Epigenetic divergence during early stages of speciation in an African crater lake cichlid fish

Abstract

Epigenetic variation can alter transcription and promote phenotypic divergence between populations facing different environmental challenges. Here, we assess the epigenetic basis of diversification during the early stages of speciation. Specifically, we focus on the extent and functional relevance of DNA methylome divergence in the very young radiation of Astatotilapia calliptera in crater Lake Masoko, southern Tanzania. Our study focuses on two lake ecomorphs that diverged approximately 1,000 years ago and a population in the nearby river from which they separated approximately 10,000 years ago. The two lake ecomorphs show no fixed genetic differentiation, yet are characterized by different morphologies, depth preferences and diets. We report extensive genome-wide methylome divergence between the two lake ecomorphs, and between the lake and river populations, linked to key biological processes and associated with altered transcriptional activity of ecologically relevant genes. Such genes differing between lake ecomorphs include those involved in steroid metabolism, hemoglobin composition and erythropoiesis, consistent with their divergent habitat occupancy. Using a common-garden experiment, we found that global methylation profiles are often rapidly remodeled across generations but ecomorph-specific differences can be inherited. Collectively, our study suggests an epigenetic contribution to the early stages of vertebrate speciation.

Ecological Speciation Promoted by Divergent Regulation of Functional Genes Within African Cichlid Fishes

“…GO terms enriched in benthic ecomorphs are related to blood cell development, vascular morphogenesis and metabolic oxidation-reduction processes. This may indicate local adaptation to increased habitat depth ( Jacobs and Elmer 2021 ; Vernaz et al 2022 ) and, more specifically, to the relatively low oxygen conditions of the deep-water benthic environment in Lake Masoko, compared with shallow-water habitat ( fig. 1 B and supplementary table S5, Supplementary Material online).…”

“…There are many alternative molecular mechanisms through which rapid transcriptional and phenotypic diversity can be generated that were not explored here. Specifically, microRNAs, transposable elements, and epigenetic markers are recently shown to facilitate adaptive phenotypic shifts in cichlids ( Xiong et al 2019 ; Carleton et al 2020 ; Vernaz et al 2022 ).…”

Epigenetics and island‐mainland divergence in an insectivorous small mammal

“…Epigenetic modifications may take a variety of forms, these include DNA methylation (DNAm), histone modifications and noncoding RNA activity, all of which can regulate gene expression without requiring changes in the DNA sequence (Moore et al, 2013). Differential patterns of epigenetic modification have been associated with early stages of speciation (Vernaz et al, 2021(Vernaz et al, , 2022Vogt, 2017) DNAm involves the transfer of a methyl group to a cytosine base (Moore et al, 2013) and can occur throughout the genome but mostly occurs on CpG dinucleotide sites (Moore et al, 2013).…”

Epigenetic and genetic differentiation betweenCoregonusspecies pairs

“…Previous studies have shown that methylation is affected by temperature (Ryu et al 2018;Venney et al 2022;Metzger & Schulte 2017;McCaw et al 2020;Anastasiadi et al 2017), salinity (Heckwolf et al 2020;Artemov et al 2017), rearing environment (Leitwein et al 2021;Le Luyer et al 2017;Wellband et al 2021;Gavery et al 2018), and other factors in various systems. Differences in habitat use can influence DNA methylation, as observed between capelin (Mallotus villosus) utilizing beach-and demersal-spawning life history tactics (Venney et al 2023), among sympatric Arctic charr morphs occupying different habitats and dietary niches (Matlosz et al 2022), between phenotypically divergent cichlid species (Vernaz et al 2022), and in freshwater snails (Potamopyrgus antipodarum) which exhibit differences in shell shape associated with water current speed (Thorson et al 2017).…”