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Research Article

Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic

View ORCID ProfileMalin L. Pinsky, Anne Maria Eikeset, Cecilia Helmerson, Ian R. Bradbury, View ORCID ProfilePaul Bentzen, View ORCID ProfileCorey Morris, Agata T. Gondek-Wyrozemska, View ORCID ProfileHelle Tessand Baalsrud, View ORCID ProfileMarine Servane Ono Brieuc, View ORCID ProfileOlav Sigurd Kjesbu, View ORCID ProfileJane A. Godiksen, View ORCID ProfileJulia M. I. Barth, Michael Matschiner, View ORCID ProfileNils Chr. Stenseth, View ORCID ProfileKjetill S. Jakobsen, View ORCID ProfileSissel Jentoft, and View ORCID ProfileBastiaan Star
  1. aDepartment of Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, NJ 08540;
  2. bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
  3. cScience Branch, Fisheries and Oceans Canada, St. John’s, NL A1C 5X1, Canada;
  4. dDepartment of Biology, Dalhousie University, Halifax, NS B3H 4R2, Canada;
  5. eMarine Ecosystems and Resources, Institute of Marine Research, NO-5817 Bergen, Norway;
  6. fDemersal Fish, Institute of Marine Research, NO-5817 Bergen, Norway;
  7. gZoological Institute, Department of Environmental Sciences, University of Basel, 4051 Basel, Switzerland;
  8. hDepartment of Palaeontology, University of Zurich, 8006 Zurich, Switzerland;
  9. iPalaeontological Museum, University of Zurich, 8006 Zurich, Switzerland;
  10. jCentre of Coastal Research, University of Agder, NO-4604 Kristiansand, Norway

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PNAS April 13, 2021 118 (15) e2025453118; https://doi.org/10.1073/pnas.2025453118
Malin L. Pinsky
aDepartment of Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, NJ 08540;
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  • ORCID record for Malin L. Pinsky
  • For correspondence: malin.pinsky@rutgers.edu n.c.stenseth@mn.uio.no bastiaan.star@ibv.uio.no
Anne Maria Eikeset
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
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Cecilia Helmerson
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
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Ian R. Bradbury
cScience Branch, Fisheries and Oceans Canada, St. John’s, NL A1C 5X1, Canada;
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Paul Bentzen
dDepartment of Biology, Dalhousie University, Halifax, NS B3H 4R2, Canada;
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  • ORCID record for Paul Bentzen
Corey Morris
cScience Branch, Fisheries and Oceans Canada, St. John’s, NL A1C 5X1, Canada;
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  • ORCID record for Corey Morris
Agata T. Gondek-Wyrozemska
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
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Helle Tessand Baalsrud
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
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  • ORCID record for Helle Tessand Baalsrud
Marine Servane Ono Brieuc
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
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  • ORCID record for Marine Servane Ono Brieuc
Olav Sigurd Kjesbu
eMarine Ecosystems and Resources, Institute of Marine Research, NO-5817 Bergen, Norway;
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  • ORCID record for Olav Sigurd Kjesbu
Jane A. Godiksen
fDemersal Fish, Institute of Marine Research, NO-5817 Bergen, Norway;
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  • ORCID record for Jane A. Godiksen
Julia M. I. Barth
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
gZoological Institute, Department of Environmental Sciences, University of Basel, 4051 Basel, Switzerland;
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  • ORCID record for Julia M. I. Barth
Michael Matschiner
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
hDepartment of Palaeontology, University of Zurich, 8006 Zurich, Switzerland;
iPalaeontological Museum, University of Zurich, 8006 Zurich, Switzerland;
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Nils Chr. Stenseth
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
jCentre of Coastal Research, University of Agder, NO-4604 Kristiansand, Norway
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  • ORCID record for Nils Chr. Stenseth
  • For correspondence: malin.pinsky@rutgers.edu n.c.stenseth@mn.uio.no bastiaan.star@ibv.uio.no
Kjetill S. Jakobsen
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
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Sissel Jentoft
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
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Bastiaan Star
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Blindern, NO-0316 Oslo, Norway;
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  • ORCID record for Bastiaan Star
  • For correspondence: malin.pinsky@rutgers.edu n.c.stenseth@mn.uio.no bastiaan.star@ibv.uio.no
  1. Contributed by Nils Chr. Stenseth, March 2, 2021 (sent for review January 8, 2021; reviewed by Tom Gilbert and Michael Knapp)

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Significance

Both theory and experiments suggest that fishing can drive the evolution of an earlier maturation age. However, determining whether changes in the wild are the result of fisheries-induced evolution has been difficult. Temporal, genome-wide datasets can directly reveal responses to selection. Here, we investigate the genomes of two wild Atlantic cod populations from samples that pre- and postdate periods of intensive fishing. Although phenotypic changes suggest fisheries-induced evolution, we do not find evidence for any strong genomic change or loss of genetic diversity. While evolution could have occurred through undetectable frequency changes at many loci, the irreversible loss of late-maturing genotypes appears unlikely. Instead, we suggest that recovery of former phenotypes is possible with reduced fishing pressure.

Abstract

The mode and extent of rapid evolution and genomic change in response to human harvesting are key conservation issues. Although experiments and models have shown a high potential for both genetic and phenotypic change in response to fishing, empirical examples of genetic responses in wild populations are rare. Here, we compare whole-genome sequence data of Atlantic cod (Gadus morhua) that were collected before (early 20th century) and after (early 21st century) periods of intensive exploitation and rapid decline in the age of maturation from two geographically distinct populations in Newfoundland, Canada, and the northeast Arctic, Norway. Our temporal, genome-wide analyses of 346,290 loci show no substantial loss of genetic diversity and high effective population sizes. Moreover, we do not find distinct signals of strong selective sweeps anywhere in the genome, although we cannot rule out the possibility of highly polygenic evolution. Our observations suggest that phenotypic change in these populations is not constrained by irreversible loss of genomic variation and thus imply that former traits could be reestablished with demographic recovery.

  • fisheries-induced evolution
  • population genomics
  • genetic diversity
  • selective sweeps
  • historical DNA

Footnotes

  • ↵1To whom correspondence may be addressed. Email: malin.pinsky{at}rutgers.edu, n.c.stenseth{at}mn.uio.no, or bastiaan.star{at}ibv.uio.no.
  • Author contributions: M.L.P., A.M.E., O.S.K., N.C.S., K.S.J., S.J., and B.S. designed research; A.T.G.-W. and B.S. performed research; M.L.P., I.R.B., P.B., C.M., H.T.B., O.S.K., J.A.G., S.J., and B.S. contributed new materials/analytic tools; M.L.P., C.H., J.M.I.B., M.M., and B.S. curated data; M.L.P. and B.S. analyzed data; M.L.P. and B.S. wrote the paper with input from A.M.E., C.H., H.T.B., M.S.O.B., O.S.K., J.A.G., J.M.I.B., M.M., N.C.S., K.S.J., and S.J.; and historical samples were provided by I.R.B., P.B., C.M., O.S.K., and J.A.G.

  • Reviewers: T.G., University of Copenhagen; and M.K., University of Otago.

  • The authors declare no competing interest.

  • See online for related content such as Commentaries.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2025453118/-/DCSupplemental.

Data Availability

Analysis scripts and associated data reported in this article are archived as a Git repository through Zenodo at https://doi.org/10.5281/zenodo.4554375. Raw sequencing reads for the historical and modern samples reported in this article are available at the European Nucleotide Archive (project no. PRJEB41431).

  • Copyright © 2021 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic
Malin L. Pinsky, Anne Maria Eikeset, Cecilia Helmerson, Ian R. Bradbury, Paul Bentzen, Corey Morris, Agata T. Gondek-Wyrozemska, Helle Tessand Baalsrud, Marine Servane Ono Brieuc, Olav Sigurd Kjesbu, Jane A. Godiksen, Julia M. I. Barth, Michael Matschiner, Nils Chr. Stenseth, Kjetill S. Jakobsen, Sissel Jentoft, Bastiaan Star
Proceedings of the National Academy of Sciences Apr 2021, 118 (15) e2025453118; DOI: 10.1073/pnas.2025453118

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Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic
Malin L. Pinsky, Anne Maria Eikeset, Cecilia Helmerson, Ian R. Bradbury, Paul Bentzen, Corey Morris, Agata T. Gondek-Wyrozemska, Helle Tessand Baalsrud, Marine Servane Ono Brieuc, Olav Sigurd Kjesbu, Jane A. Godiksen, Julia M. I. Barth, Michael Matschiner, Nils Chr. Stenseth, Kjetill S. Jakobsen, Sissel Jentoft, Bastiaan Star
Proceedings of the National Academy of Sciences Apr 2021, 118 (15) e2025453118; DOI: 10.1073/pnas.2025453118
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Proceedings of the National Academy of Sciences: 118 (15)
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