Evolutionary dynamics of the human pseudoautosomal regions

Abstract

Recombination between the X and Y human sex chromosomes is limited to the two pseudoautosomal regions (PARs) that present quite distinct evolutionary origins. Despite the crucial importance for male meiosis, genetic diversity patterns and evolutionary dynamics of these regions are poorly understood. In the present study, we analyzed and compared the genetic diversity of the PAR regions using publicly available genomic sequences encompassing both PAR1 and PAR2. Comparisons were performed through allele diversities, linkage disequilibrium status and recombination frequencies within and between X and Y chromosomes. In agreement with previous studies, we confirmed the role of PAR1 as a male-specific recombination hotspot, but also observed similar characteristic patterns of diversity in both regions although male recombination occurs at PAR2 to a much lower extent (at least one recombination event at PAR1 and in ≈1% in normal male meioses at PAR2). Furthermore, we demonstrate that both PARs harbor significantly different allele frequencies between X and Y chromosomes, which could support that recombination is not sufficient to homogenize the pseudoautosomal gene pool or is counterbalanced by other evolutionary forces. Nevertheless, the observed patterns of diversity are not entirely explainable by sexually antagonistic selection. A better understanding of such processes requires new data from intergenerational transmission studies of PARs, which would be decisive on the elucidation of PARs evolution and their role in male-driven heterosomal aneuploidies.

Fig 1. Distribution of heterozygosity along PARs at X and Y chromosomes.

Data from the 1kGP African population for polymorphic and non-polymorphic positions encompassing PAR1 and PAR2 at the X and Y chromosomes.

Fig 2. Distribution of allele frequency differences between X and Y chromosomes along PARs.

Allele frequency differences between the X and Y chromosomes for SNPs at PAR1 and PAR2 from the 1kGP African population.

Fig 3. Distribution of Fst between X and Y chromosomes along PARs.

Fst estimates between the X and Y chromosomes for SNPs at PAR1 and PAR2 from the 1kGP African population.

Fig 4. Estimated recombination rate in PAR1.

Average (A) and cumulative (B) recombination rate (ρ) at PAR1 and the immediately adjacent neighboring sex-specific region based on 180 female (orange) and male (blue) individuals from the 1kGP African population.

Fig 5. Estimated recombination rate in PAR2.

Average (A) and cumulative (B) recombination rate (ρ) at PAR2 and the immediately adjacent neighboring sex-specific region based on 180 female (orange) and male (blue) individuals of the 1kGP African population.