Pervasive Genomic Signatures of Local Adaptation to Altitude Across Highland Specialist Andean Hummingbird Populations
Abstract Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the...
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Published in | The Journal of heredity Vol. 112; no. 3; pp. 229 - 240 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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Oxford University Press
24.05.2021
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Abstract | Abstract
Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them “taller” biogeographic barriers. |
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AbstractList | Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species,
Coeligena violifer
(
n
= 62) and
Colibri coruscans
(
n
= 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them “taller” biogeographic barriers. Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them "taller" biogeographic barriers. Abstract Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them “taller” biogeographic barriers. Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them "taller" biogeographic barriers.Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow, and genetic drift. In montane systems, where species are often restricted to narrow ranges of elevation, it is unclear whether the selection is strong enough to influence functional differentiation of subpopulations differing by a few hundred meters in elevation. We used targeted capture of 12 501 exons from across the genome, including 271 genes previously implicated in altitude adaptation, to test for adaptation to local elevations for 2 highland hummingbird species, Coeligena violifer (n = 62) and Colibri coruscans (n = 101). For each species, we described population genetic structure across the complex geography of the Peruvian Andes and, while accounting for this structure, we tested whether elevational allele frequency clines in single nucleotide polymorphisms (SNPs) showed evidence for local adaptation to elevation. Although the 2 species exhibited contrasting population genetic structures, we found signatures of clinal genetic variation with shifts in elevation in both. The genes with SNP-elevation associations included candidate genes previously discovered for high-elevation adaptation as well as others not previously identified, with cellular functions related to hypoxia response, energy metabolism, and immune function, among others. Despite the homogenizing effects of gene flow and genetic drift, natural selection on parts of the genome evidently optimizes elevation-specific cellular function even within elevation range-restricted montane populations. Consequently, our results suggest local adaptation occurring in narrow elevation bands in tropical mountains, such as the Andes, may effectively make them "taller" biogeographic barriers. |
Author | Graham, Catherine H Dávalos, Liliana M Witt, Christopher C Bi, Ke Lim, Marisa C W |
AuthorAffiliation | 1 Department of Ecology and Evolution, Stony Brook University , Stony Brook, NY 4 Museum of Southwestern Biology and Department of Biology, University of New Mexico , Albuquerque, NM 2 Museum of Vertebrate Zoology, University of California , Berkeley, CA 5 Swiss Federal Research Institute (WSL) , Birmensdorf , Switzerland 3 California Institute for Quantitative Biosciences, University of California Berkeley , Berkeley, CA (Bi) 6 Consortium for Inter-Disciplinary Environmental Research, Stony Brook University , Stony Brook, NY |
AuthorAffiliation_xml | – name: 1 Department of Ecology and Evolution, Stony Brook University , Stony Brook, NY – name: 2 Museum of Vertebrate Zoology, University of California , Berkeley, CA – name: 4 Museum of Southwestern Biology and Department of Biology, University of New Mexico , Albuquerque, NM – name: 3 California Institute for Quantitative Biosciences, University of California Berkeley , Berkeley, CA (Bi) – name: 6 Consortium for Inter-Disciplinary Environmental Research, Stony Brook University , Stony Brook, NY – name: 5 Swiss Federal Research Institute (WSL) , Birmensdorf , Switzerland |
Author_xml | – sequence: 1 givenname: Marisa C W orcidid: 0000-0003-2097-8818 surname: Lim fullname: Lim, Marisa C W email: marisa_lim@pacbell.net organization: Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY – sequence: 2 givenname: Ke surname: Bi fullname: Bi, Ke organization: Museum of Vertebrate Zoology, University of California, Berkeley, CA – sequence: 3 givenname: Christopher C surname: Witt fullname: Witt, Christopher C organization: Museum of Southwestern Biology and Department of Biology, University of New Mexico, Albuquerque, NM – sequence: 4 givenname: Catherine H surname: Graham fullname: Graham, Catherine H organization: Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY – sequence: 5 givenname: Liliana M orcidid: 0000-0002-4327-7697 surname: Dávalos fullname: Dávalos, Liliana M organization: Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33631009$$D View this record in MEDLINE/PubMed |
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Keywords | gene flow clinal variation high-elevation exon capture |
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08:esaf044. doi: 10.1093/jhered/esaf044. |
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Snippet | Abstract
Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing... Populations along steep environmental gradients are subject to differentiating selection that can result in local adaptation, despite countervailing gene flow,... |
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StartPage | 229 |
SubjectTerms | Acclimatization - genetics Altitude Animals Birds - genetics Editor's Choice Gene Flow Genomics Original Peru Polymorphism, Single Nucleotide |
Title | Pervasive Genomic Signatures of Local Adaptation to Altitude Across Highland Specialist Andean Hummingbird Populations |
URI | https://www.ncbi.nlm.nih.gov/pubmed/33631009 https://www.proquest.com/docview/2494296731 https://pubmed.ncbi.nlm.nih.gov/PMC8427717 |
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