Linking Genes and the Environment: Differential DNA Methylation in Regulatory Regions is Associated With Rainbow Trout Migratory-Related Divergence

Migration is essential for the reproduction and survival of many animals, yet little is understood about its underlying molecular mechanisms. We used the salmonid Oncorhynchus mykiss to gain mechanistic insight into smoltification, which is a morphological, physiological, and behavioral transition undertaken by some juveniles that culminates in a seaward migration. Given that gene x environment interactions and phenotypic plasticity are likely critical components to migratory divergence, epigenetic modifications (e.g., DNA methylation) may regulate gene expression and partially underlie migratory phenotypic diversity. To explore this, we quantitatively measured genome-scale DNA methylation using reduced representation bisulfite sequencing of F₂ siblings produced from a cross between steelhead (migratory) and rainbow trout (non-migratory) lines. We identified 57 differentially methylated regions (DMRs) between steelhead and rainbow trout juveniles. DMRs were of high magnitude, ranging from 20-62% differential methylation between life history types, and over half of the gene-associated DMRs were in transcriptional regulatory regions. Many of the DMRs encode proteins with activity relevant to migratory-related transitions (e.g. circadian rhythm pathway, nervous system development, protein kinase activity). This study indicates that differential DNA methylation at gene regulatory elements may be a critical molecular mechanism allowing interactions between an organism and its environment to balance phenotypic stability and plasticity, and ultimately modify migratory-related phenotypes.