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Genetic variation for upper thermal tolerance diminishes within and between populations with increasing acclimation temperature in Atlantic salmon

Abstract

Populations may counteract lasting temperature changes or recurrent extremes through plasticity or adaptation. However, it remains underexplored how outbreeding, either naturally, unintentionally, or facilitated, may modify a local response potential and whether genotype-by-environment interactions or between-trait correlations can restrict this potential. We quantified population differences and outbreeding effects, within-population genetic variation, and plasticity of these, for thermal performance proxy traits using 32 pedigreed wild, domesticated, and wild-domesticated Atlantic salmon families reared under common-garden conditions. Following exposure to ambient cold (11.6 °C) or ~4° and ~8° warmer summer temperatures, populations differed notably for body length and critical thermal maximum (CTmax) and for thermal plasticity of length, condition, and CTmax, but not for haematocrit. Line-cross analysis suggested mostly additive and some dominant outbreeding effects on means and solely additive outbreeding effects on plasticity. Heritability was detected for all traits. However, with increasing acclimation temperature, differences in CTmax between populations and CTmax heritability diminished, and CTmax breeding values re-ranked. Furthermore, CTmax and body size were negatively correlated at the genetic and phenotypic levels, and there was indirect evidence for a positive correlation between growth potential and thermal performance breadth for growth. Thus, population differences (including those between wild and domesticated populations) in thermal performance and plasticity may present a genetic resource in addition to the within-population genetic variance to facilitate, or impede, thermal adaptation. However, unfavourable genotype-by-environment interactions and negative between-trait correlations may generally hamper joint evolution in response to an increase in average temperature and temporary extremes.

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Fig. 1: Pedigree depicting breeding design and line plot showing experimental temperatures.
Fig. 2: Mean estimates and associated temperature-regime-specific additive outbreeding effect estimates among wild (W), reciprocal wild-domesticated (W × D), and domesticated (D) Atlantic salmon from three temperature regimes.
Fig. 3: Temperature-regime-pair-specific thermal plasticity estimates and associated additive genetic outbreeding effect estimates for thermal plasticity (αp) among wild (W), reciprocal wild-domesticated (W × D), and domesticated (D) Atlantic salmon from three temperature regimes.
Fig. 4: Temperature-regime-specific predicted breeding values (PBV; i.e., additive genetic effects) and their thermal plasticity.

Data availability

Underlying data is available at the Dryad repository: https://doi.org/10.5061/dryad.mgqnk98x9.

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Acknowledgements

We thank the Matre Research Station staff, Norway, for invaluably helping with fish husbandry, Torfinn Aga and Martin Peter Matre for CTmax-trial heating-system design, Kristine H. Holm, Julie Eikeland and Simon Flavell for size measurements, and Sofie Knutar for microsatellite analysis. We also thank Mowi for the domesticated salmon gamete supply and the volunteers in Etne for help with the wild broodstock collection and two anonymous referees for their suggestions in improving the manuscript. This study was financed by the Research Council of Norway project QuantEscape II (grant 254852). The authors declare no conflict of interest.

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Conceptualization: PVD, KAG, MFS; Methodology: PVD; Formal analysis: PVD; Investigation: MFS, PVD, IHM, LD; Resources: KAG, IHM, LD; Data Curation: PVD; Writing—original draft preparation: PVD; Writing—review and editing: PVD MFS, KAG, IHM, LD; Visualization: PVD; Project administration: KAG, MFS; Funding acquisition: KAG.

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Correspondence to Paul V. Debes.

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Debes, P.V., Solberg, M.F., Matre, I.H. et al. Genetic variation for upper thermal tolerance diminishes within and between populations with increasing acclimation temperature in Atlantic salmon. Heredity (2021). https://doi.org/10.1038/s41437-021-00469-y

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