Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)

Abstract

Epigenetic inheritance can result in plastic responses to changing environments being faithfully transmitted to offspring. However, it remains unclear how epigenetic mechanisms such as DNA methylation can contribute to multigenerational acclimation and adaptation to environmental stressors. Brook charr ( Salvelinus fontinalis ), an economically important salmonid, is highly sensitive to thermal stress and is of conservation concern in the context of climate change. We studied the effects of temperature during parental sexual maturation and offspring rearing on whole-genome DNA methylation in brook charr juveniles (fry). Parents were split between warm and cold temperatures during sexual maturation, mated in controlled breeding designs, then offspring from each family were split between warm (8°C) and cold (5°C) rearing environments. Using whole-genome bisulfite sequencing, we found 188 differentially methylated regions (DMRs) due to parental maturation temperature after controlling for family structure. By contrast, offspring rearing temperature had a negligible effect on offspring methylation. Stable intergenerational inheritance of DNA methylation and minimal plasticity in progeny could result in the transmission of acclimatory epigenetic states to offspring, priming them for a warming environment. Our findings have implications pertaining to the role of intergenerational epigenetic inheritance in response to ongoing climate change.

DNA methylation differences during development distinguish sympatric morphs of Arctic charr (Salvelinus alpinus)

“…This study was done on embryos reared in the same experimental conditions, from multiple parents per morph caught in the wild. Because of this, and the fact that we established pure families and only one generation, we could not test for parental effects or disentangle the influence of genetic and environmental components, as was recently done by Venney et al (2022). The observed methylation differences could thus be the result of multiple factors.…”

“…Multiple epigenetic mechanisms acting across generations have been described, such as epi-alleles, maternal provisioning and metabolism, or sncRNAs in sperm [mainly tsRNAs (Peng et al, 2012) and miRNA (see Perez & Lehner, 2019)], all of which could possibly impact DNA methylation profiles of the offspring. In fish, specific cytosine methylation has been associated with maternal effects in Chinook salmon (Venney et al, 2020), parental maturation temperature corresponded with DNA methylation patterns in the offspring of Brook charr (Venney et al, 2022) and egg size has already been correlated with craniofacial shape at first feeding in this S. alpinus model (Beck et al, 2020). It would be very interesting to study parental effects and transgenerational epigenetic inheritance (see Baerwald et al, 2016;Heckwolf et al, 2020), with a multigeneration scheme and crosses (for instance, pure and reciprocal crosses of different morphs), for further inquiry into these potential causes.…”

Transcriptomic responses to within- and transgenerational environmental warming in a cold-adapted salmonid

“…egg provisioning and transfer of sperm cell cytoplasmic components) and epigenetics (Dai et al 2020; Spadafora 2020; Venney et al 2020). For example, brook trout ( S. fontinalis ) offspring incurred more differentially methylated regions due to transgenerational warm-acclimation than with within-generation warm-acclimation (Venney et al 2022). In the current study, maternal and paternal warm-acclimation separately elevated DEGs functioning in the DNA damage response ( DDIT4 ) and heat shock proteins (maternal only: HSPB1 , HSPB7 ).…”

“…The copyright holder for this preprint this version posted October 22, 2022. ; https://doi.org/10. 1101/2022 with what their offspring are expected to experience (Bernatchez 2016;Ashe et al 2021). For example, TGP could be beneficial in a population that experiences environmental warming over multiple generations whereby the offspring are phenotypically "primed" for a warmer environment (Donelan et al 2020;McCaw et al 2020;Venney et al 2022).…”

“…TGP can potentially be beneficial when a parent’s environment coincides with what their offspring are expected to experience (Bernatchez 2016; Ashe et al 2021). For example, TGP could be beneficial in a population that experiences environmental warming over multiple generations whereby the offspring are phenotypically “primed” for a warmer environment (Donelan et al 2020; McCaw et al 2020; Venney et al 2022). In the context of climate change, this phenotypic priming could buffer the effects of rapid warming, allowing additional time for evolutionary processes to occur (Bernatchez 2016; Ashe et al 2021), though the extent to which TGP can be considered adaptive is arguable (Uller et al 2013; Sánchez-Tójar et al 2020).…”