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Genome-wide signatures of synergistic epistasis during parallel adaptation in a Baltic Sea copepod

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  • David B. Stern

    (University of Wisconsin-Madison
    National Biodefense Analysis and Countermeasures Center (NBACC), Operated by Battelle National Biodefense Institute (BNBI) for the U.S. Department of Homeland Security Science and Technology Directorate)

  • Nathan W. Anderson

    (University of Wisconsin-Madison)

  • Juanita A. Diaz

    (University of Wisconsin-Madison)

  • Carol Eunmi Lee

    (University of Wisconsin-Madison)

Abstract

The role of epistasis in driving adaptation has remained an unresolved problem dating back to the Evolutionary Synthesis. In particular, whether epistatic interactions among genes could promote parallel evolution remains unexplored. To address this problem, we employ an Evolve and Resequence (E&R) experiment, using the copepod Eurytemora affinis, to elucidate the evolutionary genomic response to rapid salinity decline. Rapid declines in coastal salinity at high latitudes are a predicted consequence of global climate change. Based on time-resolved pooled whole-genome sequencing, we uncover a remarkably parallel, polygenic response across ten replicate selection lines, with 79.4% of selected alleles shared between lines by the tenth generation of natural selection. Using extensive computer simulations of our experiment conditions, we find that this polygenic parallelism is consistent with positive synergistic epistasis among alleles, far more so than other mechanisms tested. Our study provides experimental and theoretical support for a novel mechanism promoting repeatable polygenic adaptation, a phenomenon that may be common for selection on complex physiological traits.

Suggested Citation

  • David B. Stern & Nathan W. Anderson & Juanita A. Diaz & Carol Eunmi Lee, 2022. "Genome-wide signatures of synergistic epistasis during parallel adaptation in a Baltic Sea copepod," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31622-8
    DOI: 10.1038/s41467-022-31622-8
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    as
    1. Molly K. Burke & Joseph P. Dunham & Parvin Shahrestani & Kevin R. Thornton & Michael R. Rose & Anthony D. Long, 2010. "Genome-wide analysis of a long-term evolution experiment with Drosophila," Nature, Nature, vol. 467(7315), pages 587-590, September.
    2. Moises Exposito-Alonso & Hernán A. Burbano & Oliver Bossdorf & Rasmus Nielsen & Detlef Weigel, 2019. "Natural selection on the Arabidopsis thaliana genome in present and future climates," Nature, Nature, vol. 573(7772), pages 126-129, September.
    3. Moises Exposito-Alonso & Hernán A. Burbano & Oliver Bossdorf & Rasmus Nielsen & Detlef Weigel, 2019. "Publisher Correction: Natural selection on the Arabidopsis thaliana genome in present and future climates," Nature, Nature, vol. 574(7778), pages 16-16, October.
    4. Peter D. Keightley & Sarah P. Otto, 2006. "Interference among deleterious mutations favours sex and recombination in finite populations," Nature, Nature, vol. 443(7107), pages 89-92, September.
    5. Bates, Douglas & Mächler, Martin & Bolker, Ben & Walker, Steve, 2015. "Fitting Linear Mixed-Effects Models Using lme4," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i01).
    6. Reid S. Brennan & James A. deMayo & Hans G. Dam & Michael B. Finiguerra & Hannes Baumann & Melissa H. Pespeni, 2022. "Loss of transcriptional plasticity but sustained adaptive capacity after adaptation to global change conditions in a marine copepod," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    7. Maxime Lenormand & Franck Jabot & Guillaume Deffuant, 2013. "Adaptive approximate Bayesian computation for complex models," Computational Statistics, Springer, vol. 28(6), pages 2777-2796, December.
    8. Jeremy J Berg & Graham Coop, 2014. "A Population Genetic Signal of Polygenic Adaptation," PLOS Genetics, Public Library of Science, vol. 10(8), pages 1-25, August.
    9. Felicity C. Jones & Manfred G. Grabherr & Yingguang Frank Chan & Pamela Russell & Evan Mauceli & Jeremy Johnson & Ross Swofford & Mono Pirun & Michael C. Zody & Simon White & Ewan Birney & Stephen Sea, 2012. "The genomic basis of adaptive evolution in threespine sticklebacks," Nature, Nature, vol. 484(7392), pages 55-61, April.
    10. Chris Todd Hittinger & Paula Gonçalves & José Paulo Sampaio & Jim Dover & Mark Johnston & Antonis Rokas, 2010. "Remarkably ancient balanced polymorphisms in a multi-locus gene network," Nature, Nature, vol. 464(7285), pages 54-58, March.
    11. M. C. Bitter & L. Kapsenberg & J.-P. Gattuso & C. A. Pfister, 2019. "Standing genetic variation fuels rapid adaptation to ocean acidification," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    12. David Reich & Kumarasamy Thangaraj & Nick Patterson & Alkes L. Price & Lalji Singh, 2009. "Reconstructing Indian population history," Nature, Nature, vol. 461(7263), pages 489-494, September.
    13. Joseph K Pickrell & Jonathan K Pritchard, 2012. "Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data," PLOS Genetics, Public Library of Science, vol. 8(11), pages 1-17, November.
    Full references (including those not matched with items on IDEAS)

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