Evolutionary dynamics of pseudoautosomal region 1 in humans and great apes

Background The pseudoautosomal region 1 (PAR1) is a 2.7 Mb telomeric region of human sex chromosomes. PAR1 has a crucial role in ensuring proper segregation of sex chromosomes during male meiosis, exposing it to extreme recombination and mutation processes. We investigate PAR1 evolution using population genomic datasets of extant humans, eight populations of great apes, and two archaic human genome sequences. Results We find that PAR1 is fast evolving and closer to evolutionary nucleotide equilibrium than autosomal telomeres. We detect a difference between substitution patterns and extant diversity in PAR1, mainly driven by the conflict between strong mutation and recombination-associated fixation bias at CpG sites. We detect excess C-to-G mutations in PAR1 of all great apes, specific to the mutagenic effect of male recombination. Despite recent evidence for Y chromosome introgression from humans into Neanderthals, we find that the Neanderthal PAR1 retained similarity to the Denisovan sequence. We find differences between substitution spectra of these archaics suggesting rapid evolution of PAR1 in recent hominin history. Frequency analysis of alleles segregating in females and males provided no evidence for recent sexual antagonism in this region. We study repeat content and double-strand break hotspot regions in PAR1 and find that they may play roles in ensuring the obligate X-Y recombination event during male meiosis. Conclusions Our study provides an unprecedented quantification of population genetic forces governing PAR1 biology across extant and extinct hominids. PAR1 evolutionary dynamics are predominantly governed by recombination processes with a strong impact on mutation patterns across all species.

Automated summary

This study provides a comprehensive analysis of the evolutionary dynamics of the pseudoautosomal region 1 (PAR1) in both extant and extinct hominids. PAR1 is found to evolve rapidly and is primarily influenced by recombination processes. The mutation patterns in PAR1 also differ among species, with an excess of C-to-G mutations associated with male recombination. Despite evidence of Y chromosome introgression from humans to Neanderthals, the PAR1 region in Neanderthals remains similar to the Denisovan sequence. Repeat content and double-strand break hotspot regions in PAR1 may play crucial roles in ensuring proper recombination between the X and Y chromosomes during male meiosis.