Complementary genomic and epigenomic adaptation to environmental heterogeneity

Abstract

While adaptation is commonly thought to result from selection on DNA sequencebased variation, recent studies have highlighted an analogous epigenetic component as well. However, the relative roles of these mechanisms in facilitating population persistence under environmental heterogeneity remain unclear. To address the underlying genetic and epigenetic mechanisms and their relationship during environmental adaptation, we screened the genomes and epigenomes of nine global populations of a predominately sessile marine invasive tunicate, Botryllus schlosseri. We detected clear population differentiation at the genetic and epigenetic levels. Patterns of genetic and epigenetic structure were significantly influenced by local environmental variables. Among these variables, minimum annual sea surface temperature was identified as the top explanatory variable for both genetic and epigenetic variation. However, patterns of population structure driven by genetic and epigenetic variation were somewhat distinct, suggesting possible autonomy of epigenetic variation. We found both shared and specific genes and biological pathways among genetic and epigenetic loci associated with environmental factors, consistent with complementary and independent contributions of genetic and epigenetic variation to environmental adaptation in this system. Collectively, these mechanisms may facilitate population persistence under environmental change and sustain successful invasions across novel environments.

Genome‐scale signatures of adaptive gene expression changes in an invasive seaweed Gracilaria vermiculophylla

“…These molecular and epigenetic regulations may contribute to the emergence of new adaptive traits and genotypes in new habitats (Drenovsky et al, 2012; Green et al, 2020). As compared to terrestrial systems (Mounger et al, 2021; Xu et al, 2019), understanding these patterns in marine systems has not been explored to the same extent (Gao et al, 2022; Huang, Li, et al, 2017).…”

Epigenetic then genetic variations underpin rapid adaptation of oyster populations (Crassostrea gigas) to Pacific Oyster Mortality Syndrome (POMS)

“…Significant associations between genetic or epigenetic variation and environmental parameters (e.g. temperature or salinity) have previously been reported in various invertebrates [24][25][26][27][28] , with significant correlation between genetic and epigenetic variation found in six of 14 studies reviewed 29 . Analyses of genetic control of epigenetic variation using methQTL have found that the fraction of epigenetic variation under direct control of DNA sequence variation 25,27,30 is highly variable, ranging from 2% in the threespine stickleback (Gasterosteus aculeatus) 30 , 3% in the Olympia oyster (Ostrea lurida) 27 , 19% in Ciona intestinalis 25 , 70% in human (Homo sapiens) 31,32 , and 88% in this study.…”

Epigenetic variations are more substantial than genetic variations in rapid adaptation of oyster to Pacific oyster mortality syndrome

“…Significant associations between genetic or epigenetic variation and environmental parameters (e.g., temperature or salinity) have previously been reported in various invertebrates (25)(26)(27)(28)(29), with a significant correlation between genetic and epigenetic variation found in 6 of 14 studies reviewed (30). MethQTL mapping revealed that the fraction of epigenetic variation associated with DNA sequence variation (26,28,31) is highly variable, ranging from 2% in the threespine stickleback (Gasterosteus aculeatus) (31), 3% in the Olympia oyster (Ostrea lurida) (28), 19% in Ciona intestinalis (26), 70% in human (Homo sapiens) (32,33), and 88% in this study.…”