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Rearing environment affects the genetic architecture and plasticity of DNA methylation in Chinook salmon

Abstract

Genetic architecture and phenotypic plasticity are important considerations when studying trait variation within and among populations. Since environmental change can induce shifts in the genetic architecture and plasticity of traits, it is important to consider both genetic and environmental sources of phenotypic variation. While there is overwhelming evidence for environmental effects on phenotype, the underlying mechanisms are less clear. Variation in DNA methylation is a potential mechanism mediating environmental effects on phenotype due to its sensitivity to environmental stimuli, transgenerational inheritance, and influences on transcription. To characterize the effect of environment on methylation, we created two 6 × 6 (North Carolina II) Chinook salmon breeding crosses and reared the offspring in two environments: uniform hatchery tanks and seminatural stream channels. We sampled the fish twice during development, at the alevin (larval) and fry (juvenile) stages. We measured DNA methylation at 13 genes using a PCR-based bisulfite sequencing protocol. The genetic architecture of DNA methylation differed between rearing environments, with greater additive and nonadditive genetic variance in hatchery fish and greater maternal effects in seminatural channel fish, though gene-specific variation was evident. We observed plasticity in methylation across all assayed genes, as well as gene-specific effects at two genes in alevin and six genes in fry, indicating developmental stage-specific effects of rearing environment on methylation. Characterizing genetic and environmental influences on methylation is critical for future studies on DNA methylation as a potential mechanism for acclimation and adaptation.

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Fig. 1: Bar graph showing the effects of rearing environment on additive (VA), nonadditive (VNA), and maternal (VM) variance components on gene-specific DNA methylation in Chinook salmon.
Fig. 2: Scatterplot comparing genetic variance components between rearing environments, with the 1:1 line plotted for reference.
Fig. 3: Reaction norm plots showing the effects of rearing environment on gene-specific DNA methylation in Chinook salmon alevin (top half) and fry (bottom half) full-sibling families.

Data availability

Bisulfite sequencing data have been made available on Dryad for both hatchery-reared fish (https://doi.org/10.5061/dryad.5x69p8d07) and semi-naturally reared fish (https://doi.org/10.5061/dryad.0k6djh9xf).

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Acknowledgements

The authors thank Drs John and Ann Heath of Yellow Island Aquaculture, Ltd (YIAL) for the use of their facilities, as well as Jane Drown for her assistance with sampling and experimental setup. We would like to thank Mitch Dender, Pauline Capelle, Stacey McIntyre, Calvin Kellendonk, Kim Mitchell, Nate Antoniolli, Megan Mickle, Dr. Dennis Higgs, Dr. Oliver Love, Dr. Natalie Sopinka, Sabrina Larsen, and Katarina Doughty for their assistance in the field. Experiments were conducted at YIAL. Funding was provided by YIAL and a Natural Science and Engineering Council Discovery Grant to DDH (grant number 814014).

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Venney, C.J., Wellband, K.W. & Heath, D.D. Rearing environment affects the genetic architecture and plasticity of DNA methylation in Chinook salmon. Heredity 126, 38–49 (2021). https://doi.org/10.1038/s41437-020-0346-4

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