Migration-related phenotypic divergence is associated with epigenetic modifications in rainbow trout

Abstract

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 behavioural transition undertaken by juveniles in preparation for seaward migration. O. mykiss is experimentally tractable and displays intra- and interpopulation variation in migration propensity. Migratory individuals can produce nonmigratory progeny and vice versa, indicating a high degree of phenotypic plasticity. One potential way that phenotypic plasticity might be linked to variation in migration-related life history tactics is through epigenetic regulation of gene expression. To explore this, we quantitatively measured genome-scale DNA methylation in fin tissue using reduced representation bisulphite sequencing of F2 siblings produced from a cross between steelhead (migratory) and rainbow trout (nonmigratory) lines. We identified 57 differentially methylated regions (DMRs) between smolt and resident O. mykiss juveniles. DMRs were high in magnitude, with up to 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 migration-related transitions (e.g. circadian rhythm pathway, nervous system development, protein kinase activity). This study provides the first evidence of a relationship between epigenetic variation and life history divergence associated with migration-related traits in any species.

Keywords: Oncorhynchus mykiss; epigenetics; life history variation; plasticity; smoltification.

Fig. 1. Phenotypic differences between resident and smolt O. mykiss juveniles

Photographs of siblings with alternative life history types were taken on same date and age (June, age 2). Smolts are silvery and streamlined in body shape, while residents are darker in skin and fin coloration and have dark parr marks on the sides of their bodies.

Fig. 2. Hierarchical clustering of hyper- and hypo-methylated DMRs for divergent migration-related phenotypes

This heatmap graphically displays the percent DNA methylation for each individual at the 57 DMRs. Each column represents a color-coded individual: green for residents and blue for smolts. Each row represents a differentially methylated region when comparing the two life history phenotypes. The darker the red, the more methylated that individual is for that DMR. Individual dendrogram positions are based on their overall methylation patterns across the 57 DMRs. DMRs below a minimum read depth of 10 were excluded and are represented as grey boxes.

Fig. 3. Differential DNA methylation distinguishes residents and smolts

Three gene-associated DMR examples at the base-pair resolution. Points (blue=resident, red=smolt) represent DNA methylation levels of individual samples at every CpG site within the DMR and smoothed lines represent average DNA methylation levels for each life history type.

Fig. 4. Genomic features of the 57 migration-related DMRs for O. mykiss

(a) Seven chromosomes contain two or more DMRs. (b) Approximately half (29) of the DMRs are found within or proximal to CpG islands. (c) Over half (31) of the DMRs are found within gene bodies or proximal regulatory elements.