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evolutionary rates constrain the duration of the 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 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) are often considered exemplary for understanding the phenotypic and genomic evolution (7, 8). Rapid morphological of animal , 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 record with an established diversity, phyloge- diversification throughout the (3, 9, 10). However, netic disparity, and provincialism at the beginning of Cambrian the question remains as to when evolutionary rates slowed to 2 (∼521 Ma), suggesting a protracted but cryptic earlier his- norms, thus marking the end of the Cambrian ex- tory that possibly extends into the . 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 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 of biomineralized record and molecular . 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 . 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- 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 and earliest Cambrian (11 13). This, among other evidence, has been used to suggest that – (∼20 million ), 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 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 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 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 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 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, , 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 . 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 numbers of species of the same group, suddenly appear in the lowest species were preferentially selected based on fully articulated known fossiliferous rocks...For instance, I cannot doubt that all the exoskeletons and known ontogenies. Stratigraphic ages for each [Cambrian] trilobites have descended from some one , species were determined by cross-referencing associated bio- which must have lived long before the [Cambrian] ” (p. 306). zones with the calibrated Cambrian timescale (19) and other Here we test Darwin’s hypothesis (2) and later claims of ele- sources (SI Appendix). vated evolutionary rates during the early Cambrian (e.g., refs. 6 and 7) by analyzing an extensive dataset of Cambrian trilobites Cambrian Evolutionary Rates using Bayesian tip-dating clock methods (17). The phylogenetic Phenotypic and stratigraphic data were analyzed using tip-dated dataset is the largest and most comprehensive for trilobites com- Bayesian approaches (20, 21) that coestimate topologies, diver- piled to date, comprising 107 species—representing most Cam- gence dates, and evolutionary rates. To provide multiple inde- brian families (sensu ref. 18) that range from Series 2 to the pendent estimates of evolutionary tempo across the Cambrian, (ca. 521–485 Ma)—and 115 traits that cover all aspects rates of evolution of discrete, meristic, and continuous data were of the preserved phenotype [107 discrete, 2 meristic, and 6 con- each estimated separately across time, using unlinked clock tinuous (SI Appendix,Fig.S1)]. To satisfy the methodology of tip- models, which assume rates vary across time slices (but are shared dating, this dataset explicitly sampled autapomorphies with the across all lineages in the same time slice). Thus, rates of evolution same intensity as cladistically informative traits. Where possible, for the 107 discrete characters were estimated for the early (Series

Epoch Clock 480 95% HPD of node age (whisker plot)

posterior probability of node Akoldinioidia Parakoldinioidia Dikelocephalus Notchpeakia 1 (circle shading) 0 Plethopeltis Hungaia EVOLUTION Golasaphus Furongian Lonchopygella Loganellus Shergoldia Eurekia 490 Guangxiaspis Haniwa Asioptychaspis Tsinania LATE CAMBRIAN LATE Iveria Orygmaspis Burnetiella Elvinia Pterocephalia Labiostria Oligometopus Cheilocephalus Corynexochus Olenus Proceratopyge Liostracina Neodrepanura

497 Catillicephala Tricrepicephalus Jiulongshania Coosella Cedaria Norwoodia Fenghuangella Ajrikina Wanshania Monkaspis Lisania Tasmacephalus Palaeadotes 500 Prodamesella EARTH, ATMOSPHERIC, Papyriaspis Agraulos Sao Eccaparadoxides Modocia Asaphiscus Brachyaspidion Mapania Conocoryphe Bolaspidella Ptychoparia Elrathia AND PLANETARY SCIENCES Penarosa Fuchouia Dinesus Pagetia Xystridura Olenoides Xingrenaspis Kuetsingocephalus Oryctocephalus MIDDLE CAMBRIAN Bathynotus 509 Onaraspis p o a l b l u t a h o ll o a s i a ha a r e li aspi d p My P Protolenus Myopsolenites Hamatolenus Taya Ham Tayanaspis Anabaraspis Ana us h l

551010 a o c t lenell Wanneria Wanne ni s s discu uaev Olenellus O Zacanthopsis Zacant Nephrolenellus Nephro a a tocephal soce a gia Bristolia Bri Peac Peachella haran a s aca l hi r c alodi ngi s a lmi Strenuaeva Calodiscus C Stren Elliptocephala Ellip Serrodiscus Ellipsocephalus Serro Ellip eocobbo chan halu N Neocobboldia Holmia Ichangia Ho I s es s a i Megapharanaspis Megap Redlichia Estaingia Redli Estai Balcoracania Emuella Balco Emuel a a shani akut u p ll in a J Jakutus i hi u s a des sc c Yinites Yinit ll n i nocep idiscu s li xi e e i y l a o da de o a ed Zhang Zhangshania a i r s m Judomia Judom o sun naspi ad Series 2 ab ad Eoredlichia E Yunnanocephalus Yunna Hebediscina Tsunyidiscus Lemdadella Hebed T Le ertell v r onte zumas Metad Metadoxides Dolerolenus Doler e a taspi Nevadia N Montezumaspis Parabadiella Bigotina M P Bigot in Daguinaspis Dagui houb Choubertella C Fallotaspis Fallo

552020 521

EARLY CAMBRIAN EARLY DISCRETE MERISTIC CONTINUOUS 530 200 late late late 3 middle 1.5 middle middle 150 early early early 2 1 Terreneuvian 100 Density 1 50 0.5

0 0 0 2 540 0 1E-2 2E-2 3E-2 0 1 2 3 0.5 1 1.5 < slower RATE faster > < slower RATE faster > < slower RATE faster >

Fig. 1. Dated time tree of Cambrian trilobites inferred from tip-dated Bayesian analyses of discrete, meristic, and continuous traits under a multiepoch clock, which allows rates of evolution to vary across time slices. Evolutionary rates for discrete, meristic, and continuous traits were very constant across the early, middle, and late Cambrian. Notably, all three datasets failed to exhibit sharply elevated rates in the earliest time slice. Rate units are from raw BEAST (21) output; see SI Appendix, Table S1 for absolute and scaled rates. Full species names are presented in SI Appendix.

Paterson et al. PNAS | March 5, 2019 | vol. 116 | no. 10 | 4395 Downloaded by guest on September 27, 2021 2, 521–509 Ma), middle (Miaolingian, 509–497 Ma), and late All analyses reveal that rates of morphological evolution were (Furongian, 497–485 Ma) Cambrian, and likewise (separately) for homogeneous throughout the Cambrian. In the epoch clock model, the two meristic and for the six continuous traits. Alternative rates are marginally but insignificantly higher during the early models of evolutionary tempo were also evaluated using Bayes Cambrian compared with the middle and late Cambrian (Fig. 1). factors: a strict clock (which assumes rates are constant across Accordingly, a strict (or single-epoch) clock (SI Appendix,Fig.S2)— time slices and across lineages) and an uncorrelated relaxed clock which assumes rates are homogeneous across the entire time (which assumes rates vary across lineages but not necessarily sys- period spanned by the sampled fossils—fits the data better than tematically across time). Parsimony analyses were also performed does the epoch clock model. The relaxed clock also returned very to test the sensitivity of the tree topologies to analytical methods homogeneous rates of evolution across time (Figs. 2 and 3). This and to facilitate comparison of phylogeny inferred from pheno- time-constant rate pattern is consistent across the discrete, me- typic characters alone and those also incorporating temporal data. ristic, and continuous characters: for all three trait types, rates of Phenotypic and stratigraphic data, details of all analyses, and evolution are very uniform across the entire Cambrian trilobite executable scripts are in the SI Appendix and Dryad Digital fossil record. These results parallel the finding that Repository (doi.org/10.5061/dryad.v7q827k). rates among certain Cambrian Series 2 trilobites were not

480 Uncorrelated Lognormal Clock

RATES OF CHARACTER EVOLUTION

RATE COLOUR SCALE BRANCH COLOURING (L-R striping) Akoldinioidia

Discrete Meristic Continuous Parakoldinioidia Dikelocephalus Notchpeakia Fast Plethopeltis Hungaia Golasaphus Guangxiaspis Loganellus Eurekia Lonchopygella Shergoldia

Furongian 490 Meristic Discrete Tsinania Haniwa Asioptychaspis Continuous Iveria LATE CAMBRIAN LATE Orygmaspis Burnetiella Elvinia Pterocephalia Labiostria Oligometopus Cheilocephalus Corynexochus Proceratopyge Olenus Neodrepanura 497 Slow 0.0 0.0 0.07 Liostracina Catillicephala Tricrepicephalus Coosella Cedaria Norwoodia Jiulongshania Wanshania Monkaspis Ajrikina Fenghuangella Lisania Tasmacephalus Prodamesella Palaeadotes 500 Papyriaspis Ptychoparia Agraulos Sao Modocia Mapania Asaphiscus Conocoryphe Brachyaspidion Bolaspidella Eccaparadoxides Elrathia Penarosa Fuchouia Dinesus Xystridura Pagetia ocellata Olenoides Miaolingian MIDDLE CAMBRIAN Xingrenaspis Kuetsingocephalus Oryctocephalus Bathynotus 509 Onaraspis Hamatolenus Protolenus Tayanaspis Anabaraspis 510 Myopsolenites Wanneria Nephrolenellus Olenellus Zacanthopsis Bristolia Peachella Ellipsocephalus Serrodiscus Elliptocephala Strenuaeva Calodiscus Neocobboldia Ichangia Holmia Redlichia Estaingia Balcoracania Emuella Megapharanaspis Jakutus Yinites Zhangshania Judomia Eoredlichia Lemdadella Tsunyidiscus Yunnanocephalus Hebediscina Series 2 Metadoxides Dolerolenus Parabadiella Nevadia Montezumaspis Bigotina Daguinaspis Fallotaspis Choubertella

520 95% HPD of node age 521 (whisker plot)

posterior probability of node

1 (circle shading) 0 EARLY CAMBRIAN EARLY

530 Terreneuvian

Fig. 2. Dated time tree of Cambrian trilobites inferred from tip-dated Bayesian analyses of discrete, meristic, and continuous traits under an uncorrelated lognormal (UCLN) relaxed clock, which allows rates of evolution to vary across all individual branches. Full species names are presented in the SI Appendix.

4396 | www.pnas.org/cgi/doi/10.1073/pnas.1819366116 Paterson et al. Downloaded by guest on September 27, 2021 1 Discrete characters Meristic characters Continuous characters

0.5 UCLN Clock Rates (rescaled so max. rate is 1) so max. rate (rescaled

0 530 Ma 520 Ma 510 Ma 500 Ma 490 Ma

Fig. 3. Evolutionary rates for discrete, meristic, and continuous traits under an UCLN relaxed clock, showing that they were very constant across the early, middle, and late Cambrian. Rates have been rescaled so that the maximum rate is 1, to make the vertical axis comparable across discrete, meristic, and continuous characters.

unusually high, although slightly elevated relative to later Cambrian Series 2 onward, taxonomic conservatism is apparent (22); however, there appears to be no obvious correlation between among shelly and soft-bodied faunas, further suggesting un- morphological evolutionary rates and levels of intraspecific mor- remarkable evolutionary rates during this interval; for example,

phological variation for Cambrian trilobites (23). Given the large the many shared families and genera across Series 2 and EVOLUTION number of taxa sampled (relative to the number of variable char- Miaolingian Konservat-Lagerstätten (1, 26). Although the ho- acters), there is substantial phylogenetic uncertainty, many nodes mogeneous rates across the Cambrian are here interpreted to have weak support, and the consensus trees differ in certain clades indicate a rapid attainment of postexplosion normality, there is an between analyses (Figs. 1 and 2 and SI Appendix, Figs. S2 and S3). alternative interpretation: that rateswereelevatedacrossmostof However, the above inferences of evolutionary rates accommodate the Cambrian. However, the longevity of trilobite morphotypes this phylogenetic uncertainty by integrating all parameter estimates (e.g., genera and families) across the Cambrian (28) and general and error intervals across the full pool of sampled trees. stability of faunas discussed above make the alternative in- The basal divergence in Trilobita is estimated by our dated trees terpretation less likely. Thus, Chengjiang and younger Cambrian EARTH, ATMOSPHERIC,

to be within the Terreneuvian (Figs. 1 and 2). In our epoch clock -type (BST) deposits should not be considered AND PLANETARY SCIENCES model (Fig. 1), this divergence is consistently within the , snapshots of the unfolding explosion but rather the early (post- with the upper (older) 95% highest posterior density (HPD) in- explosion) records of modern-style marine ecosystems. terval being 541.3 Ma. This inferred origin of trilobites sometime – Despite ongoing debate over the true origins of animal phyla, after the Ediacaran Cambrian boundary represents a very conser- our data, as well as the Ediacaran–Cambrian geochemical, body, vative maximum age for the group. Because this analysis did not and trace fossil records (1, 3, 9), indicate that a modern-style deliberately impose any node age constraints, the rates and di- marine biosphere was fully established by Series 2, followed by vergence dates for the basal portion of the tree preceding the broad-scale evolutionary stasis throughout the remainder of the oldest species analyzed (519 Ma) are necessarily extrapolated Cambrian. Given the apparent paucity of unequivocal eumeta- from estimates derived from the subsequent (preserved) trilobite zoan representatives in the Ediacaran (4, 29), it seems that many fossil record. If evolutionary rates were faster before the first tri- stem- and crown-group members of most bilaterian phyla had lobites appear as body fossils, then the inferred rates before 519 Ma ∼ in our trees will be underestimates, and the inferred dates would be definitively appeared and diversified in 20 My (Fig. 4) (8, 9, 29, overestimates. Faster evolutionary rates would allow for the initial 30). Among these novel body plans is rampant convergence in phenotypic disparity of trilobite fossils to be established in less time. various forms of biomineralization (24, 30) and other anatomical Imposing a root node age constraint of 522 Ma (13) predictably innovations that allowed animals increased mobility and ways of increased rates at the base of the tree preceding the oldest fossils sensing their environment (1, 8). Notwithstanding the patchy analyzed (519 Ma), but rates in the early, middle, and late Cam- Terreneuvian fossil record, it is clear that a new style of eco- — brian remained very similar (SI Appendix,TableS1). logical network including greatly expanded food webs and as- sociated nutrient cycling, plus complex tiering above and below Duration of the Cambrian Explosion the substrate that helped reengineer the marine ecosystem— Unexpectedly homogeneous rates of morphological evolution rapidly emerged during this interval (1). throughout the entire Cambrian trilobite fossil record support the idea that the explosion represents a truly brief evolutionary A Cambrian Origin for Trilobites burst that began in the Terreneuvian (at the latest) and had A Terreneuvian origin for trilobites contradicts previous infer- largely concluded by Series 2 (6, 8–10, 24). Regardless of the ences of a protracted Precambrian history (2, 14–16). Further- potential biological and analytical factors responsible for fast more, our results are supported by evidence from the euarthropod initial rates (1, 7, 8, 25), our results provide compelling quanti- trace fossil record and molecular clocks (Fig. 4). The oldest tative evidence that this burst had ended by 519 Ma. This time trilobite-like traces (e.g., Rusophycus) are early Fortunian in age constraint is also exemplified by the well-established diversity of (5, 9), and recent molecular clocks (e.g., ref. 31) place the origin of eumetazoans in the Chengjiang biota of China (26), which has a euarthropods in the late Ediacaran or earliest Cambrian. A con- maximum age of 518.03 ± 0.69/0.71 Ma (27). In fact, from servative late Ediacaran root age for euarthropods still permits a

Paterson et al. PNAS | March 5, 2019 | vol. 116 | no. 10 | 4397 Downloaded by guest on September 27, 2021 Fig. 4. Key records of early animal evolution, seawater chemistry, and exceptional fossil preservation during the latest Ediacaran to Cambrian. Temporal range of BST deposits (5, 19) shows important examples in ascending stratigraphic order: 1, Khatyspyt Formation (); 2, Chengjiang (China) and (North Greenland); 3, Guanshan (China); 4, Burgess Shale (Canada) and (China); 5, Wheeler Formation (United States); 6, Marjum Formation (United States). BST deposits are less common by the Furongian. Other data sources are as follows: date for origin of Euarthropoda represents the posterior mean node age (figure 6 in ref. 31); date for origin of trilobites is the mean node age of the epoch clock model (Fig. 1); (FAD) for trilobite-like traces (5), rhynchonelliform (24), echinoderms (33), and trilobite body fossils (13); seawater chemistry (30, 34); and diversity of phyla (3), classes (3), and genera(10).

Cambrian origin for trilobites, given their derived phylogenetic The existence of nonbiomineralized trilobites in the Terreneuvian position within Euarthropoda (32). would have required multiple lineages to simultaneously con- The absence of Terreneuvian trilobite body fossils can be verge upon a calcite exoskeleton at around 521 Ma, unless initial explained under two potential scenarios. The first scenario is that evolutionary rates were much faster, thus bringing their origin and the fossil record is a reasonably accurate representation of early fewer lineages closer to the lower boundary of Series 2 (in support trilobite evolution, implying that rates of morphological evolu- of the first scenario discussed above). Synchronous biomineraliza- tion before 519 Ma were substantially faster than subsequently tion across two or more trilobite lineages is consistent with the (SI Appendix, Table S1). This hypothesis forces rapid dispersal observation that other disparate bilaterians, such as echinoderms between widely separated paleocontinents and is difficult to and rhynchonelliform brachiopods, also acquired calcitic skeletons reconcile with the provincialism observed in the earliest trilo- around this time (Fig. 4) (24, 33). Notably, this time coincides with a bites. However, if correct, this may also explain the perceived change in ocean chemistry, particularly the onset of a calcite sea (30, diachronism of the first trilobite fossils on different paleo- 34); ambient seawater chemistry influences the type of biomineral continents (12, 13), with the group potentially originating and secreted at the time skeletons evolved de novo in a clade (34). rapidly radiating out from Siberia, West , or West These repeated patterns suggest that compelling environmental Gondwana (15, 16). The scenario—more consistent with [e.g., changing Mg/Ca ratios and oxygen levels (1, 30, 35)] and/or our results, plus trace fossil, molecular clock, and biogeographic biological factors [e.g., predation (30, 36)] were influencing this major data (5, 11)—is that the earliest trilobites (pre-521 Ma) have not episode of biomineralization and diversification during the final been preserved or yet discovered in Terreneuvian rocks. The stages of the Cambrian explosion. The shelly fossil record of animals diversity of other skeletonized animals from a range of envi- thus dramatically improves only around 521 Ma, but by that , ronments throughout the Terreneuvian (24, 30) indicates an the Cambrian explosion was largely over. adequate shelly fossil record. Thus, the absence of trilobites and indeed other euarthropod body fossils in Terreneuvian rocks ACKNOWLEDGMENTS. We thank N. Campione, R. Gaines, L. Holmer, could be explained by their nonbiomineralized exoskeletons and R. Lerosey-Aubril, G. Mángano, and S. Zamora for discussions and feed- back; S. Gon III for trilobite drawings; and G. Budd and N. Hughes for the unusual dearth of soft-tissue preservation (especially BST constructive reviews. J.R.P. was supported by an Australian Research deposits) for this time interval (Fig. 4) (4, 5, 19). Council Fellowship (FT120100770).

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