Rates of Phenotypic and Genomic Evolution during the Cambrian Explosion

Abstract

The near-simultaneous appearance of most modern animal body plans (phyla) ~530 million years ago during the Cambrian explosion is strong evidence for a brief interval of rapid phenotypic and genetic innovation, yet the exact speed and nature of this grand adaptive radiation remain debated. Crucially, rates of morphological evolution in the past (i.e., in ancestral lineages) can be inferred from phenotypic differences among living organisms-just as molecular evolutionary rates in ancestral lineages can be inferred from genetic divergences. We here employed Bayesian and maximum likelihood phylogenetic clock methods on an extensive anatomical and genomic data set for arthropods, the most diverse phylum in the Cambrian and today. Assuming an Ediacaran origin for arthropods, phenotypic evolution was ~4 times faster, and molecular evolution ~5.5 times faster, during the Cambrian explosion compared to all subsequent parts of the Phanerozoic. These rapid evolutionary rates are robust to assumptions about the precise age of arthropods. Surprisingly, these fast early rates do not change substantially even if the radiation of arthropods is compressed entirely into the Cambrian (~542 mega-annum [Ma]) or telescoped into the Cryogenian (~650 Ma). The fastest inferred rates are still consistent with evolution by natural selection and with data from living organisms, potentially resolving "Darwin's dilemma." However, evolution during the Cambrian explosion was unusual (compared to the subsequent Phanerozoic) in that fast rates were present across many lineages.