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Dynamic evolution of great ape Y chromosomes

The mammalian male-specific Y chromosome plays a critical role in sex determination and male fertility. However, because of its repetitive and haploid nature, it is frequently absent from genome assemblies and remains enigmatic. The Y chromosomes of great apes represent a particular puzzle: their ge...

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Autores principales: Cechova, Monika, Vegesna, Rahulsimham, Tomaszkiewicz, Marta, Harris, Robert S., Chen, Di, Rangavittal, Samarth, Medvedev, Paul, Makova, Kateryna D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7585023/
https://www.ncbi.nlm.nih.gov/pubmed/33020265
http://dx.doi.org/10.1073/pnas.2001749117
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author Cechova, Monika
Vegesna, Rahulsimham
Tomaszkiewicz, Marta
Harris, Robert S.
Chen, Di
Rangavittal, Samarth
Medvedev, Paul
Makova, Kateryna D.
author_facet Cechova, Monika
Vegesna, Rahulsimham
Tomaszkiewicz, Marta
Harris, Robert S.
Chen, Di
Rangavittal, Samarth
Medvedev, Paul
Makova, Kateryna D.
author_sort Cechova, Monika
collection PubMed
description The mammalian male-specific Y chromosome plays a critical role in sex determination and male fertility. However, because of its repetitive and haploid nature, it is frequently absent from genome assemblies and remains enigmatic. The Y chromosomes of great apes represent a particular puzzle: their gene content is more similar between human and gorilla than between human and chimpanzee, even though human and chimpanzee share a more recent common ancestor. To solve this puzzle, here we constructed a dataset including Ys from all extant great ape genera. We generated assemblies of bonobo and orangutan Ys from short and long sequencing reads and aligned them with the publicly available human, chimpanzee, and gorilla Y assemblies. Analyzing this dataset, we found that the genus Pan, which includes chimpanzee and bonobo, experienced accelerated substitution rates. Pan also exhibited elevated gene death rates. These observations are consistent with high levels of sperm competition in Pan. Furthermore, we inferred that the great ape common ancestor already possessed multicopy sequences homologous to most human and chimpanzee palindromes. Nonetheless, each species also acquired distinct ampliconic sequences. We also detected increased chromatin contacts between and within palindromes (from Hi-C data), likely facilitating gene conversion and structural rearrangements. Our results highlight the dynamic mode of Y chromosome evolution and open avenues for studies of male-specific dispersal in endangered great ape species.
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spelling pubmed-75850232020-10-30 Dynamic evolution of great ape Y chromosomes Cechova, Monika Vegesna, Rahulsimham Tomaszkiewicz, Marta Harris, Robert S. Chen, Di Rangavittal, Samarth Medvedev, Paul Makova, Kateryna D. Proc Natl Acad Sci U S A Biological Sciences The mammalian male-specific Y chromosome plays a critical role in sex determination and male fertility. However, because of its repetitive and haploid nature, it is frequently absent from genome assemblies and remains enigmatic. The Y chromosomes of great apes represent a particular puzzle: their gene content is more similar between human and gorilla than between human and chimpanzee, even though human and chimpanzee share a more recent common ancestor. To solve this puzzle, here we constructed a dataset including Ys from all extant great ape genera. We generated assemblies of bonobo and orangutan Ys from short and long sequencing reads and aligned them with the publicly available human, chimpanzee, and gorilla Y assemblies. Analyzing this dataset, we found that the genus Pan, which includes chimpanzee and bonobo, experienced accelerated substitution rates. Pan also exhibited elevated gene death rates. These observations are consistent with high levels of sperm competition in Pan. Furthermore, we inferred that the great ape common ancestor already possessed multicopy sequences homologous to most human and chimpanzee palindromes. Nonetheless, each species also acquired distinct ampliconic sequences. We also detected increased chromatin contacts between and within palindromes (from Hi-C data), likely facilitating gene conversion and structural rearrangements. Our results highlight the dynamic mode of Y chromosome evolution and open avenues for studies of male-specific dispersal in endangered great ape species. National Academy of Sciences 2020-10-20 2020-10-05 /pmc/articles/PMC7585023/ /pubmed/33020265 http://dx.doi.org/10.1073/pnas.2001749117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Cechova, Monika
Vegesna, Rahulsimham
Tomaszkiewicz, Marta
Harris, Robert S.
Chen, Di
Rangavittal, Samarth
Medvedev, Paul
Makova, Kateryna D.
Dynamic evolution of great ape Y chromosomes
title Dynamic evolution of great ape Y chromosomes
title_full Dynamic evolution of great ape Y chromosomes
title_fullStr Dynamic evolution of great ape Y chromosomes
title_full_unstemmed Dynamic evolution of great ape Y chromosomes
title_short Dynamic evolution of great ape Y chromosomes
title_sort dynamic evolution of great ape y chromosomes
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7585023/
https://www.ncbi.nlm.nih.gov/pubmed/33020265
http://dx.doi.org/10.1073/pnas.2001749117
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