D., Muller K. J., Upper Cambrian stem-lineage crustaceans and their bearing upon the monophyletic origin of Crustacea and the position of Agnostus. Lethaia 23, 409 (1990).
146
Hou X.-G., Bergstrom J., Hu G.-H., The Lower Cambrian crustacean Pectocaris from the Chengjiang Biota, Yunnan, China. J. Paleontol. 78, 700 (2004).
147
Zhang X. G., Siveter D. J., Waloszek D., Maas A., An epipodite-bearing crown-group crustacean from the Lower Cambrian. Nature 449, 595 (2007).
148
Brooks H. K., A crustacean from the Tesnus Formation (Pennsylvanian) of Texas. J. Paleontol. 29, 852 (1955).
149
Walossek D., The Upper Cambrian Rehbachiella, its larval development, morphology and significance for the phylogeny of Branchiopoda and Crustacea. Hydrobiologia 298, 1 (1995).
150
Walossek D., Repetski J., Muller K. J., An exceptionally preserved parasitic arthropod, Heymonsicambria taylori n. sp. (Arthropoda incertae cedis: Pentastomida), from Cambrian-Ordovician boundary beds of Newfoundland, Canada. Can. J. Earth Sci. 31, 1664 (1994).
151
Williams M., et al., The earliest ostracodes: The geological evidence. Palaeobiodiversity and Palaeoenvironments 88, 11 (2008).
152
Fayers S. R., Trewin N. H., A hexapod from the Early Devonian Windyfield Chert, Rhynie, Scotland. Palaeontology 48, 1117 (2005).
153
P. Greenslade, P. E. S. Whalley, in: Second International Seminar on Apterygota, R. Dallai, ed. (University of Siena, Siena, 1986), pp. 319-323.
154
Aldridge R. J., Xian-Guang H. O. U., Siveter D. A. V. I. D. J., Siveter D. E. R. E. K. J., Gabbott S. A. R. A. H. E., The systematics and phylogenetic relationships of vetulicolians. Palaeontology 50, 131 (2007).
155
Caron J. B., Banfifia constricta, a putative vetulicolid from the Middle Cambrian Burgess Shale. Trans. R. Soc. Edinb. Earth Sci. 96, 95 (2005).
156
Zhu M., Zhao Y., Chen J., Revision of the Cambrian discoidal animals Stellostomites eumorphus and Pararotadiscus guizhouensis from South China. Geobios 35, 165 (2002).
157
Caron J. B., Conway Morris S., Shu D., Tentaculate fossils from the Cambrian of Canada (British Columbia) and China (Yunnan) interpreted as primitive deuterostomes. PLoS ONE 5, e9586 (2010).
158
Hou X. G., et al., An early Cambrian hemichordate zooid. Curr. Biol. 21, 612 (2011).
159
Arduini P., Pinna G., Teruzzi G., Megaderaion sinemuriense n.g. n.sp., a new fossil enteropneust of the Sinemurian of Osteno in Lombardy. Atti Soc. It. Sci. Nat. Museo Milano 122, 462 (1981).
160
Zamora S., Middle Cambrian echinoderms from north Spain show echinoderms diversified earlier in Gondwana. Geology 38, 507 (2010).
161
Rahman I. A., Zamora S., The oldest cinctan carpoid (stem-group Echinodermata), and the evolution of the water vascular system. Zool. J. Linn. Soc. 157, 420 (2009).
162
Chen J.-Y., et al., The first tunicate from the Early Cambrian of South China. Proc. Natl. Acad. Sci. U.S.A. 100, 8314 (2003).
163
Shu D. G., Morris S. C., Zhang X. L., A Pikaia-like chordate from the Lower Cambrian of China. Nature 384, 157 (1996).
164
Zhang X.-G., Hou X.-G., Evidence for a single median fin-fold and tail in the Lower Cambrian vertebrate, Haikouichthys ercaicunensis. J. Evol. Biol. 17, 1162 (2004).
165
M. P. Smith, I. J. Sansom, K. D. Cochrane, in: Major Events in Early Vertebrate Evolution—Palaeontology, Phylogeny, Genetics, and Development, P. E. Ahlberg, Ed. (Systematics Association Special Volume, London, 2001), vol. 61, pp. 67–84
166
Gazave E., et al., No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera. Hydrobiologia (2011).
167
Neiber M. T., et al.Global Biodiversity and Phylogenetic Evaluation of Remipedia, Global biodiversity and phylogenetic evaluation of remipedia (crustacea). PLoS ONE 6, e19627 (2011).
168
Benton M. J., Donoghue P. C. J., Paleontological evidence to date the tree of life. Mol. Biol. Evol. 24, 26 (2007).
169
Maloof A. C., et al., Constraints on early Cambrian carbon cycling from the duration of the Nemakit-Daldynian-Tommotian boundary Delta 13C shift, Morocco. Geology 38, 623 (2010).
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Published In
Science
Volume 334 | Issue 6059
25 November 2011
25 November 2011
Copyright
Copyright © 2011, American Association for the Advancement of Science.
Submission history
Received: 9 June 2011
Accepted: 5 October 2011
Published in print: 25 November 2011
Acknowledgments
This work was supported by a NASA National Astrobiology Institute grant (D.H.E and K.J.P) supporting M.L., S.M.T., and E.A.S., and a Smithsonian Institution Fellowship (M.L). E.A.S is also supported by an Agouron Geobiology Fellowship. K.J.P. is also supported by the NSF. D.P. is supported by a Science Foundation Ireland Research Frontier Programme grant (08/RFP/EOB1595). All molecular analyses were performed with the computing infrastructures provided by the Irish Center for High End Computing and the National University of Ireland Maynooth High Performance Computing facility. All data used in the paper are included as files in the SOM. We appreciate technical assistance from L. Campbell and comments from P. Donoghue, G. Edgecombe, G. Narbonne, B. Runnegar, two anonymous reviewers, and the Bio 28 Class of Dartmouth College (2011).
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