Life history effects on the molecular clock of autosomes and sex chromosomes

Abstract

One of the foundational results of molecular evolution is that the rate at which neutral substitutions accumulate on a lineage equals the rate at which mutations arise. Traits that affect rates of mutation therefore also affect the phylogenetic \"molecular clock\". We consider the effects of sex-specific generation times and mutation rates in species with two sexes. In particular, we focus on the effects that the age of onset of male puberty and rates of spermatogenesis have likely had in extant hominines (i.e., human, chimpanzee and gorilla), considering a model that approximates features of the mutational process in most mammals and birds and some other vertebrates. As we show, this model helps explain and reconcile a number of seemingly puzzling observations. In hominines, it can explain the puzzlingly low X-to-autosome ratios of substitution rates and how the ratios and rates of autosomal substitutions differ among lineages. Importantly, it suggests how to translate pedigree-based estimates of human mutation rates into split times among apes, given sex-specific life histories. In so doing, it helps bridge the gap between estimates of split times of apes based on fossil and molecular evidence. Finally, considering these effects can help to reconcile recent evidence that changes in generation times should have small effects on mutation rates in humans with classic studies suggesting that they have had major effects on rates of evolution in the mammalian phylogeny.