(Epi)genomic adaptation driven by fine geographical scale environmental heterogeneity after recent biological invasions

Abstract

Elucidating processes and mechanisms involved in rapid local adaptation to varied environments is a poorly understood but crucial component in management of invasive species. Recent studies have proposed that genetic and epigenetic variation could both contribute to ecological adaptation, yet it remains unclear on the interplay between these two components underpinning rapid adaptation in wild animal populations. To assess their respective contributions to local adaptation, we explored epigenomic and genomic responses to environmental heterogeneity in eight recently colonized ascidian (Ciona intestinalis) populations at a relatively fine geographical scale. Based on MethylRADseq data, we detected strong patterns of local environment‐driven DNA methylation divergence among populations, significant epigenetic isolation by environment (IBE), and a large number of local environment‐associated epigenetic loci. Meanwhile, multiple genetic analyses based on single nucleotide polymorphisms (SNPs) showed genomic footprints of divergent selection. In addition, for five genetically similar populations, we detected significant methylation divergence and local environment‐driven methylation patterns, indicating the strong effects of local environments on epigenetic variation. From a functional perspective, a majority of functional genes, Gene Ontology (GO) terms, and biological pathways were largely specific to one of these two types of variation, suggesting partial independence between epigenetic and genetic adaptation. The methylation quantitative trait loci (mQTL) analysis showed that the genetic variation explained only 18.67% of methylation variation, further confirming the autonomous relationship between these two types of variation. Altogether, we highlight the complementary interplay of genetic and epigenetic variation involved in local adaptation, which may jointly promote populations' rapid adaptive capacity and successful invasions in different environments. The findings here provide valuable insights into interactions between invaders and local environments to allow invasive species to rapidly spread, thus contributing to better prediction of invasion success and development of management strategies.

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

“…temperature or salinity) have previously been reported in various invertebrates 24-28 , 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. Complementary approaches in invertebrates and vertebrates have shown that 27% of inter-individual epigenetic variation is genotype-dependent 27 and 24–35% of epigenetic variation is explained by additive genetic components 30 .…”

“…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. Complementary approaches in invertebrates and vertebrates have shown that 27% of interindividual epigenetic variation is genotype dependent (28) and 24-35% of the epigenetic variation is explained by additive genetic components (31).…”

Perspectives of invasive alien species management in China

“…Rapid adaptive evolution is typically associated with genetic and epigenetic changes, but the interplay between these two components underlying rapid adaptation in invasive species remains unclear. Chen et al (2023) found that the complementary interplay of genetic and epigenetic variation was involved in the local adaptation of a marine invasive model ascidian ( Ciona intestinalis ). This complementary interplay collectively promoted the rapid adaptive capacity of populations, enabling successful invasions in different environments.…”