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Recurrent selection and reduction in recombination shape the genomic landscape of divergence across multiple population pairs of Green-backed Tit

Speciation is fundamental for building and maintaining biodiversity. The formation of the highly differentiated genomic regions between diverging taxa has been interpreted as a result of divergence with gene flow, linked selection, and reduction in recombination. It is challenging to unravel these n...

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Autores principales: Jiang, Zhiyong, Song, Gang, Luo, Xu, Zhang, Dezhi, Lei, Fumin, Qu, Yanhua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10078914/
https://www.ncbi.nlm.nih.gov/pubmed/37033875
http://dx.doi.org/10.1093/evlett/qrad005
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author Jiang, Zhiyong
Song, Gang
Luo, Xu
Zhang, Dezhi
Lei, Fumin
Qu, Yanhua
author_facet Jiang, Zhiyong
Song, Gang
Luo, Xu
Zhang, Dezhi
Lei, Fumin
Qu, Yanhua
author_sort Jiang, Zhiyong
collection PubMed
description Speciation is fundamental for building and maintaining biodiversity. The formation of the highly differentiated genomic regions between diverging taxa has been interpreted as a result of divergence with gene flow, linked selection, and reduction in recombination. It is challenging to unravel these nonexclusive processes in shaping genomic divergence. Here, we investigate the relative roles of these processes in shaping genomic differentiation in a montane bird, the Green-backed Tit (Parus monticolus). Our genetic structure and demographic analyses identify that four genetic lineages diverge between 838 and 113 thousand years ago and there is evidence of secondary gene flow. The highly divergent genomic regions do not increase with the divergence time, as we found that the old lineages show relatively fewer numbers and smaller sizes of highly differentiated regions than the young divergent lineages (numbers, 118–138 vs. 156–289; sizes, 5.9–6.9 vs. 7.8–14.5 megabase). Across the genome, the outlier windows show a reduction in nucleotide diversity, absolute genetic divergence, and recombination rate, suggesting recurrent selection in regions with low recombination being the major driver of genomic divergence. Finally, we show that secondary gene flow tends to affect the highly differentiated genomic regions if these regions are less likely to be the targets of selection. Altogether, our study shows how common ancestry, recurrent selection, low recombination rate, and gene flow have contributed to the emergence of genomic islands at different stages of speciation.
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spelling pubmed-100789142023-04-07 Recurrent selection and reduction in recombination shape the genomic landscape of divergence across multiple population pairs of Green-backed Tit Jiang, Zhiyong Song, Gang Luo, Xu Zhang, Dezhi Lei, Fumin Qu, Yanhua Evol Lett Letters Speciation is fundamental for building and maintaining biodiversity. The formation of the highly differentiated genomic regions between diverging taxa has been interpreted as a result of divergence with gene flow, linked selection, and reduction in recombination. It is challenging to unravel these nonexclusive processes in shaping genomic divergence. Here, we investigate the relative roles of these processes in shaping genomic differentiation in a montane bird, the Green-backed Tit (Parus monticolus). Our genetic structure and demographic analyses identify that four genetic lineages diverge between 838 and 113 thousand years ago and there is evidence of secondary gene flow. The highly divergent genomic regions do not increase with the divergence time, as we found that the old lineages show relatively fewer numbers and smaller sizes of highly differentiated regions than the young divergent lineages (numbers, 118–138 vs. 156–289; sizes, 5.9–6.9 vs. 7.8–14.5 megabase). Across the genome, the outlier windows show a reduction in nucleotide diversity, absolute genetic divergence, and recombination rate, suggesting recurrent selection in regions with low recombination being the major driver of genomic divergence. Finally, we show that secondary gene flow tends to affect the highly differentiated genomic regions if these regions are less likely to be the targets of selection. Altogether, our study shows how common ancestry, recurrent selection, low recombination rate, and gene flow have contributed to the emergence of genomic islands at different stages of speciation. Oxford University Press 2023-03-16 /pmc/articles/PMC10078914/ /pubmed/37033875 http://dx.doi.org/10.1093/evlett/qrad005 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEN). https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Letters
Jiang, Zhiyong
Song, Gang
Luo, Xu
Zhang, Dezhi
Lei, Fumin
Qu, Yanhua
Recurrent selection and reduction in recombination shape the genomic landscape of divergence across multiple population pairs of Green-backed Tit
title Recurrent selection and reduction in recombination shape the genomic landscape of divergence across multiple population pairs of Green-backed Tit
title_full Recurrent selection and reduction in recombination shape the genomic landscape of divergence across multiple population pairs of Green-backed Tit
title_fullStr Recurrent selection and reduction in recombination shape the genomic landscape of divergence across multiple population pairs of Green-backed Tit
title_full_unstemmed Recurrent selection and reduction in recombination shape the genomic landscape of divergence across multiple population pairs of Green-backed Tit
title_short Recurrent selection and reduction in recombination shape the genomic landscape of divergence across multiple population pairs of Green-backed Tit
title_sort recurrent selection and reduction in recombination shape the genomic landscape of divergence across multiple population pairs of green-backed tit
topic Letters
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10078914/
https://www.ncbi.nlm.nih.gov/pubmed/37033875
http://dx.doi.org/10.1093/evlett/qrad005
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