Unraveling molecular mechanisms of adaptation to complex environments is crucial to understanding tolerance of abiotic pressures and responses to climatic change. Epigenetic variation is increasingly recognized as a mechanism that can facilitate rapid responses to changing environmental cues. To investigate variation in genetic and epigenetic diversity at spatial and thermal extremes, we use whole genome and methylome sequencing to generate a high-resolution map of DNA methylation in the bumble bee
Epigenetic modifications are thought to be one of the molecular mechanisms involved in plastic adaptive responses to environmental variation. However, studies reporting associations between genome-wide epigenetic changes and habitat-specific variations in life history traits (e.g., lifespan, reproduction) are still scarce, likely due to the recent application of methylome resequencing methods to non-model species. In this study, we examined associations between whole genome DNA methylation and environmentally driven life history variation in 2 lineages of a marine fish, the capelin (Mallotus villosus), from North America and Europe. In both lineages, capelin harbor 2 contrasting life history tactics (demersal vs. beach-spawning). Performing whole genome and methylome sequencing, we showed that life history tactics are associated with epigenetic changes in both lineages, though the effect was stronger in European capelin. Genetic differentiation between the capelin harboring different life history tactics was negligible, but we found genome-wide methylation changes in both lineages. We identified 9,125 European and 199 North American differentially methylated regions (DMRs) due to life history. Gene ontology (GO) enrichment analysis for both lineages revealed an excess of terms related to neural function. Our results suggest that environmental variation causes important epigenetic changes that are associated with contrasting life history tactics in lineages with divergent genetic backgrounds, with variable importance of genetic variation in driving epigenetic variation. Our study emphasizes the potential role of genome-wide epigenetic variation in adaptation to environmental variation.
more » « less- NSF-PAR ID:
- 10390432
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Evolution
- ISSN:
- 0014-3820
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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INTRODUCTION Transposable elements (TEs), repeat expansions, and repeat-mediated structural rearrangements play key roles in chromosome structure and species evolution, contribute to human genetic variation, and substantially influence human health through copy number variants, structural variants, insertions, deletions, and alterations to gene transcription and splicing. Despite their formative role in genome stability, repetitive regions have been relegated to gaps and collapsed regions in human genome reference GRCh38 owing to the technological limitations during its development. The lack of linear sequence in these regions, particularly in centromeres, resulted in the inability to fully explore the repeat content of the human genome in the context of both local and regional chromosomal environments. RATIONALE Long-read sequencing supported the complete, telomere-to-telomere (T2T) assembly of the pseudo-haploid human cell line CHM13. This resource affords a genome-scale assessment of all human repetitive sequences, including TEs and previously unknown repeats and satellites, both within and outside of gaps and collapsed regions. Additionally, a complete genome enables the opportunity to explore the epigenetic and transcriptional profiles of these elements that are fundamental to our understanding of chromosome structure, function, and evolution. Comparative analyses reveal modes of repeat divergence, evolution, and expansion or contraction with locus-level resolution. RESULTS We implemented a comprehensive repeat annotation workflow using previously known human repeats and de novo repeat modeling followed by manual curation, including assessing overlaps with gene annotations, segmental duplications, tandem repeats, and annotated repeats. Using this method, we developed an updated catalog of human repetitive sequences and refined previous repeat annotations. 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Abstract Recent studies show that epigenetic variation in the form of
DNA methylation may serve as a substrate for selection. Theory suggests that heritable epigenetic marks that increase fitness should increase in frequency in a population, and these changes may result in novel morphology, behaviour, or physiology, and ultimately reproductive isolation. Therefore, epigenetic variation might provide the first substrate for selection during the course of evolutionary divergence. This hypothesis predicts that populations in the earliest stages of divergence will differentiate in their methylome prior to any genetic differentiation. While several studies have investigated natural epigenetic variation, empirical studies that test predictions about its role in speciation are surprisingly scarce. Here, we investigateDNA methylation variation using an isoschizomeric digest method, Methyl‐Sensitive Amplified Polymorphism, across multiple stages of evolutionary divergence in natural populations of North American stream fishes. We show that epigenetic differentiation between methylomes is greater than genetic divergence among closely related populations across two river drainages. Additionally, we demonstrate that epigenetic divergence is a stronger predictor of the strength of behavioural reproductive isolation and suggest that changes in the methylome could influence the evolution of reproductive isolation between species. Our findings suggest a role for epigenetics not only in the initiation of divergence, but also in the maintenance of species boundaries over greater evolutionary timescales.
