Trilobite evolutionary rates constrain the duration of the Cambrian explosion

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.

Keywords: Bayesian tip-dating; Cambrian explosion; evolutionary rates; morphological clock; trilobites.

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.

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).