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Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species

Speciation is one of the most important processes in biology, yet the study of the genomic changes underlying this process is in its infancy. North American warbler species Setophaga townsendi and Setophaga occidentalis hybridize in a stable hybrid zone, following a period of geographic separation....

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Autores principales: Wang, Silu, Rohwer, Sievert, de Zwaan, Devin R., Toews, David P. L., Lovette, Irby J., Mackenzie, Jacqueline, Irwin, Darren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7719548/
https://www.ncbi.nlm.nih.gov/pubmed/33312686
http://dx.doi.org/10.1002/evl3.198
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author Wang, Silu
Rohwer, Sievert
de Zwaan, Devin R.
Toews, David P. L.
Lovette, Irby J.
Mackenzie, Jacqueline
Irwin, Darren
author_facet Wang, Silu
Rohwer, Sievert
de Zwaan, Devin R.
Toews, David P. L.
Lovette, Irby J.
Mackenzie, Jacqueline
Irwin, Darren
author_sort Wang, Silu
collection PubMed
description Speciation is one of the most important processes in biology, yet the study of the genomic changes underlying this process is in its infancy. North American warbler species Setophaga townsendi and Setophaga occidentalis hybridize in a stable hybrid zone, following a period of geographic separation. Genomic differentiation accumulated during geographic isolation can be homogenized by introgression at secondary contact, whereas genetic regions that cause low hybrid fitness can be shielded from such introgression. Here, we examined the genomic underpinning of speciation by investigating (1) the genetic basis of divergent pigmentation traits between species, (2) variation in differentiation across the genome, and (3) the evidence for selection maintaining differentiation in the pigmentation genes. Using tens of thousands of single nucleotide polymorphisms (SNPs) genotyped in hundreds of individuals within and near the hybrid zone, genome‐wide association mapping revealed a single SNP associated with cheek, crown, breast coloration, and flank streaking, reflecting pleiotropy (one gene affecting multiple traits) or close physical linkage of different genes affecting different traits. This SNP is within an intron of the RALY gene, hence we refer to it as the RALY SNP. We then examined between‐species genomic differentiation, using both genotyping‐by‐sequencing and whole genome sequencing. We found that the RALY SNP is within one of the highest peaks of differentiation, which contains three genes known to influence pigmentation: ASIP, EIF2S2, and RALY (the ASIP‐RALY gene block). Heterozygotes at this gene block are likely of reduced fitness, as the geographic cline of the RALY SNP has been narrow over two decades. Together, these results reflect at least one barrier to gene flow within this narrow (∼200 kb) genomic region that modulates plumage difference between species. Despite extensive gene flow between species across the genome, this study provides evidence that selection on a phenotype‐associated genomic region maintains a stable species boundary.
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spelling pubmed-77195482020-12-11 Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species Wang, Silu Rohwer, Sievert de Zwaan, Devin R. Toews, David P. L. Lovette, Irby J. Mackenzie, Jacqueline Irwin, Darren Evol Lett Letters Speciation is one of the most important processes in biology, yet the study of the genomic changes underlying this process is in its infancy. North American warbler species Setophaga townsendi and Setophaga occidentalis hybridize in a stable hybrid zone, following a period of geographic separation. Genomic differentiation accumulated during geographic isolation can be homogenized by introgression at secondary contact, whereas genetic regions that cause low hybrid fitness can be shielded from such introgression. Here, we examined the genomic underpinning of speciation by investigating (1) the genetic basis of divergent pigmentation traits between species, (2) variation in differentiation across the genome, and (3) the evidence for selection maintaining differentiation in the pigmentation genes. Using tens of thousands of single nucleotide polymorphisms (SNPs) genotyped in hundreds of individuals within and near the hybrid zone, genome‐wide association mapping revealed a single SNP associated with cheek, crown, breast coloration, and flank streaking, reflecting pleiotropy (one gene affecting multiple traits) or close physical linkage of different genes affecting different traits. This SNP is within an intron of the RALY gene, hence we refer to it as the RALY SNP. We then examined between‐species genomic differentiation, using both genotyping‐by‐sequencing and whole genome sequencing. We found that the RALY SNP is within one of the highest peaks of differentiation, which contains three genes known to influence pigmentation: ASIP, EIF2S2, and RALY (the ASIP‐RALY gene block). Heterozygotes at this gene block are likely of reduced fitness, as the geographic cline of the RALY SNP has been narrow over two decades. Together, these results reflect at least one barrier to gene flow within this narrow (∼200 kb) genomic region that modulates plumage difference between species. Despite extensive gene flow between species across the genome, this study provides evidence that selection on a phenotype‐associated genomic region maintains a stable species boundary. John Wiley and Sons Inc. 2020-10-19 /pmc/articles/PMC7719548/ /pubmed/33312686 http://dx.doi.org/10.1002/evl3.198 Text en © 2020 The Authors. Evolution Letters published by Wiley Periodicals, LLC on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB). This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Letters
Wang, Silu
Rohwer, Sievert
de Zwaan, Devin R.
Toews, David P. L.
Lovette, Irby J.
Mackenzie, Jacqueline
Irwin, Darren
Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species
title Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species
title_full Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species
title_fullStr Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species
title_full_unstemmed Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species
title_short Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species
title_sort selection on a small genomic region underpins differentiation in multiple color traits between two warbler species
topic Letters
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7719548/
https://www.ncbi.nlm.nih.gov/pubmed/33312686
http://dx.doi.org/10.1002/evl3.198
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