Life history effects on neutral diversity levels of autosomes and sex chromosomes

Abstract All else being equal, the ratio of genetic diversity levels on X and autosomes at selectively neutral sites should mirror the ratio of their numbers in the population and thus equal ¾. Because X chromosomes spend twice as many generations in females as in males, however, the ratio of diversity levels is also affected by sex differences in life history. The effects of life history on diversity levels, notably those of sex-specific age structures and reproductive variances, have been studied for decades, yet existing theory relies on many parameters that are difficult to measure and lacks generality in ways that limit their applicability. We derive general yet simple expressions for these effects and show that life history effects on X-to-autosome (X:A) ratios of diversity levels depend only on sex-ratios of mutation rates, generation times, and reproductive variances. These results reveal that changing the sex-ratio of generation times has opposite effects on X:A ratios of polymorphism and divergence. They also explain how sex-specific life histories modulate the response of X:A polymorphism ratios to changes in population size. More generally, they clarify that sex-specific life history—generation times in particular—should have a marked effect on X:A polymorphism ratios in many taxa and enable the investigation of these effects. Significance Statement Understanding the determinants of neutral diversity patterns on autosomes and sex chromosomes provides a bedrock for our interpretation of population genetic data. Sex-specific age-structure and variation in reproductive success have long been thought to affect neutral diversity, but theoretical descriptions of these effects were complicated and/or lacked in generality, stymying attempts to relate diversity patterns of species with their life history. We derive general yet simple expressions for these effects, which clarify how they impact neutral diversity and should enable studies of relative diversity levels on the autosomes and sex chromosomes in many taxa.