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Predictable genome‐wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish

Genomic studies of parallel (or convergent) evolution often compare multiple populations diverged into two ecologically different habitats to search for loci repeatedly involved in adaptation. Because the shared ancestor of these populations is generally unavailable, the source of the alleles at ada...

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Autores principales: Haenel, Quiterie, Roesti, Marius, Moser, Dario, MacColl, Andrew D. C., Berner, Daniel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6369934/
https://www.ncbi.nlm.nih.gov/pubmed/30788140
http://dx.doi.org/10.1002/evl3.99
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author Haenel, Quiterie
Roesti, Marius
Moser, Dario
MacColl, Andrew D. C.
Berner, Daniel
author_facet Haenel, Quiterie
Roesti, Marius
Moser, Dario
MacColl, Andrew D. C.
Berner, Daniel
author_sort Haenel, Quiterie
collection PubMed
description Genomic studies of parallel (or convergent) evolution often compare multiple populations diverged into two ecologically different habitats to search for loci repeatedly involved in adaptation. Because the shared ancestor of these populations is generally unavailable, the source of the alleles at adaptation loci, and the direction in which their frequencies were shifted during evolution, remain elusive. To shed light on these issues, we here use multiple populations of threespine stickleback fish adapted to two different types of derived freshwater habitats—basic and acidic lakes on the island of North Uist, Outer Hebrides, Scotland—and the present‐day proxy of their marine ancestor. In a first step, we combine genome‐wide pooled sequencing and targeted individual‐level sequencing to demonstrate that ecological and phenotypic parallelism in basic‐acidic divergence is reflected by genomic parallelism in dozens of genome regions. Exploiting data from the ancestor, we next show that the acidic populations, residing in ecologically more extreme derived habitats, have adapted by accumulating alleles rare in the ancestor, whereas the basic populations have retained alleles common in the ancestor. Genomic responses to selection are thus predictable from the ecological difference of each derived habitat type from the ancestral one. This asymmetric sorting of standing genetic variation at loci important to basic‐acidic divergence has further resulted in more numerous selective sweeps in the acidic populations. Finally, our data suggest that the maintenance in marine fish of standing variation important to adaptive basic‐acidic differentiation does not require extensive hybridization between the marine and freshwater populations. Overall, our study reveals striking genome‐wide determinism in both the loci involved in parallel divergence, and in the direction in which alleles at these loci have been selected.
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spelling pubmed-63699342019-02-20 Predictable genome‐wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish Haenel, Quiterie Roesti, Marius Moser, Dario MacColl, Andrew D. C. Berner, Daniel Evol Lett Letters Genomic studies of parallel (or convergent) evolution often compare multiple populations diverged into two ecologically different habitats to search for loci repeatedly involved in adaptation. Because the shared ancestor of these populations is generally unavailable, the source of the alleles at adaptation loci, and the direction in which their frequencies were shifted during evolution, remain elusive. To shed light on these issues, we here use multiple populations of threespine stickleback fish adapted to two different types of derived freshwater habitats—basic and acidic lakes on the island of North Uist, Outer Hebrides, Scotland—and the present‐day proxy of their marine ancestor. In a first step, we combine genome‐wide pooled sequencing and targeted individual‐level sequencing to demonstrate that ecological and phenotypic parallelism in basic‐acidic divergence is reflected by genomic parallelism in dozens of genome regions. Exploiting data from the ancestor, we next show that the acidic populations, residing in ecologically more extreme derived habitats, have adapted by accumulating alleles rare in the ancestor, whereas the basic populations have retained alleles common in the ancestor. Genomic responses to selection are thus predictable from the ecological difference of each derived habitat type from the ancestral one. This asymmetric sorting of standing genetic variation at loci important to basic‐acidic divergence has further resulted in more numerous selective sweeps in the acidic populations. Finally, our data suggest that the maintenance in marine fish of standing variation important to adaptive basic‐acidic differentiation does not require extensive hybridization between the marine and freshwater populations. Overall, our study reveals striking genome‐wide determinism in both the loci involved in parallel divergence, and in the direction in which alleles at these loci have been selected. John Wiley and Sons Inc. 2019-01-23 /pmc/articles/PMC6369934/ /pubmed/30788140 http://dx.doi.org/10.1002/evl3.99 Text en © 2019 The Author(s). Evolution Letters published by Wiley Periodicals, Inc. 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
Haenel, Quiterie
Roesti, Marius
Moser, Dario
MacColl, Andrew D. C.
Berner, Daniel
Predictable genome‐wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish
title Predictable genome‐wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish
title_full Predictable genome‐wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish
title_fullStr Predictable genome‐wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish
title_full_unstemmed Predictable genome‐wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish
title_short Predictable genome‐wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish
title_sort predictable genome‐wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish
topic Letters
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6369934/
https://www.ncbi.nlm.nih.gov/pubmed/30788140
http://dx.doi.org/10.1002/evl3.99
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