Epigenetic divergence as a potential first step in darter speciation

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 investigate DNA 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.

Genome‐scale sampling suggests cryptic epigenetic structuring and insular divergence in Canada lynx

“…Importantly, our demographic inferences suggesting a relatively recent (20–33 KYA) evolutionary establishment of Newfoundland Canada lynx supports DNA methylation as a marker to examine rapid evolutionary change. Evolutionary theory in model organisms has predicted that epimutations and methylome evolution often precede genomic changes (Smith, Martin, Nguyen, & Mendelson, ; Vidalis et al, ), which has been further substantiated with empirical evidence examining epigenetic changes over structural genomic variants in the absence of (Ichikawa et al, ) and phenotypic responses in the absence of standing genetic variation (Sentis et al, ).…”

Molecular Mechanisms behind the Physiological Resistance to Intense Transient Warming in an Iconic Marine Plant

“…Accordingly, only these shallow plants showed the activation of heat shock factors, which are transcriptional activators of heat shock genes (Kotak et al, 2007; von Koskull-Doring et al, 2007) and that mutually progress with epigenetic processes in regulating the abiotic stress responses in plants. These epigenetic modifications can be involved in the evolution of adaptive strategies and speciation (Flatscher et al, 2012; Smith et al, 2016) and potentially also in the genetic disjunction existing between shallow and deep meadow stands in P. oceanica (Migliaccio et al, 2005). Epigenetic modifications could also be at the basis of the survival of millenary clones of the species in the face of the environmental changes they have experienced along their evolutionary history (Arnaud-Haond et al, 2012).…”

The sources of adaptive variation

“…Recent claims for such effects have been based on evidence that changes affecting the methylome are more numerous than some types of sequence variants in evolving lineages of Darwin's finches [88] and darter fish [89]. Such comparisons, however, provide no evidence that the epigenetic variants in question had any role in phenotypic evolution.…”