Can a sex-biased human demography account for the reduced effective population size of chromosome X in non-Africans?

Abstract

Sex-biased demographic events can result in asymmetries in female and male effective population size that can lead to different patterns of genetic variation on chromosome X than are expected based on the patterns on the autosomes. Previous studies point to a period around the time of the dispersal of anatomically modern humans out of Africa when chromosome X experienced a significant reduction in effective population size relative to the autosomes. Here, we explore whether a sex-biased demographic history could explain these observations. We use coalescent simulations to show that a model of primarily male migration during the out-of-Africa dispersal can produce the striking patterns that are observed when comparing patterns of genetic variation on the autosomes and chromosome X. The model involves a history in which after the founder population of non-Africans lost much of its genetic diversity, subsequent mostly male gene flow from an African source brought new diversity into the population. We also explore two additional models, one of sex-biased generation time and one of a substructured population during the dispersal out of Africa with primarily female migration among demes. These latter models cannot account for the magnitude of the observed reduction in chromosome X effective population size, although it is plausible that they played a more minor role in producing the striking chromosome X/autosome patterns.

FIG. 1.

Model of sex-biased migration during the dispersal of modern humans from Africa. The figure outlines the primarily male migration model, a detailed description of which is provided in Materials and Methods. N_ancestral is the ancestral N_e, N_African the African N_e, and N_non-African the N_e of the ancestral population of North Europeans; t is the split time of the African and non-African populations; F is the severity of the out-of-Africa population bottleneck; g denotes the number of generations migration lasted following the bottleneck; m denotes its rate; and p the proportion of migrants who were male.

FIG. 2.

Signatures of X-autosome asymmetry decay over tens of thousands of generations after primarily male migration. The figure shows the Q and T ratios as a function of varying the time since the dispersal out of Africa t within the model of primarily male migration. A range of times consistent with the split of Africans and non-African populations is illustrated by the vertical band (40,000–80,000 years ago of 20–30 years per generation; the baseline model discussed in the main text is at the middle of that range). The signals captured by the two different ratios exhibit different behavior with time, but both are predicted to be very strong at present time and to practically vanish by 35,000 generations (∼875,000 years) after the event. (The horizontal dotted line provides the ¾ prediction of a sex-symmetric history of constant N_e.)