Cargando…
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 popul...
Autores principales: | , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9575207/ https://www.ncbi.nlm.nih.gov/pubmed/36253794 http://dx.doi.org/10.1186/s13059-022-02784-x |
_version_ | 1784811268036624384 |
---|---|
author | Bergman, Juraj Schierup, Mikkel Heide |
author_facet | Bergman, Juraj Schierup, Mikkel Heide |
author_sort | Bergman, Juraj |
collection | PubMed |
description | 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02784-x. |
format | Online Article Text |
id | pubmed-9575207 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-95752072022-10-18 Evolutionary dynamics of pseudoautosomal region 1 in humans and great apes Bergman, Juraj Schierup, Mikkel Heide Genome Biol Research 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02784-x. BioMed Central 2022-10-17 /pmc/articles/PMC9575207/ /pubmed/36253794 http://dx.doi.org/10.1186/s13059-022-02784-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Bergman, Juraj Schierup, Mikkel Heide Evolutionary dynamics of pseudoautosomal region 1 in humans and great apes |
title | Evolutionary dynamics of pseudoautosomal region 1 in humans and great apes |
title_full | Evolutionary dynamics of pseudoautosomal region 1 in humans and great apes |
title_fullStr | Evolutionary dynamics of pseudoautosomal region 1 in humans and great apes |
title_full_unstemmed | Evolutionary dynamics of pseudoautosomal region 1 in humans and great apes |
title_short | Evolutionary dynamics of pseudoautosomal region 1 in humans and great apes |
title_sort | evolutionary dynamics of pseudoautosomal region 1 in humans and great apes |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9575207/ https://www.ncbi.nlm.nih.gov/pubmed/36253794 http://dx.doi.org/10.1186/s13059-022-02784-x |
work_keys_str_mv | AT bergmanjuraj evolutionarydynamicsofpseudoautosomalregion1inhumansandgreatapes AT schierupmikkelheide evolutionarydynamicsofpseudoautosomalregion1inhumansandgreatapes |