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Trilobite Evolutionary Rates Constrain the Duration of the Cambrian Explosion

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Trilobite Evolutionary Rates Constrain the Duration of the Cambrian Explosion Trilobite evolutionary rates constrain the duration of the Cambrian explosion John R. Patersona,1, Gregory D. Edgecombeb, and Michael S. Y. Leec,d aPalaeoscience Research Centre, School of Environmental & Rural Science, University of New England, Armidale, NSW 2351, Australia; bDepartment of Earth Sciences, The Natural History Museum, London SW7 5BD, United Kingdom; cCollege of Science and Engineering, Flinders University, SA 5001, Australia; and dEarth Sciences Section, South Australian Museum, Adelaide, SA 5000, Australia Edited by Andrew H. Knoll, Harvard University, Cambridge, MA, and approved January 9, 2019 (received for review November 12, 2018) Trilobites are often considered exemplary for understanding the phenotypic and genomic evolution (7, 8). Rapid morphological Cambrian explosion of animal life, due to their unsurpassed di- and molecular evolution during the earliest Cambrian almost versity and abundance. These biomineralized arthropods appear certainly underpinned the pronounced pulses of origination and abruptly in the fossil record with an established diversity, phyloge- diversification throughout the Terreneuvian (3, 9, 10). However, netic disparity, and provincialism at the beginning of Cambrian the question remains as to when evolutionary rates slowed to Series 2 (∼521 Ma), suggesting a protracted but cryptic earlier his- Phanerozoic norms, thus marking the end of the Cambrian ex- tory that possibly extends into the Precambrian. However, recent plosion. For instance, the calibrations used in ref. 7 were mostly analyses indicate elevated rates of phenotypic and genomic evolu- 488 Ma or younger; that analysis therefore only had weak power tion for arthropods during the early Cambrian, thereby shortening to constrain fast early rates further back than that time point. the phylogenetic fuse. Furthermore, comparatively little research Indirect measures using trends in animal diversity and disparity has been devoted to understanding the duration of the Cambrian suggest that rates were elevated throughout the early Cambrian explosion, after which normal Phanerozoic evolutionary rates were (3, 9, 10), but no study has yet quantified rates of evolution established. We test these hypotheses by applying Bayesian tip- across a broad selection of Cambrian lineages using direct phe- dating methods to a comprehensive dataset of Cambrian trilobites. notypic information from the fossil record. We show that trilobites have a Cambrian origin, as supported by the Trilobites are a diverse and abundant clade of biomineralized trace fossil record and molecular clocks. Surprisingly, they exhibit crown-group euarthropods that best exemplify the disjunct be- constant evolutionary rates across the entire Cambrian, for all as- tween the Cambrian rock record and any expected gradualist pects of the preserved phenotype: discrete, meristic, and continuous history of a clade before its first appearance as fossils. The oldest morphological traits. Our data therefore provide robust, quantita- – tive evidence that by the time the typical Cambrian fossil record trilobite body fossils around the world, at or near the Terreneuvian begins (∼521 Ma), the Cambrian explosion had already largely con- Cambrian Series 2 boundary (ca. 521 Ma), already show established cluded. This suggests that a modern-style marine biosphere had diversity, phylogenetic disparity, and biogeographic provincialism – rapidly emerged during the latest Ediacaran and earliest Cambrian (11 13). This, among other evidence, has been used to suggest that – (∼20 million years), followed by broad-scale evolutionary stasis trilobites had a much earlier, Precambrian origin (e.g., refs. 14 16). throughout the remainder of the Cambrian. In fact, Darwin (2) chose trilobites as an exemplar group to high- light his dilemma about animal origins: “There is another and allied Cambrian explosion | evolutionary rates | trilobites | Bayesian tip-dating | difficulty, which is much graver. I allude to the manner in which morphological clock Significance he abrupt first appearance of a multitude of animal fossils in Tearly Cambrian rocks (Terreneuvian to Series 2; ca. 541– The Cambrian explosion was arguably the most important bi- 509 Ma) epitomizes one of the most significant evolutionary ological event after the origin of life. Extensive research has events in Earth’s history (1). This sudden burst of diversity and been devoted to understanding when it began but far less on abundance across most eumetazoan (especially bilaterian) phyla when this burst of evolution ended. We present a quantitative over a relatively short geologic time span, and lack of obvious study that addresses these issues, using a large new dataset of Precambrian precursors, poses a conundrum when attempting to Cambrian trilobites, the most abundant and diverse organisms reconcile the fossil record with the true tempo of early animal during this time. Using probabilistic clock methods, we calcu- evolution. This issue even troubled Darwin (2) because it chal- late rates of evolution in the earliest trilobites virtually iden- lenged his ideas on gradual evolutionary change. He suggested tical to those throughout their Cambrian fossil history. We that the incompleteness of the geologic record can account for a conclude that the Cambrian explosion was over by the time the protracted, cryptic history of animals before their appearance as typical Cambrian fossil record commences and reject an diverse fossils. Over the 150+ years since On the Origin of Species unfossilized Precambrian history for trilobites, solving a prob- was published, fossil discoveries in Ediacaran and Cambrian rocks lem that had long troubled biologists since Darwin. and advances in chronostratigraphy, geochronology, and molecu- ’ Author contributions: J.R.P., G.D.E., and M.S.Y.L. designed research; J.R.P., G.D.E., and lar clocks have diminished Darwin s dilemma (3, 4). However, M.S.Y.L. performed research; M.S.Y.L. analyzed data; J.R.P. and G.D.E. collected pheno- there remain conspicuous gaps in the Cambrian records of many typic and stratigraphic data; and J.R.P., G.D.E., and M.S.Y.L. wrote the paper. animal lineages—for example, the decoupled first appearances of The authors declare no conflict of interest. euarthropod trace and body fossils (5)—perpetuating the idea of This article is a PNAS Direct Submission. an older hidden history for many clades. Published under the PNAS license. Fast evolutionary rates during the early Cambrian have been Data deposition: Data related to this work has been deposited in the Dryad Digital Re- used to explain the rapid emergence of animals, providing sup- pository (doi:10.5061/dryad.v7q827k). port for a more literal reading of the fossil record. Evidence 1To whom correspondence should be addressed. Email: [email protected]. consistent with the radiation of animals within a short time pe- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. riod (∼20 Ma) includes radiometric ages that have refined the 1073/pnas.1819366116/-/DCSupplemental. Cambrian timescale (e.g., ref. 6), as well as elevated rates of Published online February 19, 2019. 4394–4399 | PNAS | March 5, 2019 | vol. 116 | no. 10 www.pnas.org/cgi/doi/10.1073/pnas.1819366116 Downloaded by guest on September 27, 2021 Downloaded by guest on September 27, 2021 output; see middle, and late Cambrian.which Notably, allows all rates three of datasets evolution failed to to vary exhibit across sharply time elevated slices. rates Evolutionary in rates the for earliest discrete, time meristic, and slice. continuous Rate traits units were are very from constant raw across BEA the early, Fig. 1. Paterson et al. known fossiliferous rocks numbers of species of the same group, suddenly appear in the lowest same intensity as cladisticallydating, informative traits. this Where dataset possible, explicitly sampled autapomorphies with the which must have lived[Cambrian] long trilobites before the have [Cambrian] descended age from some one crustacean, tinuous ( of the preserved phenotypeFurongian [107 (ca. 521 discrete, 2 meristic,brian and families 6 (sensu con- piled ref. to 18) date, thatdataset comprising is 107 range the species from largest andusing Series most Bayesian comprehensive 2 tip-dating for clock trilobites toand com- methods 7) the (17). by Thevated analyzing phylogenetic evolutionary an rates extensive during dataset the of early Cambrian Cambrian trilobites (e.g., refs. 6 EARLY CAMBRIAN MIDDLE CAMBRIAN LATE CAMBRIAN Here we test Darwin 521 509 497 Miaolingian Furongian Dated time tree of Cambrian trilobites inferred from tip-dated Bayesian analyses of discrete, meristic, and continuous traits under a multiepoch clock, Terreneuvian Series 2 540 530 5 520 510 5 500 490 480 SI Appendix 2 1 0 0 SI Appendix FallotaspisFallotaspis (whisker plot) 95% HPDofnodeage ChoubertellaChoubertella DaguinaspisDaguinaspis CCalodiscusalodiscus SerrodiscusSerrodiscus – HebediscinaHebediscina 485 Ma) 1 ,Fig.S1 , Table S1 NNeocobboldiaeocobboldia Pagetia posterior probabilityofnode TsunyidiscusTsunyidiscus ’ NevadiaNevadia ... Epoch Clock OlenellusOlenellu s hypothesis (2) and later claims of ele- NephrolenellusNephrol (circle shading) BristoliaBristolia For instance, I cannot doubt that all the PeachellaPeachella — JudomJudomiaia )]. To satisfy the methodology of tip- for absolute and scaled rates. Full species names are presented in EllipElliptocephalatocephala and 115 traits that cover all aspects WanneriaWanne HolmiaHolmia MontezumaspisMontezumaspis
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