Female-to-male breeding ratio in modern humans-an analysis based on historical recombinations

Abstract

Was the past genetic contribution of women and men to the current human population equal? Was polygyny (excess of breeding women) present among hominid lineages? We addressed these questions by measuring the ratio of population recombination rates between the X chromosome and the autosomes, rho(X)/rho(A). The X chromosome recombines only in female meiosis, whereas autosomes undergo crossovers in both sexes; thus, rho(X)/rho(A) reflects the female-to-male breeding ratio, beta. We estimated beta from rho(X)/rho(A) inferred from genomic diversity data and calibrated with recombination rates derived from pedigree data. For the HapMap populations, we obtained beta of 1.4 in the Yoruba from West Africa, 1.3 in Europeans, and 1.1 in East Asian samples. These values are consistent with a high prevalence of monogamy and limited polygyny in human populations. More mutations occur during male meiosis as compared to female meiosis at the rate ratio referred to as alpha. We show that at alpha not equal 1, the divergence rates and genetic diversities of the X chromosome relative to the autosomes are complex functions of both alpha and beta, making their independent estimation difficult. Because our estimator of beta does not require any knowledge of the mutation rates, our approach should allow us to dissociate the effects of alpha and beta on the genetic diversity and divergence rate ratios of the sex chromosomes to the autosomes.

Figure 1

Relationships among Population Size Ratio, Population Recombination Rate Ratio, and the Breeding Ratio The X chromosome to the autosomes effective population size ratio, N_eX/N_eA = δ (red line), and the corresponding population recombination rate ratio, ρ_X/ρ_A (blue line), are plotted as a function of the breeding ratio β = N_f/N_m. Note that the normalized recombination rate ratio, (ρ_X.r_A)/(ρ_A.r_X), is equivalent to ρ_X/ρ_A because in humans r_X/r_A = 1. The red and blue curves represent the following equations, respectively: $N_{eX}/N_{eA}=(9\beta +9)/(8\beta +16)$ and $({\rho }_X·r_A)/({\rho }_A·r_X)=9\beta \left(1+\beta \right)/4\left(2+\beta \right)\left(2\beta +1\right)$ (c.f Material and Methods).

Figure 2

Genetic Diversity Ratio and Divergence Ratio as a Function of the Breeding Ratio at Different Values of α Dependence of the X chromosome to the autosomes genetic diversity ratio Θ_X/Θ_A = 2(9β + 9)(2β + α)/(8β + 16)/(2β + 1)(α + 1) [A], and of the mutational divergence ratio $dX/dA=2\left(2\beta +\alpha \right)/\left(\alpha +1\right)\left(2\beta +1\right)$ [B] on the breeding ratio β for different α = μ_m/μ_f as indicated on the right of the graphs.