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. We focus on the extent and functional relevance of DNA methylome divergence between two Astatotilapia calliptera ecomorphs in crater Lake Masoko, southern Tanzania. We report extensive genome-wide methylome divergence between populations linked to key biological processes, including transcriptional activity of ecologically-relevant genes. These include genes involved in steroid metabolism, haemoglobin composition and erythropoiesis, consistent with divergent habitat occupancy of the ecomorphs. Using a common garden experiment, we found that global methylation profiles are rapidly remodelled across generations, but ecomorph-specific differences can be inherited. Collectively, our study suggests an epigenetic contribution to early stages of vertebrate speciation.

Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

“…Trait inheritance and phenotypic diversification are primarily explained by the transmission of genetic information encoded in the DNA sequence. In addition, a variety of epigenetic processes have recently been reported to mediate heritable transmission of phenotypes in animals and plants [1][2][3][4][5][6][7] . However, current understanding of the evolutionary significance of epigenetic processes, and of their roles in organismal diversification, is in its infancy.…”

“…In total, the radiation comprises over 800 endemic species 34 , that are estimated to have evolved from common ancestry approximately 800,000 years ago 35 . Species within the radiation can be grouped into seven distinct ecomorphological groups based on their ecology, morphology and genetic differences: (1) shallow benthic, (2) deep benthic, (3) deep pelagic zooplanktivorous/piscivorous Diplotaxodon, (4) the rock-dwelling 'mbuna', (5) zooplanktivorous 'utaka', (6) Astatotilapia calliptera specialised for shallow weedy habitats (also found in surrounding rivers and lakes), and (7) the midwater pelagic piscivores Rhamphochromis 36,37 .…”

Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

“…T rait inheritance and phenotypic diversification are primarily explained by the transmission of genetic information encoded in the DNA sequence. In addition, a variety of epigenetic processes have recently been reported to mediate heritable transmission of phenotypes in animals and plants [1][2][3][4][5][6][7] . However, the current understanding of the evolutionary significance of epigenetic processes, and of their roles in organismal diversification, is in its infancy.…”

“…In total, the radiation comprises over 800 endemic species 34 , that are estimated to have evolved from common ancestry approximately 800,000 years ago 35 . Species within the radiation can be grouped into seven distinct ecomorphological groups based on their ecology, morphology, and genetic differences: (1) shallow benthic, (2) deep benthic, (3) deep pelagic zooplanktivorous/piscivorous Diplotaxodon, (4) the rockdwelling ‛mbuna', (5) zooplanktivorous ‛utaka', (6) Astatotilapia calliptera specialised for shallow weedy habitats (also found in surrounding rivers and lakes), and (7) the midwater pelagic piscivores Rhamphochromis 36,37 . Recent large-scale genetic studies have revealed that the Lake Malawi cichlid flock is characterised by an overall very low genetic divergence among species (0.1−0.25%), combined with a low mutation rate, a high rate of hybridisation and extensive incomplete lineage sorting (shared retention of ancestral genetic variation across species) 34,36,38,39 .…”

Epigenetics and island-mainland divergence in an insectivorous small mammal

“…Epigenetic changes can be heritable and have been associated with early stages of speciation (Quadrana & Colot, 2016;Vernaz, Hudson, et al, 2021;Vogt, 2017). Epigenetic modifications can regulate gene expression through chemical or structural modifications without directly changing the DNA sequence (Razin & Riggs, 1980).…”