Population Epigenetics: The Extent of DNA Methylation Variation in Wild Animal Populations

Abstract

Population epigenetics explores the extent of epigenetic variation and its dynamics in natural populations encountering changing environmental conditions. In contrast to population genetics, the basic concepts of this field are still in their early stages, especially in animal populations. Epigenetic variation may play a crucial role in phenotypic plasticity and local adaptation as it can be affected by the environment, it is likely to have higher spontaneous mutation rate than nucleotide sequences do, and it may be inherited via non-mendelian processes. In this review, we aim to bring together natural animal population epigenetic studies to generate new insights into ecological epigenetics and its evolutionary implications. We first provide an overview of the extent of DNA methylation variation and its autonomy from genetic variation in wild animal population. Second, we discuss DNA methylation dynamics which create observed epigenetic population structures by including basic population genetics processes. Then, we highlight the relevance of DNA methylation variation as an evolutionary mechanism in the extended evolutionary synthesis. Finally, we suggest new research directions by highlighting gaps in the knowledge of the population epigenetics field. As for our results, DNA methylation diversity was found to reveal parameters that can be used to characterize natural animal populations. Some concepts of population genetics dynamics can be applied to explain the observed epigenetic structure in natural animal populations. The set of recent advancements in ecological epigenetics, especially in transgenerational epigenetic inheritance in wild animal population, might reshape the way ecologists generate predictive models of the capacity of organisms to adapt to changing environments.

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 – 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.…”

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 24-28 , 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.…”

Population genetics and phylogeographic history of the insular lizardPodarcis lilfordi(Gunther, 1874) from the Balearic Islands based on genome-wide polymorphic data

“…Moreover, most genes with outliers were associated with protein binding and catalytic activities and were involved in metabolic and growth processes (Figure S3), critical molecular functions for gene expression regulation and phenotypic diversification (Van Nostrand et al, 2020). In small, isolated populations, extensive modulation of gene expression conferring phenotypic plasticity could represent a major mechanism to counteract the loss of genetic diversity (Fulgione et al, 2023; Sherpa et al, 2023), a hypothesis that needs to be validated by whole transcriptome and epigenome data (Chapelle and Silvestre, 2022; Fulgione et al, 2023).…”