Genome architecture enables local adaptation of Atlantic cod despite high connectivity

Julia M I Barth, Paul R Berg, Per R. Jonsson, Sara Bonanomi, Hanna Corell, Jakob Hemmer Hansen, Kjetill S. Jakobsen, Kerstin Johannesson, Per Erik Jorde, Halvor Knutsen, Per-Olav Moksnes, Bastiaan Star, Nils Chr. Stenseth, Henrik Svedäng, Sissel Jentoft, Carl Andre

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Abstract

Adaptation to local conditions is a fundamental process in evolution; however, mechanisms maintaining local adaptation despite high gene flow are still poorly understood. Marine ecosystems provide a wide array of diverse habitats that frequently promote ecological adaptation even in species characterized by strong levels of gene flow. As one example, populations of the marine fish Atlantic cod (Gadus morhua) are highly connected due to immense dispersal capabilities but nevertheless show local adaptation in several key traits. By combining population genomic analyses based on 12K single-nucleotide polymorphisms with larval dispersal patterns inferred using a biophysical ocean model, we show that Atlantic cod individuals residing in sheltered estuarine habitats of Scandinavian fjords mainly belong to offshore oceanic populations with considerable connectivity between these diverse ecosystems. Nevertheless, we also find evidence for discrete fjord populations that are genetically differentiated from offshore populations, indicative of local adaptation, the degree of which appears to be influenced by connectivity. Analyses of the genomic architecture reveal a significant overrepresentation of a large ~5 Mb chromosomal rearrangement in fjord cod, previously proposed to comprise genes critical for the survival at low salinities. This suggests that despite considerable connectivity with offshore populations, local adaptation to fjord environments may be enabled by suppression of recombination in the rearranged region. Our study provides new insights into the potential of local adaptation in high gene flow species within fine geographical scales and highlights the importance of genome architecture in analyses of ecological adaptation. This article is protected by copyright. All rights reserved.
Original languageEnglish
JournalMolecular Ecology
Volume26
Issue number17
Pages (from-to)4452-4466
ISSN0962-1083
DOIs
Publication statusPublished - 2017

Keywords

  • Gadus morhua
  • chromosomal inversion
  • ecological adaptation
  • gene flow
  • population divergence

Cite this

Barth, J. M. I., Berg, P. R., Jonsson, P. R., Bonanomi, S., Corell, H., Hansen, J. H., ... Andre, C. (2017). Genome architecture enables local adaptation of Atlantic cod despite high connectivity. Molecular Ecology, 26(17), 4452-4466. https://doi.org/10.1111/mec.14207
Barth, Julia M I ; Berg, Paul R ; Jonsson, Per R. ; Bonanomi, Sara ; Corell, Hanna ; Hansen, Jakob Hemmer ; Jakobsen, Kjetill S. ; Johannesson, Kerstin ; Jorde, Per Erik ; Knutsen, Halvor ; Moksnes, Per-Olav ; Star, Bastiaan ; Stenseth, Nils Chr. ; Svedäng, Henrik ; Jentoft, Sissel ; Andre, Carl. / Genome architecture enables local adaptation of Atlantic cod despite high connectivity. In: Molecular Ecology. 2017 ; Vol. 26, No. 17. pp. 4452-4466.
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abstract = "Adaptation to local conditions is a fundamental process in evolution; however, mechanisms maintaining local adaptation despite high gene flow are still poorly understood. Marine ecosystems provide a wide array of diverse habitats that frequently promote ecological adaptation even in species characterized by strong levels of gene flow. As one example, populations of the marine fish Atlantic cod (Gadus morhua) are highly connected due to immense dispersal capabilities but nevertheless show local adaptation in several key traits. By combining population genomic analyses based on 12K single-nucleotide polymorphisms with larval dispersal patterns inferred using a biophysical ocean model, we show that Atlantic cod individuals residing in sheltered estuarine habitats of Scandinavian fjords mainly belong to offshore oceanic populations with considerable connectivity between these diverse ecosystems. Nevertheless, we also find evidence for discrete fjord populations that are genetically differentiated from offshore populations, indicative of local adaptation, the degree of which appears to be influenced by connectivity. Analyses of the genomic architecture reveal a significant overrepresentation of a large ~5 Mb chromosomal rearrangement in fjord cod, previously proposed to comprise genes critical for the survival at low salinities. This suggests that despite considerable connectivity with offshore populations, local adaptation to fjord environments may be enabled by suppression of recombination in the rearranged region. Our study provides new insights into the potential of local adaptation in high gene flow species within fine geographical scales and highlights the importance of genome architecture in analyses of ecological adaptation. This article is protected by copyright. All rights reserved.",
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author = "Barth, {Julia M I} and Berg, {Paul R} and Jonsson, {Per R.} and Sara Bonanomi and Hanna Corell and Hansen, {Jakob Hemmer} and Jakobsen, {Kjetill S.} and Kerstin Johannesson and Jorde, {Per Erik} and Halvor Knutsen and Per-Olav Moksnes and Bastiaan Star and Stenseth, {Nils Chr.} and Henrik Sved{\"a}ng and Sissel Jentoft and Carl Andre",
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Barth, JMI, Berg, PR, Jonsson, PR, Bonanomi, S, Corell, H, Hansen, JH, Jakobsen, KS, Johannesson, K, Jorde, PE, Knutsen, H, Moksnes, P-O, Star, B, Stenseth, NC, Svedäng, H, Jentoft, S & Andre, C 2017, 'Genome architecture enables local adaptation of Atlantic cod despite high connectivity', Molecular Ecology, vol. 26, no. 17, pp. 4452-4466. https://doi.org/10.1111/mec.14207

Genome architecture enables local adaptation of Atlantic cod despite high connectivity. / Barth, Julia M I; Berg, Paul R; Jonsson, Per R.; Bonanomi, Sara; Corell, Hanna; Hansen, Jakob Hemmer; Jakobsen, Kjetill S.; Johannesson, Kerstin ; Jorde, Per Erik; Knutsen, Halvor; Moksnes, Per-Olav; Star, Bastiaan; Stenseth, Nils Chr.; Svedäng, Henrik; Jentoft, Sissel; Andre, Carl.

In: Molecular Ecology, Vol. 26, No. 17, 2017, p. 4452-4466.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Genome architecture enables local adaptation of Atlantic cod despite high connectivity

AU - Barth, Julia M I

AU - Berg, Paul R

AU - Jonsson, Per R.

AU - Bonanomi, Sara

AU - Corell, Hanna

AU - Hansen, Jakob Hemmer

AU - Jakobsen, Kjetill S.

AU - Johannesson, Kerstin

AU - Jorde, Per Erik

AU - Knutsen, Halvor

AU - Moksnes, Per-Olav

AU - Star, Bastiaan

AU - Stenseth, Nils Chr.

AU - Svedäng, Henrik

AU - Jentoft, Sissel

AU - Andre, Carl

PY - 2017

Y1 - 2017

N2 - Adaptation to local conditions is a fundamental process in evolution; however, mechanisms maintaining local adaptation despite high gene flow are still poorly understood. Marine ecosystems provide a wide array of diverse habitats that frequently promote ecological adaptation even in species characterized by strong levels of gene flow. As one example, populations of the marine fish Atlantic cod (Gadus morhua) are highly connected due to immense dispersal capabilities but nevertheless show local adaptation in several key traits. By combining population genomic analyses based on 12K single-nucleotide polymorphisms with larval dispersal patterns inferred using a biophysical ocean model, we show that Atlantic cod individuals residing in sheltered estuarine habitats of Scandinavian fjords mainly belong to offshore oceanic populations with considerable connectivity between these diverse ecosystems. Nevertheless, we also find evidence for discrete fjord populations that are genetically differentiated from offshore populations, indicative of local adaptation, the degree of which appears to be influenced by connectivity. Analyses of the genomic architecture reveal a significant overrepresentation of a large ~5 Mb chromosomal rearrangement in fjord cod, previously proposed to comprise genes critical for the survival at low salinities. This suggests that despite considerable connectivity with offshore populations, local adaptation to fjord environments may be enabled by suppression of recombination in the rearranged region. Our study provides new insights into the potential of local adaptation in high gene flow species within fine geographical scales and highlights the importance of genome architecture in analyses of ecological adaptation. This article is protected by copyright. All rights reserved.

AB - Adaptation to local conditions is a fundamental process in evolution; however, mechanisms maintaining local adaptation despite high gene flow are still poorly understood. Marine ecosystems provide a wide array of diverse habitats that frequently promote ecological adaptation even in species characterized by strong levels of gene flow. As one example, populations of the marine fish Atlantic cod (Gadus morhua) are highly connected due to immense dispersal capabilities but nevertheless show local adaptation in several key traits. By combining population genomic analyses based on 12K single-nucleotide polymorphisms with larval dispersal patterns inferred using a biophysical ocean model, we show that Atlantic cod individuals residing in sheltered estuarine habitats of Scandinavian fjords mainly belong to offshore oceanic populations with considerable connectivity between these diverse ecosystems. Nevertheless, we also find evidence for discrete fjord populations that are genetically differentiated from offshore populations, indicative of local adaptation, the degree of which appears to be influenced by connectivity. Analyses of the genomic architecture reveal a significant overrepresentation of a large ~5 Mb chromosomal rearrangement in fjord cod, previously proposed to comprise genes critical for the survival at low salinities. This suggests that despite considerable connectivity with offshore populations, local adaptation to fjord environments may be enabled by suppression of recombination in the rearranged region. Our study provides new insights into the potential of local adaptation in high gene flow species within fine geographical scales and highlights the importance of genome architecture in analyses of ecological adaptation. This article is protected by copyright. All rights reserved.

KW - Gadus morhua

KW - chromosomal inversion

KW - ecological adaptation

KW - gene flow

KW - population divergence

U2 - 10.1111/mec.14207

DO - 10.1111/mec.14207

M3 - Journal article

VL - 26

SP - 4452

EP - 4466

JO - Molecular Ecology

JF - Molecular Ecology

SN - 0962-1083

IS - 17

ER -