Life history effects on the molecular clock of autosomes and sex chromosomes
Guy Amster a,1 and Guy Sella a,1
aDepartment of Biological Sciences, Columbia University, New York, NY 10027
Edited by Michael Lynch, Indiana University, Bloomington, IN, and approved December 7, 2015 (received for review August 9, 2015)
Recent estimates of mutation rates obtained by sequencing human pedigrees have challenged conceptions about split times between humans and our closest living relatives. In particular, estimates of human split times from chimpanzees and gorillas based on the new mutation rate estimates are more than twofold shorter than previously believed, seemingly at odds with the fossil record. Here we show that accounting for the effects of sex-specific life histories on mutation rates along the hominid phylogeny largely bridges this apparent gap and leads to more accurate split time estimates. Doing so can also explain other intriguing phylogenetic patterns in hominid and mammalian evolution.
One of the foundational results in 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 hominids (great apes), considering a model that approximates features of the mutational process in mammals, birds, and some other vertebrates. As we show, this model can account for a number of seemingly disparate observations: notably, the puzzlingly low X-to-autosome ratios of substitution rates in humans and chimpanzees and differences in rates of autosomal substitutions among hominine lineages (i.e., humans, chimpanzees, and gorillas). The model further suggests how to translate pedigree-based estimates of human mutation rates into split times among extant hominoids (apes), given sex-specific life histories. In so doing, it largely bridges the gap reported between estimates of split times based on fossil and molecular evidence, in particular suggesting that the human–chimpanzee split may have occurred as recently as 6.6 Mya. The model also implies that the “generation time effect” should be stronger in short-lived species, explaining why the generation time has a major influence on yearly substitution rates in mammals but only a subtle one in human pedigrees.
molecular clock mutational slowdown generation time effect human–chimpanzee split male mutation bias
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Author contributions: G.A. and G.S. designed research; G.A. and G.S. performed research; and G.A. and G.S. wrote the paper.
The authors declare no conflict of interest.
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