trilobite evolutionary rates constrain the duration of the cambrian … · 2, 521–509 ma), middle...
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Trilobite evolutionary rates constrain the duration ofthe Cambrian explosionJohn 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 EarthSciences, 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 theCambrian explosion of animal life, due to their unsurpassed di-versity and abundance. These biomineralized arthropods appearabruptly in the fossil record with an established diversity, phyloge-netic disparity, and provincialism at the beginning of CambrianSeries 2 (∼521 Ma), suggesting a protracted but cryptic earlier his-tory that possibly extends into the Precambrian. However, recentanalyses indicate elevated rates of phenotypic and genomic evolu-tion for arthropods during the early Cambrian, thereby shorteningthe phylogenetic fuse. Furthermore, comparatively little researchhas been devoted to understanding the duration of the Cambrianexplosion, after which normal Phanerozoic evolutionary rates wereestablished. We test these hypotheses by applying Bayesian tip-dating methods to a comprehensive dataset of Cambrian trilobites.We show that trilobites have a Cambrian origin, as supported by thetrace fossil record and molecular clocks. Surprisingly, they exhibitconstant evolutionary rates across the entire Cambrian, for all as-pects of the preserved phenotype: discrete, meristic, and continuousmorphological traits. Our data therefore provide robust, quantita-tive evidence that by the time the typical Cambrian fossil recordbegins (∼521 Ma), the Cambrian explosion had already largely con-cluded. This suggests that a modern-style marine biosphere hadrapidly emerged during the latest Ediacaran and earliest Cambrian(∼20 million years), followed by broad-scale evolutionary stasisthroughout the remainder of the Cambrian.
Cambrian explosion | evolutionary rates | trilobites | Bayesian tip-dating |morphological clock
The abrupt first appearance of a multitude of animal fossils inearly Cambrian rocks (Terreneuvian to Series 2; ca. 541–
509 Ma) epitomizes one of the most significant evolutionaryevents in Earth’s history (1). This sudden burst of diversity andabundance across most eumetazoan (especially bilaterian) phylaover a relatively short geologic time span, and lack of obviousPrecambrian precursors, poses a conundrum when attempting toreconcile the fossil record with the true tempo of early animalevolution. This issue even troubled Darwin (2) because it chal-lenged his ideas on gradual evolutionary change. He suggestedthat the incompleteness of the geologic record can account for aprotracted, cryptic history of animals before their appearance asdiverse fossils. Over the 150+ years since On the Origin of Specieswas published, fossil discoveries in Ediacaran and Cambrian rocksand advances in chronostratigraphy, geochronology, and molecu-lar clocks have diminished Darwin’s dilemma (3, 4). However,there remain conspicuous gaps in the Cambrian records of manyanimal lineages—for example, the decoupled first appearances ofeuarthropod trace and body fossils (5)—perpetuating the idea ofan older hidden history for many clades.Fast evolutionary rates during the early Cambrian have been
used to explain the rapid emergence of animals, providing sup-port for a more literal reading of the fossil record. Evidenceconsistent with the radiation of animals within a short time pe-riod (∼20 Ma) includes radiometric ages that have refined theCambrian timescale (e.g., ref. 6), as well as elevated rates of
phenotypic and genomic evolution (7, 8). Rapid morphologicaland molecular evolution during the earliest Cambrian almostcertainly underpinned the pronounced pulses of origination anddiversification throughout the Terreneuvian (3, 9, 10). However,the question remains as to when evolutionary rates slowed toPhanerozoic norms, thus marking the end of the Cambrian ex-plosion. For instance, the calibrations used in ref. 7 were mostly488 Ma or younger; that analysis therefore only had weak powerto constrain fast early rates further back than that time point.Indirect measures using trends in animal diversity and disparitysuggest that rates were elevated throughout the early Cambrian(3, 9, 10), but no study has yet quantified rates of evolutionacross a broad selection of Cambrian lineages using direct phe-notypic information from the fossil record.Trilobites are a diverse and abundant clade of biomineralized
crown-group euarthropods that best exemplify the disjunct be-tween the Cambrian rock record and any expected gradualisthistory of a clade before its first appearance as fossils. The oldesttrilobite body fossils around the world, at or near the Terreneuvian–Cambrian Series 2 boundary (ca. 521 Ma), already show establisheddiversity, phylogenetic disparity, and biogeographic provincialism(11–13). This, among other evidence, has been used to suggest thattrilobites had a much earlier, Precambrian origin (e.g., refs. 14–16).In fact, Darwin (2) chose trilobites as an exemplar group to high-light his dilemma about animal origins: “There is another and allieddifficulty, which is much graver. I allude to the manner in which
Significance
The Cambrian explosion was arguably the most important bi-ological event after the origin of life. Extensive research hasbeen devoted to understanding when it began but far less onwhen this burst of evolution ended. We present a quantitativestudy that addresses these issues, using a large new dataset ofCambrian trilobites, the most abundant and diverse organismsduring this time. Using probabilistic clock methods, we calcu-late rates of evolution in the earliest trilobites virtually iden-tical to those throughout their Cambrian fossil history. Weconclude that the Cambrian explosion was over by the time thetypical Cambrian fossil record commences and reject anunfossilized Precambrian history for trilobites, solving a prob-lem that had long troubled biologists since Darwin.
Author contributions: J.R.P., G.D.E., and M.S.Y.L. designed research; J.R.P., G.D.E., andM.S.Y.L. performed research; M.S.Y.L. analyzed data; J.R.P. and G.D.E. collected pheno-typic and stratigraphic data; and J.R.P., G.D.E., and M.S.Y.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Published under the PNAS license.
Data deposition: Data related to this work has been deposited in the Dryad Digital Re-pository (doi:10.5061/dryad.v7q827k).1To whom correspondence should be addressed. Email: [email protected].
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1819366116/-/DCSupplemental.
Published online February 19, 2019.
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numbers of species of the same group, suddenly appear in the lowestknown fossiliferous rocks. . . For instance, I cannot doubt that all the[Cambrian] trilobites have descended from some one crustacean,which must have lived long before the [Cambrian] age” (p. 306).Here we test Darwin’s hypothesis (2) and later claims of ele-
vated evolutionary rates during the early Cambrian (e.g., refs. 6and 7) by analyzing an extensive dataset of Cambrian trilobitesusing Bayesian tip-dating clock methods (17). The phylogeneticdataset is the largest and most comprehensive for trilobites com-piled to date, comprising 107 species—representing most Cam-brian families (sensu ref. 18) that range from Series 2 to theFurongian (ca. 521–485 Ma)—and 115 traits that cover all aspectsof the preserved phenotype [107 discrete, 2 meristic, and 6 con-tinuous (SI Appendix, Fig. S1)]. To satisfy the methodology of tip-dating, this dataset explicitly sampled autapomorphies with thesame intensity as cladistically informative traits. Where possible,
species were preferentially selected based on fully articulatedexoskeletons and known ontogenies. Stratigraphic ages for eachspecies were determined by cross-referencing associated bio-zones with the calibrated Cambrian timescale (19) and othersources (SI Appendix).
Cambrian Evolutionary RatesPhenotypic and stratigraphic data were analyzed using tip-datedBayesian approaches (20, 21) that coestimate topologies, diver-gence dates, and evolutionary rates. To provide multiple inde-pendent estimates of evolutionary tempo across the Cambrian,rates of evolution of discrete, meristic, and continuous data wereeach estimated separately across time, using unlinked epoch clockmodels, which assume rates vary across time slices (but are sharedacross all lineages in the same time slice). Thus, rates of evolutionfor the 107 discrete characters were estimated for the early (Series
posterior probability of node(circle shading)1
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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.
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2, 521–509 Ma), middle (Miaolingian, 509–497 Ma), and late(Furongian, 497–485 Ma) Cambrian, and likewise (separately) forthe two meristic and for the six continuous traits. Alternativemodels of evolutionary tempo were also evaluated using Bayesfactors: a strict clock (which assumes rates are constant acrosstime slices and across lineages) and an uncorrelated relaxed clock(which assumes rates vary across lineages but not necessarily sys-tematically across time). Parsimony analyses were also performedto test the sensitivity of the tree topologies to analytical methodsand to facilitate comparison of phylogeny inferred from pheno-typic characters alone and those also incorporating temporal data.Phenotypic and stratigraphic data, details of all analyses, andexecutable scripts are in the SI Appendix and Dryad DigitalRepository (doi.org/10.5061/dryad.v7q827k).
All analyses reveal that rates of morphological evolution werehomogeneous throughout the Cambrian. In the epoch clock model,rates are marginally but insignificantly higher during the earlyCambrian compared with the middle and late Cambrian (Fig. 1).Accordingly, a strict (or single-epoch) clock (SI Appendix, Fig. S2)—which assumes rates are homogeneous across the entire timeperiod spanned by the sampled fossils—fits the data better thandoes the epoch clock model. The relaxed clock also returned veryhomogeneous rates of evolution across time (Figs. 2 and 3). Thistime-constant rate pattern is consistent across the discrete, me-ristic, and continuous characters: for all three trait types, rates ofevolution are very uniform across the entire Cambrian trilobitefossil record. These results parallel the finding that speciationrates among certain Cambrian Series 2 trilobites were not
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Fig. 2. Dated time tree of Cambrian trilobites inferred from tip-dated Bayesian analyses of discrete, meristic, and continuous traits under an uncorrelatedlognormal (UCLN) relaxed clock, which allows rates of evolution to vary across all individual branches. Full species names are presented in the SI Appendix.
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unusually high, although slightly elevated relative to later times(22); however, there appears to be no obvious correlation betweenmorphological evolutionary rates and levels of intraspecific mor-phological variation for Cambrian trilobites (23). Given the largenumber of taxa sampled (relative to the number of variable char-acters), there is substantial phylogenetic uncertainty, many nodeshave weak support, and the consensus trees differ in certain cladesbetween analyses (Figs. 1 and 2 and SI Appendix, Figs. S2 and S3).However, the above inferences of evolutionary rates accommodatethis phylogenetic uncertainty by integrating all parameter estimatesand error intervals across the full pool of sampled trees.The basal divergence in Trilobita is estimated by our dated trees
to be within the Terreneuvian (Figs. 1 and 2). In our epoch clockmodel (Fig. 1), this divergence is consistently within the Fortunian,with the upper (older) 95% highest posterior density (HPD) in-terval being 541.3 Ma. This inferred origin of trilobites sometimeafter the Ediacaran–Cambrian boundary represents a very conser-vative maximum age for the group. Because this analysis did notdeliberately impose any node age constraints, the rates and di-vergence dates for the basal portion of the tree preceding theoldest species analyzed (519 Ma) are necessarily extrapolatedfrom estimates derived from the subsequent (preserved) trilobitefossil record. If evolutionary rates were faster before the first tri-lobites appear as body fossils, then the inferred rates before 519 Main our trees will be underestimates, and the inferred dates would beoverestimates. Faster evolutionary rates would allow for the initialphenotypic disparity of trilobite fossils to be established in less time.Imposing a root node age constraint of 522 Ma (13) predictablyincreased rates at the base of the tree preceding the oldest fossilsanalyzed (519 Ma), but rates in the early, middle, and late Cam-brian remained very similar (SI Appendix, Table S1).
Duration of the Cambrian ExplosionUnexpectedly homogeneous rates of morphological evolutionthroughout the entire Cambrian trilobite fossil record supportthe idea that the explosion represents a truly brief evolutionaryburst that began in the Terreneuvian (at the latest) and hadlargely concluded by Series 2 (6, 8–10, 24). Regardless of thepotential biological and analytical factors responsible for fastinitial rates (1, 7, 8, 25), our results provide compelling quanti-tative evidence that this burst had ended by 519 Ma. This timeconstraint is also exemplified by the well-established diversity ofeumetazoans in the Chengjiang biota of China (26), which has amaximum age of 518.03 ± 0.69/0.71 Ma (27). In fact, from
Cambrian Series 2 onward, taxonomic conservatism is apparentamong shelly and soft-bodied faunas, further suggesting un-remarkable evolutionary rates during this interval; for example,the many shared families and genera across Series 2 andMiaolingian Konservat-Lagerstätten (1, 26). Although the ho-mogeneous rates across the Cambrian are here interpreted toindicate a rapid attainment of postexplosion normality, there is analternative interpretation: that rates were elevated across most ofthe Cambrian. However, the longevity of trilobite morphotypes(e.g., genera and families) across the Cambrian (28) and generalstability of faunas discussed above make the alternative in-terpretation less likely. Thus, Chengjiang and younger CambrianBurgess Shale-type (BST) deposits should not be consideredsnapshots of the unfolding explosion but rather the early (post-explosion) records of modern-style marine ecosystems.Despite ongoing debate over the true origins of animal phyla,
our data, as well as the Ediacaran–Cambrian geochemical, body,and trace fossil records (1, 3, 9), indicate that a modern-stylemarine biosphere was fully established by Series 2, followed bybroad-scale evolutionary stasis throughout the remainder of theCambrian. Given the apparent paucity of unequivocal eumeta-zoan representatives in the Ediacaran (4, 29), it seems that manystem- and crown-group members of most bilaterian phyla haddefinitively appeared and diversified in ∼20 My (Fig. 4) (8, 9, 29,30). Among these novel body plans is rampant convergence invarious forms of biomineralization (24, 30) and other anatomicalinnovations that allowed animals increased mobility and ways ofsensing their environment (1, 8). Notwithstanding the patchyTerreneuvian fossil record, it is clear that a new style of eco-logical network—including greatly expanded food webs and as-sociated nutrient cycling, plus complex tiering above and belowthe substrate that helped reengineer the marine ecosystem—
rapidly emerged during this interval (1).
A Cambrian Origin for TrilobitesA Terreneuvian origin for trilobites contradicts previous infer-ences of a protracted Precambrian history (2, 14–16). Further-more, our results are supported by evidence from the euarthropodtrace fossil record and molecular clocks (Fig. 4). The oldesttrilobite-like traces (e.g., Rusophycus) are early Fortunian in age(5, 9), and recent molecular clocks (e.g., ref. 31) place the origin ofeuarthropods in the late Ediacaran or earliest Cambrian. A con-servative late Ediacaran root age for euarthropods still permits a
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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, andcontinuous characters.
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Cambrian origin for trilobites, given their derived phylogeneticposition within Euarthropoda (32).The absence of Terreneuvian trilobite body fossils can be
explained under two potential scenarios. The first scenario is thatthe fossil record is a reasonably accurate representation of earlytrilobite evolution, implying that rates of morphological evolu-tion before 519 Ma were substantially faster than subsequently(SI Appendix, Table S1). This hypothesis forces rapid dispersalbetween widely separated paleocontinents and is difficult toreconcile with the provincialism observed in the earliest trilo-bites. However, if correct, this may also explain the perceiveddiachronism of the first trilobite fossils on different paleo-continents (12, 13), with the group potentially originating andrapidly radiating out from Siberia, West Laurentia, or WestGondwana (15, 16). The second scenario—more consistent withour results, plus trace fossil, molecular clock, and biogeographicdata (5, 11)—is that the earliest trilobites (pre-521 Ma) have notbeen preserved or yet discovered in Terreneuvian rocks. Thediversity of other skeletonized animals from a range of envi-ronments throughout the Terreneuvian (24, 30) indicates anadequate shelly fossil record. Thus, the absence of trilobites andindeed other euarthropod body fossils in Terreneuvian rockscould be explained by their nonbiomineralized exoskeletons andthe unusual dearth of soft-tissue preservation (especially BSTdeposits) for this time interval (Fig. 4) (4, 5, 19).
The existence of nonbiomineralized trilobites in the Terreneuvianwould have required multiple lineages to simultaneously con-verge upon a calcite exoskeleton at around 521 Ma, unless initialevolutionary rates were much faster, thus bringing their origin andfewer lineages closer to the lower boundary of Series 2 (in supportof the first scenario discussed above). Synchronous biomineraliza-tion across two or more trilobite lineages is consistent with theobservation that other disparate bilaterians, such as echinodermsand rhynchonelliform brachiopods, also acquired calcitic skeletonsaround this time (Fig. 4) (24, 33). Notably, this time coincides with achange in ocean chemistry, particularly the onset of a calcite sea (30,34); ambient seawater chemistry influences the type of biomineralsecreted at the time skeletons evolved de novo in a clade (34).These repeated patterns suggest that compelling environmental[e.g., changing Mg/Ca ratios and oxygen levels (1, 30, 35)] and/orbiological factors [e.g., predation (30, 36)] were influencing this majorepisode of biomineralization and diversification during the finalstages of the Cambrian explosion. The shelly fossil record of animalsthus dramatically improves only around 521 Ma, but by that stage,the Cambrian explosion was largely over.
ACKNOWLEDGMENTS. We thank N. Campione, R. Gaines, L. Holmer,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 forconstructive reviews. J.R.P. was supported by an Australian ResearchCouncil Future Fellowship (FT120100770).
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