DOI: 10.1126/science.1206375, 1091 (2011);334 Science
et al.Douglas H. ErwinSuccess in the Early History of AnimalsThe Cambrian Conundrum: Early Divergence and Later Ecological
This copy is for your personal, non-commercial use only.
clicking here.colleagues, clients, or customers by , you can order high-quality copies for yourIf you wish to distribute this article to others
here.following the guidelines
can be obtained byPermission to republish or repurpose articles or portions of articles
): September 18, 2012 www.sciencemag.org (this information is current as of
The following resources related to this article are available online at
http://www.sciencemag.org/content/334/6059/1091.full.htmlversion of this article at:
including high-resolution figures, can be found in the onlineUpdated information and services,
http://www.sciencemag.org/content/suppl/2011/11/22/334.6059.1091.DC1.html can be found at: Supporting Online Material
can berelated to this article A list of selected additional articles on the Science Web sites
http://www.sciencemag.org/content/334/6059/1091.full.html#ref-list-1, 50 of which can be accessed free:cites 149 articlesThis article
http://www.sciencemag.org/content/334/6059/1091.full.html#related-urls3 articles hosted by HighWire Press; see:cited by This article has been
subject collections:This article appears in the following
registered trademark of AAAS. is aScience2011 by the American Association for the Advancement of Science; all rights reserved. The title
CopyrightAmerican Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by theScience
The Cambrian Conundrum: EarlyDivergence and Later EcologicalSuccess in the Early History of AnimalsDouglas H. Erwin,1,2* Marc Laflamme,1 Sarah M. Tweedt,1,3 Erik A. Sperling,4
Davide Pisani,5 Kevin J. Peterson6*
Diverse bilaterian clades emerged apparently within a few million years during the earlyCambrian, and various environmental, developmental, and ecological causes have been proposedto explain this abrupt appearance. A compilation of the patterns of fossil and moleculardiversification, comparative developmental data, and information on ecological feeding strategiesindicate that the major animal clades diverged many tens of millions of years before theirfirst appearance in the fossil record, demonstrating a macroevolutionary lag between theestablishment of their developmental toolkits during the Cryogenian [(850 to 635 million yearsago 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 formsof developmental regulation, as well as innovations in networks of ecological interaction withinthe context of permissive environmental circumstances.
When Charles Darwin published TheOrigin of Species (1), the sudden ap-pearance of animal fossils in the rockrecord was one of the more troubling facts hewas compelled to address. He wrote: There isanother and allied difficulty, which is muchgraver. I allude to the manner in which numbersof species of the same group, suddenly appear inthe lowest known fossiliferous rocks (p. 306).Darwin argued that the incompleteness of thefossil record gives the illusion of an explosiveevent, but with the eventual discovery of olderand better-preserved rocks, the ancestors ofthese Cambrian taxa would be found. Studiesof Ediacaran and Cambrian fossils continue toexpand the morphologic variety of clades, butthe appearance of the remains and traces of bi-laterian animals in the Cambrian remains abrupt(Fig. 1 and tables S1 and S2).
The fossil record is now supplemented withgeochemical proxies of environmental change; aprecise temporal framework allowing for cor-relation of rocks in different areas of the worldand evaluation of rates of evolutionary and envi-ronmental change; an increasingly rigorous un-derstanding of the phylogenetic relationships
between various living and fossil metazoan cladesand their dates of origin, based largely on mo-lecular sequences; and growing knowledge ofthe evolution of developmental processes throughcomparative studies of living groups. Collectively,these records allow an understanding of the en-vironmental potential, genetic and developmentalpossibility, and ecological opportunity that ex-isted before and during the Cambrian. Here, weprovide an updated synthesis (2, 3) of theserecords and thereby a macroevolutionary frame-work for understanding the Cambrian explosion.
Pattern of Animal DiversificationThe Cambrian fossil record. The beginning ofthe Cambrian Period dated at 541 T 0.13 millionyears ago (Ma) (4) is defined by the first appear-ance of the trace fossil Treptichnus pedum (5) inthe rock record, representing the first appearanceof bilaterian animals with the ability to makecomplex burrows both horizontally (Fig. 2A)and vertically (6). The earliest skeletal fossils oc-cur in the latest Ediacaran, but the first appear-ance of an array of plates, spines, shells, and otherskeletal elements of bilaterian affinity begins dur-ing the early Cambrian Fortunian Stage (541to ~530 Ma) (7, 8) (Fig. 3). Most of these aredisarticulated elements larger than 2 mm in size,but some complete scleritomes (Fig. 2B) havebeen recovered. They reveal a fauna with con-siderable morphologic and phylogenetic diver-sity and are collectively referred to as the smallshelly fauna (SSF). The earliest SSF are largelyof lophotrochozoan affinities; only in CambrianStage 3 do biomineralized ecdysozoans and deu-terostomes appear (8).Many of the SSF elementsare preserved as phosphate minerals, and theirdiversity peaks in abundant phosphate depos-
its (9). Although Ediacaran phosphate depos-its are common, they lack SSF, suggesting thatbilaterian clades acquired skeletons during theCambrian.
The pattern seen from the skeletal and tracefossil record is mirrored by soft-bodied fossilsfound in exceptionally preserved Cambrian fau-nas in China, Greenland, Australia, Canada (Fig.2C), and elsewhere. Although many new groupshave been described over the past decade, thepattern of diversification of both body fossilsand trace fossils has remained largely robust: Arecompilation (SOM text 1 and table S1) of thefirst occurrences of all metazoan phyla, classes,and stem-classes (extinct clades) of equivalentmorphologic disparity (Fig. 2, D and E) showstheir first occurrences in the latest Ediacaran(by 555 Ma), with a dramatic rise over about25 million years in the first several stages of theCambrian, and continuing into the Ordovician(Figs. 1 and 3 and table S3). However, from theearly Paleozoic onward there is little addition ofnew phyla and classes (Fig. 1), and those thatare added are largely artifactual, as they repre-sent occurrences of taxa with little or no pres-ervation potential (10).
The molecular record. Given the clear sig-nal for an explosive appearance of animal fos-sils in the early Cambrian (Figs. 1 and 3), mostpaleontologists favor a near literal reading ofthe fossil record, supporting a rapid (~25-million-year) evolutionary divergence of most animalclades near the base of the Cambrian [e.g., (11)].But teasing apart the mechanisms underlyingthe Cambrian explosion requires disentanglingevolutionary origins from geological first ap-pearances, and the only way to separate the twois to use a molecular clock (12). Many earlierproblems with molecular divergence estimateshave been addressed, allowing confident esti-mates of the robustness of the known geologicrecord (13, 14).
Building upon a previously assembled dataset (14) and a generally accepted phylogenetictree, we estimated divergence times for >100species of animals (alignment available as data-base S1), encompassing all major metazoan clades(Fig. 1, SOM text 2, table S4, figs. S1 to S4, anddatabase S2). Although much of the topologyis well accepted, including the tripartite divisionof bilaterians into lophotrochozoans, ecdysozoans,and deuterostomes and the paraphyletic nature ofdiploblasts with respect to triploblasts (1517),the paraphyletic nature of sponges is more con-troversial (15, 17). However, the estimated di-vergence times (SOM text and figs. S5 to S10)do not depend on this presumption; they are alsorobust to the choice of the root prior, the molec-ular clock model, subsampling of the calibrationpoints, and relaxation of the bounds of the cali-bration point intervals themselves (table S4). Al-though acoelomorphs have figured prominentlyin discussions about the reconstruction of ances-tral bilaterians (18, 19), they are not included in
1Department of Paleobiology, MRC-121, National Museumof Natural History, Post Office Box 37012, Washington, DC200137012, USA. 2Santa Fe Institute, 139