Population epigenetic divergence exceeds genetic divergence in the Eastern oyster <i>Crassostrea virginica</i> in the Northern Gulf of Mexico

Johnson, Kevin M.; Kelly, Morgan W.

doi:10.1111/eva.12912

Cited by 44 publications

(66 citation statements)

References 67 publications

(114 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Although DML were found across various genome features, they were mostly in exons and introns. This is consistent with a recent study of C. virginica gill tissue found differentially methylated regions in response to a salinity gradient were primarily in genic regions (Johnson and Kelly, 2019). Interestingly, DML were not found consistently in one particular region of a gene.…”

Section: Discussionsupporting

confidence: 92%

“…The association between DNA methylation and phenotypic differences in these corals demonstrates that epigenetic regulation of genes is potentially important for acclimatization and adaptation to environmental perturbation. Recent examination of C. virginica methylation patterns in response to a natural salinity gradient suggests that differential methylation may modulate environmental response in this species (Johnson and Kelly, 2019).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

General DNA Methylation Patterns and Environmentally-Induced Differential Methylation in the Eastern Oyster (Crassostrea virginica)

et al. 2020

View full text Add to dashboard Cite

Epigenetic modification, specifically DNA methylation, is one possible mechanism for intergenerational plasticity. Before inheritance of methylation patterns can be characterized, we need a better understanding of how environmental change modifies the parental epigenome. To examine the influence of experimental ocean acidification on eastern oyster (Crassostrea virginica) gonad tissue, oysters were cultured in the laboratory under control (491 ± 49 µatm) or high (2550 ± 211 µatm) pCO 2 conditions for 4 weeks. DNA from reproductive tissue was isolated from five oysters per treatment, then subjected to bisulfite treatment and DNA sequencing. Irrespective of treatment, DNA methylation was primarily found in gene bodies with approximately 22% of CpGs (2.7% of total cytosines) in the C. virginica genome predicted to be methylated. In response to elevated pCO 2 , we found 598 differentially methylated loci primarily overlapping with gene bodies. A majority of differentially methylated loci were in exons (61.5%) with less intron overlap (31.9%). While there was no evidence of a significant tendency for the genes with differentially methylated loci to be associated with distinct biological processes, the concentration of these loci in gene bodies, including genes involved in protein ubiquitination and biomineralization, suggests DNA methylation may be important for transcriptional control in response to ocean acidification. Changes in gonad methylation also indicate potential for these methylation patterns to be inherited by offspring. Understanding how experimental ocean acidification conditions modify the oyster epigenome, and if these modifications are inherited, allows for a better understanding of how ecosystems will respond to environmental change.

show abstract

Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

General DNA Methylation Patterns and Environmentally-Induced Differential Methylation in the Eastern Oyster (Crassostrea virginica)

et al. 2020

View full text Add to dashboard Cite

show abstract

“…In the eastern oyster (C. virginica) DNA methylation is more divergent between populations than single nucleotide polymorphism-based estimates of divergence, suggesting a nongenetic (i.e., environmental) influence on DNA methylation (Johnson and Kelly, 2020). Together, these studies provide some evidence of an association between DNA methylation and transcriptomic expression levels; however, the functional consequences of changes in DNA methylation are still largely unknown in bivalves.…”

Section: Introductionmentioning

confidence: 87%

“…Presence of high molecular weight DNA was confirmed using a 1.5% agarose gel, and DNA concentration was verified using a Qubit 3.0 Fluorometric dsDNA BR assay kit (Q32850; Life Technologies). The epiGBS library preparation followed previously published methods (Van Gurp et al, 2016;Johnson and Kelly, 2020). Briefly, a total of 500 ng of purified genomic DNA was double digested using the two frequent cutter enzymes AseI and NsiI (NEB-R0127L and NEB-R0526L; Van Gurp 2016).…”

Section: Dna Methylation Analysismentioning

confidence: 99%

“…The bismark commands used in the mapping allowed for 1 mismatch in a seed alignment of 10 with a minimum alignment score setting of −0.6 (-score_min L, 0, −0.6). These settings having previously been used in this species and were selected to account for genomic variations between C. virginica collected from the northern Gulf of Mexico (nGOM, this study) and the disease-resistant inbred line from the United States East Coast used for the construction of the reference genome (Gómez-Chiarri et al, 2015;Johnson and Kelly, 2020). CpG methylation was extracted from the non-deduplicated mapped reads using the bismark command bismark_methylation_extractor with the following commands; -ignore_r2 2, -bedGraph, -zero_based, -no_overlap, -cytosine_report, and -report.…”

Section: Dna Methylation Analysismentioning

confidence: 99%

See 1 more Smart Citation

Characterizing the Epigenetic and Transcriptomic Responses to Perkinsus marinus Infection in the Eastern Oyster Crassostrea virginica

et al. 2020

Self Cite

View full text Add to dashboard Cite

Eastern oysters in the northern Gulf of Mexico are routinely infected with the protistan parasite Perkinsus marinus, the cause of the disease commonly known as dermo. Recent experimental challenges among Atlantic coast populations have identified both resistant and susceptible genotypes using comparative transcriptomics. While controlled experimental challenges are essential first assessments, expanding this analysis to field reared individuals provides an opportunity to identify key genomic signatures of infection that appear both in the laboratory and in the field. In this study we combined reduced representation bisulfite sequencing with 3 RNA sequencing (Tag-seq) to describe two molecular phenotypes associated with infection in oysters outplanted at a common garden field site. These combined approaches allowed us to examine changes in DNA methylation and gene expression for a large number of individuals (n = 40) that developed infections during the course of a common garden outplant experiment. Our epigenetic analysis of DNA methylation identified significant changes in gene body methylation associated with increasing infection intensity, across genes associated with immune responses. There was a smaller transcriptomic response to increasing infection intensities with 32 genes showing differential expression; however, only 40% of these genes were found to also be differentially methylated. While there was no clear pattern between direction of differential methylation and gene expression, there was a significant effect of percent methylation on gene-by-gene expression levels and the coefficient of variation in gene body methylation between treatments. These results show that in C. virginica, heavily methylated genes have high levels of gene expression with low levels of variation. Comparing our differential expression results with previously published experimental P. marinus challenges identified overlapping expression patterns for genes associated with C1q-domain-containing and V-type proton ATPase proteins. Through our comparative transcriptomic approach using field reared individuals and co-expression network analysis we have also been able to identify a network of genes

show abstract

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

Chen

et al. 2022

Ecological Applications

View full text Add to dashboard Cite

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.

show abstract

Population epigenetic divergence exceeds genetic divergence in the Eastern oyster Crassostrea virginica in the Northern Gulf of Mexico

Cited by 44 publications

References 67 publications

General DNA Methylation Patterns and Environmentally-Induced Differential Methylation in the Eastern Oyster (Crassostrea virginica)

General DNA Methylation Patterns and Environmentally-Induced Differential Methylation in the Eastern Oyster (Crassostrea virginica)

Characterizing the Epigenetic and Transcriptomic Responses to Perkinsus marinus Infection in the Eastern Oyster Crassostrea virginica

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

Contact Info

Product

Resources

About