Rates of Molecular Evolution Suggest Natural History of Life History Traits and a Post-K-Pg Nocturnal Bottleneck of Placentals

Abstract

Life history and behavioral traits are often difficult to discern from the fossil record, but evolutionary rates of genes and their changes over time can be inferred from extant genomic data. Under the neutral theory, molecular evolutionary rate is a product of mutation rate and the proportion of neutral mutations [1, 2]. Mutation rates may be shared across the genome, whereas proportions of neutral mutations vary among genes because functional constraints vary. By analyzing evolutionary rates of 1,185 genes in a phylogeny of 89 mammals, we extracted historical profiles of functional constraints on these rates in the form of gene-branch interactions. By applying a novel statistical approach to these profiles, we reconstructed the history of ten discrete traits related to activity, diet, and social behaviors. Our results indicate that the ancestor of placental mammals was solitary,seasonally breeding, insectivorous, and likely nocturnal. The results suggest placental diversification began 10-20 million years before the K-Pg boundary (66 million years ago), with some ancestors of extant placental mammals becoming diurnal and adapted to different diets. However, from the Paleocene to the Eocene-Oligocene transition (EOT, 33.9 mya), we detect a post-K-Pg nocturnal bottleneck where all ancestral lineages of extant placentals were nocturnal. Although diurnal placentals may have existed during the elevated global temperatures of the Paleocene-Eocene thermal maximum [3], we hypothesize that diurnal placentals were selectively extirpated during or after the global cooling of the EOT, whereas some nocturnal lineages survived due to preadaptations to cold environments [4].