Stabilizing selection on Atlantic cod supergenes through a millennium of extensive exploitation - PubMed
- ️Sat Jan 01 2022
. 2022 Feb 22;119(8):e2114904119.
doi: 10.1073/pnas.2114904119.
Sissel Jentoft 3 , Per Erik Jorde 2 , Morten Mattingsdal 4 , Jon Albretsen 2 , Alf Ring Kleiven 2 , Ann-Elin Wårøy Synnes 4 , Sigurd Heiberg Espeland 4 2 , Esben Moland Olsen 4 2 , Carl Andrè 5 , Nils Chr Stenseth 1 3 , Halvor Knutsen 1 2
Affiliations
- PMID: 35165196
- PMCID: PMC8872764
- DOI: 10.1073/pnas.2114904119
Stabilizing selection on Atlantic cod supergenes through a millennium of extensive exploitation
Marte Sodeland et al. Proc Natl Acad Sci U S A. 2022.
Abstract
Life on Earth has been characterized by recurring cycles of ecological stasis and disruption, relating biological eras to geological and climatic transitions through the history of our planet. Due to the increasing degree of ecological abruption caused by human influences many advocate that we now have entered the geological era of the Anthropocene, or "the age of man." Considering the ongoing mass extinction and ecosystem reshuffling observed worldwide, a better understanding of the drivers of ecological stasis will be a requisite for identifying routes of intervention and mitigation. Ecosystem stability may rely on one or a few keystone species, and the loss of such species could potentially have detrimental effects. The Atlantic cod (Gadus morhua) has historically been highly abundant and is considered a keystone species in ecosystems of the northern Atlantic Ocean. Collapses of cod stocks have been observed on both sides of the Atlantic and reported to have detrimental effects that include vast ecosystem reshuffling. By whole-genome resequencing we demonstrate that stabilizing selection maintains three extensive "supergenes" in Atlantic cod, linking these genes to species persistence and ecological stasis. Genomic inference of historic effective population sizes shows continued declines for cod in the North Sea-Skagerrak-Kattegat system through the past millennia, consistent with an early onset of the marine Anthropocene through industrialization and commercialization of fisheries throughout the medieval period.
Keywords: balancing selection; exploitation; genomics; inversions; marine.
Copyright © 2022 the Author(s). Published by PNAS.
Conflict of interest statement
The authors declare no competing interest.
Figures

(A) For each of 16 sampling locations, pies show frequencies of coastal cod (gray) and offshore cod (black) as determined by discriminant analysis on principal components using genome-wide distributed SNPs (excluding all SNPs on chromosomes 2, 7, and 12). (B) Bars show genotype frequencies (I/I in light color, I/II in intermediate color, and II/II in dark color) for supergenes SG02 (orange, Top), SG07 (burgundy, Middle), and SG12 (green, Bottom) in coastal cod and offshore cod within 16 sampling locations. Bars are ordered from left to right by increasing fraction of coastal cod relative to offshore cod within each sampling location.

Allele-frequency spectrums for SNPs within supergenes (A–C) SG02 (orange), (D–F) SG07 (burgundy), and (G–I) SG12 (green) and (J–L) genome-wide (gray) distributed SNPs (excluding all SNPs on chromosomes 2, 7, and 12) for coastal cod from locations LIL (A, D, G, and J), RIS (B, E, H, and K), and offshore cod from location NS1 (C, F, I, and L). Derived SNP allele frequencies are shown on the x axis, with relative fraction of SNPs on the y axis. For comparison with observed allele frequencies a theoretical distribution of allele frequencies under neutral equilibrium conditions is included as stippled lines.

Sliding-window analysis of Tajima’s D (A–C) and nucleotide diversity (D–F) was conducted for bins of 100 kb for coastal cod from locations LIL and RIS and for offshore cod from location NS1 across the 23 Atlantic cod chromosomes. Chromosomes 2, 7, and 12, harboring supergenes SG02, SG07, and SG12, are highlighted in orange, burgundy, and green, respectively.

Historic effective population sizes (Ne) were inferred from whole-genome resequencing data by Markovian coalescent for coastal cod (Middle) and offshore cod (Bottom) in the North Sea–Skagerrak–Kattegat system. Inference of historic Ne for generation times in the range of 2 to 7 y is shown (higher generation times depicted in darker shades of gray). Years before present are given on the x axis. (Top) Prehistoric and historic time periods in Northern Europe are indicated, with illustrations portraying the development of fisheries in the region.
Comment in
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Supergenes promote ecological stasis in a keystone species.
Wellenreuther M. Wellenreuther M. Trends Genet. 2022 Jul;38(7):629-631. doi: 10.1016/j.tig.2022.04.002. Epub 2022 Apr 26. Trends Genet. 2022. PMID: 35487824
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