TY - JOUR
T1 - Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species
AU - Wang, Silu
AU - Rohwer, Sievert
AU - de Zwaan, Devin R.
AU - Toews, David P.L.
AU - Lovette, Irby J.
AU - Mackenzie, Jacqueline
AU - Irwin, Darren
N1 - Funding Information:
R. Midgley and E. Mikkelsen provided excellent assistance in the field and lab for this study. We thank C. Wood (Burke Museum) for help relocating the historical sites and accessing the historical plumage samples, and S. Birks (Burke Museum) for accessing tissue samples for sequencing. S. Otto, A. MacPherson, D. Chen, D. Schluter, L. Rieseberg, A. Geraldes, T. Booker, T. Bradshaw, and members of the Irwin Lab provided helpful discussion. We thank research funding provided by the Natural Sciences and Engineering Research Council of Canada (grants 311931–2012, RGPIN‐2017‐03919, and RGPAS‐2017‐507830 to DEI and PGS D 331015731 to SW), the Cornell Lab of Ornithology, a Werner and Hildegard Hesse Research Award in Ornithology, and a UBC Four Year Doctoral Fellowship to SW. Finally, we thank Environment Canada, U.S. Geological Survey, Departments of Fish and Wildlife of Washington, Oregon, California, Idaho, and Montana, and the UBC Animal Care Committee for providing research permits. We thank J. Slate, Z. Gompert, and five anonymous reviewers for Evolution Letters for helpful comments on the manuscript.
Funding Information:
R. Midgley and E. Mikkelsen provided excellent assistance in the field and lab for this study. We thank C. Wood (Burke Museum) for help relocating the historical sites and accessing the historical plumage samples, and S. Birks (Burke Museum) for accessing tissue samples for sequencing. S. Otto, A. MacPherson, D. Chen, D. Schluter, L. Rieseberg, A. Geraldes, T. Booker, T. Bradshaw, and members of the Irwin Lab provided helpful discussion. We thank research funding provided by the Natural Sciences and Engineering Research Council of Canada (grants 311931–2012, RGPIN-2017-03919, and RGPAS-2017-507830 to DEI and PGS D 331015731 to SW), the Cornell Lab of Ornithology, a Werner and Hildegard Hesse Research Award in Ornithology, and a UBC Four Year Doctoral Fellowship to SW. Finally, we thank Environment Canada, U.S. Geological Survey, Departments of Fish and Wildlife of Washington, Oregon, California, Idaho, and Montana, and the UBC Animal Care Committee for providing research permits. We thank J. Slate, Z. Gompert, and five anonymous reviewers for Evolution Letters for helpful comments on the manuscript.
Publisher Copyright:
© 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).
PY - 2020/12
Y1 - 2020/12
N2 - 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.
AB - 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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U2 - 10.1002/evl3.198
DO - 10.1002/evl3.198
M3 - Letter
AN - SCOPUS:85097889251
SN - 2056-3744
VL - 4
SP - 502
EP - 515
JO - Evolution Letters
JF - Evolution Letters
IS - 6
ER -