Heritability of DNA methylation in threespine stickleback (Gasterosteus aculeatus).

Epigenetic mechanisms underlying phenotypic change are hypothesized to contribute to population persistence and adaptation in the face of environmental change. To date, few studies have explored the heritability of intergenerationally stable methylation levels in natural populations, and little is known about the relative contribution of cis- and trans-regulatory changes to methylation variation. Here, we explore the heritability of DNA methylation, and conduct methylation quantitative trait loci (meQTLs) analysis to investigate the genetic architecture underlying methylation variation between marine and freshwater ecotypes of threespine stickleback (Gasterosteus aculeatus). We quantitatively measured genome-wide DNA methylation in fin tissue using reduced representation bisulfite sequencing of F1 and F2 crosses, and their marine and freshwater source populations. We identified cytosines (CpG sites) that exhibited stable methylation levels across generations. We found that additive genetic variance explained an average of 24-35% of the methylation variance, with a number of CpG sites possibly autonomous from genetic control. We also detected both cis- and trans-meQTLs, with only trans-meQTLs overlapping with previously identified genomic regions of high differentiation between marine and freshwater ecotypes. Finally, we identified the genetic architecture underlying two key CpG sites that were differentially methylated between ecotypes. These findings demonstrate a potential role for DNA methylation in facilitating adaptation to divergent environments and improve our understanding of the heritable basis of population epigenomic variation.

A framework for understanding gene expression plasticity and its influence on stress tolerance.

Phenotypic plasticity can serve as a stepping stone towards adaptation. Recently, studies have shown that gene expression contributes to emergent stress responses such as thermal tolerance, with tolerant and susceptible populations showing distinct transcriptional profiles. However, given the dynamic nature of gene expression, interpreting transcriptomic results in a way that elucidates the functional connection between gene expression and the observed stress response is challenging. Here, we present a conceptual framework to guide interpretation of gene expression reaction norms in the context of stress tolerance. We consider the evolutionary and adaptive potential of gene expression reaction norms and discuss the influence of sampling timing, transcriptomic resilience, as well as complexities related to life history when interpreting gene expression dynamics and how these patterns relate to host tolerance. We highlight corals as a case study to demonstrate the value of this framework for non-model systems. As species face rapidly changing environmental conditions, modulating gene expression can serve as a mechanistic link from genetic and cellular processes to the physiological responses that allow organisms to thrive under novel conditions. Interpreting how or whether a species can employ gene expression plasticity to ensure short-term survival will be critical for understanding the global impacts of climate change across diverse taxa.