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

Abstract

Disease emergence is accelerating with global changes. Understanding by which mechanisms host populations can rapidly adapt will be crucial for management practices. Pacific oyster mortality syndrome (POMS) imposes a substantial and recurrent selective pressure on oyster populations, and rapid adaptation may arise through genetics and epigenetics. In this study, we used (epi)genome-wide association mapping to show that oysters differentially exposed to POMS displayed genetic and epigenetic signatures of selection. Consistent with higher resistance to POMS, the genes targeted included many genes in several pathways related to immunity. By combining correlation, DNA methylation quantitative trait loci, and variance partitioning, we revealed that a third of phenotypic variation was explained by interactions between the genetic and epigenetic information, ~14% by the genome, and up to 25% by the epigenome alone. Similar to genetically based adaptation, epigenetic mechanisms notably governing immune responses can contribute substantially to the rapid adaptation of hosts to emerging infectious diseases.

Microbial education plays a crucial role in harnessing the beneficial properties of microbiota for infectious disease protection inCrassostrea gigas

“…For this purpose, wild oysters aged between 12 and 18 months were sampled closed to farming areas. Oysters located in these areas are submitted to high pathogen pressure and have been shown to be resistant to POMS disease (Gawra et al 2023). To maximise the biodiversity of the bacterial collection, oysters were sampled from 4 geographical French sites at two different seasons.…”

Ancestors’ Gift: Parental Early Exposure to the Environmentally Realistic Pesticide Mixture Drives Offspring Phenotype in a Larger Extent Than Direct Exposure in the Pacific Oyster, Crassostrea gigas

“…However, the assessment of parental effects being the result of nongenetic inheritance of chemical-induced effects requires to detangle nongenetic from genetic effects, which is recognized as a highly tricky task . Indeed, epigenetic mechanisms could mediate nongenetic effects, and epigenetic divergence could be faster and predominant over genetic divergence in rapid adaptation of oysters . Besides, the data herein do not allow to quantify the relative prevalence of genetic and epigenetic effects.…”

“…61 Indeed, epigenetic mechanisms could mediate nongenetic effects, 62 and epigenetic divergence could be faster and predominant over genetic divergence in rapid adaptation of oysters. 63 Besides, the data herein do not allow to quantify the relative prevalence of genetic and epigenetic effects. In addition, the Pacific oyster has a highly variable genome, and laboratory experiments are likely to increase genetic drift 64 or selection, 65 which may explain the genetic divergence observed here between control and exposed lineages.…”

Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life

“…Moreover, this phenotype was associated with heritable changes in epigenetic signatures (DNA methylation patterns) that are reminiscent of mechanisms underlying innate immune memory response in mammals and plants [ 89 , 90 ]. Remarkably, epigenetic variations affecting immune pathways have been shown to confer rapid adaptation to pathogenic pressure in oyster [ 91 ]. The hypothesis beyond a microbiota-induced memory is a continuous reshaping of cellular signaling pathways and microbiota, which resulted in long-term heritable epigenetic imprinting ( figure 2 , left panel).…”