Abstract
Populations may respond to environmental heterogeneity via evolutionary divergence or phenotypic plasticity. While evolutionary divergence occurs through DNA sequence differences among populations, plastic divergence among populations may be generated by changes in the epigenome. Here, we present the results of a genome‐wide comparison of DNA methylation patterns and genetic structure among four populations of Eastern oyster (Crassostrea virginica) in the northern Gulf of Mexico. We used a combination of restriction site‐associated DNA sequencing (RADseq) and reduced representation bisulfite sequencing (RRBS) to explore population structure, gene‐wide averages of F ST, and DNA methylation differences between oysters inhabiting four estuaries with unique salinity profiles. This approach identified significant population structure despite a moderately low F ST (0.02) across the freshwater boundary of the Mississippi river, a finding that may reflect recent efforts to restore oyster stock populations. Divergence between populations in CpG methylation was greater than for divergence in F ST, likely reflecting environmental effects on DNA methylation patterns. Assessment of CpG methylation patterns across all populations identified that only 26% of methylated DNA was intergenic; and, only 17% of all differentially methylated regions (DMRs) were within these same regions. DMRs within gene bodies between sites were associated with genes known to be involved in DNA damage repair, ion transport, and reproductive timing. Finally, when assessing the correlation between genomic variation and DNA methylation between these populations, we observed population‐specific DNA methylation profiles that were not directly associated with single nucleotide polymorphisms or broader gene‐body mean F ST trends. Our results suggest that C. virginica may use DNA methylation to generate environmentally responsive plastic phenotypes and that there is more divergence in methylation than divergence in allele frequencies.
Highlights
In highly variable marine environments, phenotypic plasticity allows organisms to persist in suboptimum environmental conditions (Somero, 2010)
The enrichment was among the broad category extracellular region. Genes associated with this ontology were hypermethylated in Vermilion Bay and may reflect differences in developmental stages between individuals at these sites. One caveat regarding these data is that the collections presented here was measured on individuals that had significant variation in size; growth rate in C.virginica is dependent on environmental conditions; attributing age based on size is not a dependable method when comparing oysters from estuaries known to differ in salinity
The differentially methylated regions (DMRs) identified here serve to highlight the diversity of methylation in the Eastern oyster and provide further evidence of the dynamic nature of CpG methylation in response to both environmental conditions and phenology
Summary
In highly variable marine environments, phenotypic plasticity allows organisms to persist in suboptimum environmental conditions (Somero, 2010). Examining the degree of genetic and epigenetic variation between populations of C. virginica that inhabit estuaries with distinct salinity conditions is an important step in understanding the observed signals of local adaptation and phenotypic plasticity in response to changes in environmental conditions along the northern GOM. We characterize single nucleotide polymorphisms and DNA methylation patterns for four populations of Eastern oysters (Crassostrea virginica) along the northern GOM This region is highly variable with respect to salinity, with shallow oyster reefs existing across regions with distinct annual salinity profiles (Figure 1). For the other two sites (LC and VB), all 20 individuals were measured and weighed; the labeling of these individuals was lost, and so, only mean length and mean wet weight are reported
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