Trilobite evolutionary rates constrain the duration of the Cambrian explosion

Significance

The Cambrian explosion was arguably the most important biological event after the origin of life. Extensive research has been devoted to understanding when it began but far less on when this burst of evolution ended. We present a quantitative study that addresses these issues, using a large new dataset of Cambrian trilobites, the most abundant and diverse organisms during this time. Using probabilistic clock methods, we calculate rates of evolution in the earliest trilobites virtually identical to those throughout their Cambrian fossil history. We conclude that the Cambrian explosion was over by the time the typical Cambrian fossil record commences and reject an unfossilized Precambrian history for trilobites, solving a problem that had long troubled biologists since Darwin.

Abstract

Trilobites are often considered exemplary for understanding the Cambrian explosion of animal life, due to their unsurpassed diversity and abundance. These biomineralized arthropods appear abruptly in the fossil record with an established diversity, phylogenetic disparity, and provincialism at the beginning of Cambrian Series 2 (∼521 Ma), suggesting a protracted but cryptic earlier history that possibly extends into the Precambrian. However, recent analyses indicate elevated rates of phenotypic and genomic evolution for arthropods during the early Cambrian, thereby shortening the phylogenetic fuse. Furthermore, comparatively little research has been devoted to understanding the duration of the Cambrian explosion, after which normal Phanerozoic evolutionary rates were established. 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 the trace fossil record and molecular clocks. Surprisingly, they exhibit constant evolutionary rates across the entire Cambrian, for all aspects of the preserved phenotype: discrete, meristic, and continuous morphological traits. Our data therefore provide robust, quantitative evidence that by the time the typical Cambrian fossil record begins (∼521 Ma), the Cambrian explosion had already largely concluded. This suggests that a modern-style marine biosphere had rapidly emerged during the latest Ediacaran and earliest Cambrian (∼20 million years), followed by broad-scale evolutionary stasis throughout the remainder of the Cambrian.

The abrupt first appearance of a multitude of animal fossils in early Cambrian rocks (Terreneuvian to Series 2; ca. 541–509 Ma) epitomizes one of the most significant evolutionary events in Earth’s history (1). This sudden burst of diversity and abundance across most eumetazoan (especially bilaterian) phyla over a relatively short geologic time span, and lack of obvious Precambrian precursors, poses a conundrum when attempting to reconcile the fossil record with the true tempo of early animal evolution. This issue even troubled Darwin (2) because it challenged his ideas on gradual evolutionary change. He suggested that the incompleteness of the geologic record can account for a protracted, cryptic history of animals before their appearance as diverse fossils. Over the 150+ years since On the Origin of Species was published, fossil discoveries in Ediacaran and Cambrian rocks and advances in chronostratigraphy, geochronology, and molecular clocks have diminished Darwin’s dilemma (3, 4). However, there remain conspicuous gaps in the Cambrian records of many animal lineages—for example, the decoupled first appearances of euarthropod trace and body fossils (5)—perpetuating the idea of an older hidden history for many clades.

Fast evolutionary rates during the early Cambrian have been used to explain the rapid emergence of animals, providing support for a more literal reading of the fossil record. Evidence consistent with the radiation of animals within a short time period (∼20 Ma) includes radiometric ages that have refined the Cambrian timescale (e.g., ref. 6), as well as elevated rates of phenotypic and genomic evolution (7, 8). Rapid morphological and molecular evolution during the earliest Cambrian almost certainly underpinned the pronounced pulses of origination and diversification throughout the Terreneuvian (3, 9, 10). However, the question remains as to when evolutionary rates slowed to Phanerozoic norms, thus marking the end of the Cambrian explosion. For instance, the calibrations used in ref. 7 were mostly 488 Ma or younger; that analysis therefore only had weak power to constrain fast early rates further back than that time point. Indirect measures using trends in animal diversity and disparity suggest that rates were elevated throughout the early Cambrian (3, 9, 10), but no study has yet quantified rates of evolution across a broad selection of Cambrian lineages using direct phenotypic information from the fossil record.

Trilobites are a diverse and abundant clade of biomineralized crown-group euarthropods that best exemplify the disjunct between the Cambrian rock record and any expected gradualist history of a clade before its first appearance as fossils. The oldest trilobite body fossils around the world, at or near the Terreneuvian–Cambrian Series 2 boundary (ca. 521 Ma), already show established diversity, phylogenetic disparity, and biogeographic provincialism (11–13). This, among other evidence, has been used to suggest that trilobites had a much earlier, Precambrian origin (e.g., refs. 14–16). In fact, Darwin (2) chose trilobites as an exemplar group to highlight his dilemma about animal origins: “There is another and allied difficulty, which is much graver. I allude to the manner in which numbers of species of the same group, suddenly appear in the lowest known 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 elevated evolutionary rates during the early Cambrian (e.g., refs. 6 and 7) by analyzing an extensive dataset of Cambrian trilobites using Bayesian tip-dating clock methods (17). The phylogenetic dataset is the largest and most comprehensive for trilobites compiled to date, comprising 107 species—representing most Cambrian families (sensu ref. 18) that range from Series 2 to the Furongian (ca. 521–485 Ma)—and 115 traits that cover all aspects of the preserved phenotype [107 discrete, 2 meristic, and 6 continuous (SI Appendix, Fig. S1)]. To satisfy the methodology of tip-dating, this dataset explicitly sampled autapomorphies with the same intensity as cladistically informative traits. Where possible, species were preferentially selected based on fully articulated exoskeletons and known ontogenies. Stratigraphic ages for each species were determined by cross-referencing associated biozones with the calibrated Cambrian timescale (19) and other sources (SI Appendix).

Cambrian Evolutionary Rates

Phenotypic and stratigraphic data were analyzed using tip-dated Bayesian approaches (20, 21) that coestimate topologies, divergence dates, and evolutionary rates. To provide multiple independent estimates of evolutionary tempo across the Cambrian, rates of evolution of discrete, meristic, and continuous data were each estimated separately across time, using unlinked epoch clock models, which assume rates vary across time slices (but are shared across all lineages in the same time slice). Thus, rates of evolution for the 107 discrete characters were estimated for the early (Series 2, 521–509 Ma), middle (Miaolingian, 509–497 Ma), and late (Furongian, 497–485 Ma) Cambrian, and likewise (separately) for the two meristic and for the six continuous traits. Alternative models of evolutionary tempo were also evaluated using Bayes factors: a strict clock (which assumes rates are constant across time slices and across lineages) and an uncorrelated relaxed clock (which assumes rates vary across lineages but not necessarily systematically across time). Parsimony analyses were also performed to test the sensitivity of the tree topologies to analytical methods and to facilitate comparison of phylogeny inferred from phenotypic characters alone and those also incorporating temporal data. Phenotypic and stratigraphic data, details of all analyses, and executable scripts are in the SI Appendix and Dryad Digital Repository (doi.org/10.5061/dryad.v7q827k).

All analyses reveal that rates of morphological evolution were homogeneous throughout the Cambrian. In the epoch clock model, rates are marginally but insignificantly higher during the early Cambrian 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 time period spanned by the sampled fossils—fits the data better than does the epoch clock model. The relaxed clock also returned very homogeneous rates of evolution across time (Figs. 2 and 3). This time-constant rate pattern is consistent across the discrete, meristic, and continuous characters: for all three trait types, rates of evolution are very uniform across the entire Cambrian trilobite fossil record. These results parallel the finding that speciation rates among certain Cambrian Series 2 trilobites were not unusually high, although slightly elevated relative to later times (22); however, there appears to be no obvious correlation between morphological evolutionary rates and levels of intraspecific morphological variation for Cambrian trilobites (23). Given the large number of taxa sampled (relative to the number of variable characters), there is substantial phylogenetic uncertainty, many nodes have weak support, and the consensus trees differ in certain clades between analyses (Figs. 1 and 2 and SI Appendix, Figs. S2 and S3). However, the above inferences of evolutionary rates accommodate this phylogenetic uncertainty by integrating all parameter estimates and error intervals across the full pool of sampled trees.

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.

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.

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.

The basal divergence in Trilobita is estimated by our dated trees to be within the Terreneuvian (Figs. 1 and 2). In our epoch clock model (Fig. 1), this divergence is consistently within the Fortunian, with the upper (older) 95% highest posterior density (HPD) interval being 541.3 Ma. This inferred origin of trilobites sometime after the Ediacaran–Cambrian boundary represents a very conservative maximum age for the group. Because this analysis did not deliberately impose any node age constraints, the rates and divergence dates for the basal portion of the tree preceding the oldest species analyzed (519 Ma) are necessarily extrapolated from estimates derived from the subsequent (preserved) trilobite fossil record. If evolutionary rates were faster before the first trilobites appear as body fossils, then the inferred rates before 519 Ma in our trees will be underestimates, and the inferred dates would be overestimates. Faster evolutionary rates would allow for the initial phenotypic disparity of trilobite fossils to be established in less time. Imposing a root node age constraint of 522 Ma (13) predictably increased rates at the base of the tree preceding the oldest fossils analyzed (519 Ma), but rates in the early, middle, and late Cambrian remained very similar (SI Appendix, Table S1).

Duration of the Cambrian Explosion

Unexpectedly homogeneous rates of morphological evolution throughout the entire Cambrian trilobite fossil record support the idea that the explosion represents a truly brief evolutionary burst that began in the Terreneuvian (at the latest) and had largely concluded by Series 2 (6, 8–10, 24). Regardless of the potential biological and analytical factors responsible for fast initial rates (1, 7, 8, 25), our results provide compelling quantitative evidence that this burst had ended by 519 Ma. This time constraint is also exemplified by the well-established diversity of eumetazoans in the Chengjiang biota of China (26), which has a maximum age of 518.03 ± 0.69/0.71 Ma (27). In fact, from Cambrian Series 2 onward, taxonomic conservatism is apparent among shelly and soft-bodied faunas, further suggesting unremarkable evolutionary rates during this interval; for example, the many shared families and genera across Series 2 and Miaolingian Konservat-Lagerstätten (1, 26). Although the homogeneous rates across the Cambrian are here interpreted to indicate a rapid attainment of postexplosion normality, there is an alternative interpretation: that rates were elevated across most of the Cambrian. However, the longevity of trilobite morphotypes (e.g., genera and families) across the Cambrian (28) and general stability of faunas discussed above make the alternative interpretation less likely. Thus, Chengjiang and younger Cambrian Burgess Shale-type (BST) deposits should not be considered snapshots of the unfolding explosion but rather the early (postexplosion) 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-style marine biosphere was fully established by Series 2, followed by broad-scale evolutionary stasis throughout the remainder of the Cambrian. Given the apparent paucity of unequivocal eumetazoan representatives in the Ediacaran (4, 29), it seems that many stem- and crown-group members of most bilaterian phyla had definitively appeared and diversified in ∼20 My (Fig. 4) (8, 9, 29, 30). Among these novel body plans is rampant convergence in various forms of biomineralization (24, 30) and other anatomical innovations that allowed animals increased mobility and ways of sensing their environment (1, 8). Notwithstanding the patchy Terreneuvian fossil record, it is clear that a new style of ecological network—including greatly expanded food webs and associated nutrient cycling, plus complex tiering above and below the substrate that helped reengineer the marine ecosystem—rapidly emerged during this interval (1).

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 (Siberia); 2, Chengjiang (China) and Sirius Passet (North Greenland); 3, Guanshan (China); 4, Burgess Shale (Canada) and Kaili Formation (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: molecular clock 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); first appearance datum (FAD) for trilobite-like traces (5), rhynchonelliform brachiopods (24), echinoderms (33), and trilobite body fossils (13); seawater chemistry (30, 34); and diversity of phyla (3), classes (3), and genera (10).

A Cambrian Origin for Trilobites

A Terreneuvian origin for trilobites contradicts previous inferences of a protracted Precambrian history (2, 14–16). Furthermore, our results are supported by evidence from the euarthropod trace fossil record and molecular clocks (Fig. 4). The oldest trilobite-like traces (e.g., Rusophycus) are early Fortunian in age (5, 9), and recent molecular clocks (e.g., ref. 31) place the origin of euarthropods in the late Ediacaran or earliest Cambrian. A conservative late Ediacaran root age for euarthropods still permits a Cambrian origin for trilobites, given their derived phylogenetic position within Euarthropoda (32).

The absence of Terreneuvian trilobite body fossils can be explained under two potential scenarios. The first scenario is that the fossil record is a reasonably accurate representation of early trilobite evolution, implying that rates of morphological evolution before 519 Ma were substantially faster than subsequently (SI Appendix, Table S1). This hypothesis forces rapid dispersal between widely separated paleocontinents and is difficult to reconcile with the provincialism observed in the earliest trilobites. However, if correct, this may also explain the perceived diachronism of the first trilobite fossils on different paleocontinents (12, 13), with the group potentially originating and rapidly radiating out from Siberia, West Laurentia, or West Gondwana (15, 16). The second scenario—more consistent with our results, plus trace fossil, molecular clock, and biogeographic data (5, 11)—is that the earliest trilobites (pre-521 Ma) have not been preserved or yet discovered in Terreneuvian rocks. The diversity of other skeletonized animals from a range of environments throughout the Terreneuvian (24, 30) indicates an adequate shelly fossil record. Thus, the absence of trilobites and indeed other euarthropod body fossils in Terreneuvian rocks could be explained by their nonbiomineralized exoskeletons and the unusual dearth of soft-tissue preservation (especially BST deposits) for this time interval (Fig. 4) (4, 5, 19).

The existence of nonbiomineralized trilobites in the Terreneuvian would have required multiple lineages to simultaneously converge upon a calcite exoskeleton at around 521 Ma, unless initial evolutionary rates were much faster, thus bringing their origin and fewer lineages closer to the lower boundary of Series 2 (in support of the first scenario discussed above). Synchronous biomineralization across two or more trilobite lineages is consistent with the observation that other disparate bilaterians, such as echinoderms and rhynchonelliform brachiopods, also acquired calcitic skeletons around this time (Fig. 4) (24, 33). Notably, this time coincides with a change in ocean chemistry, particularly the onset of a calcite sea (30, 34); ambient seawater chemistry influences the type of biomineral secreted 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/or biological factors [e.g., predation (30, 36)] were influencing this major episode of biomineralization and diversification during the final stages of the Cambrian explosion. The shelly fossil record of animals thus dramatically improves only around 521 Ma, but by that stage, the Cambrian explosion was largely over.