Molecules and Fossils Tell Distinct Yet Complementary Stories of Mammal Diversification

Abstract

Reconstructing how biodiversity arose is a fundamental goal of evolutionary biologists. Yet whether the fossil record or time-calibrated phylogenies of living species yield comparable evolutionary rate estimates is controversial, and possibly affected by the temporal scale of question being asked. Here we investigate diversification timing across mammals by comparing rate signatures in a credible set of molecular timetrees (N =5,911 species, ~ 70% from DNA) to those in fossil genus durations (N =5,262). Fossil-corrected and timetree-based rate estimates begin converging ~23 million years ago (Ma) and are equal at the present, in accord with progressively fewer unsampled extinctions ‘pulling’ on the timetree rates toward the present to cause underestimates. ‘Pushing’ the pulled timetree rates by means of fossil-recorded extinctions identifies a major pulse of speciation ~60 Ma, soon after the Cretaceous-Paleogene mass extinction event, due to the radiation of fossil stem lineages. For groups without substantial fossil records, all is not lost, however. We show that species-specific ‘tip’ rates of speciation are unbiased estimators of recent evolutionary processes; in turn, the clade-level skewness of tip rates approximates the extent of past shifts in net diversification. Molecular timetrees need fossil-correction to address deep-time questions, but timetrees are sufficient for shallower time questions for which extinctions are fewer and ecological diversity can be fully sampled.