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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.

Rapid ecological speciation along depth gradients has taken place repeatedly in freshwater fishes, yet molecular mechanisms facilitating such diversification are typically unclear. In Lake Masoko, an African crater lake, the cichlid Astatotilapia calliptera has diverged into shallow littoral and deep benthic ecomorphs with strikingly different jaw structures within the last 1,000 years. Using genome-wide transcriptome data, we explore two major regulatory transcriptional mechanisms, expression and splicing QTL variants, and examine their contributions to differential gene expression underpinning functional phenotypes. We identified 7,550 genes with significant differential expression between ecomorphs, of which 5.4% were regulated by cis-regulatory expression QTLs, and 9.2% were regulated by cis-regulatory splicing QTLs. We also found strong signals of divergent selection on differentially expressed genes associated with craniofacial development. These results suggest that large-scale transcriptome modification plays an important role during early-stage speciation. We conclude that regulatory-variants are important targets of selection driving ecologically-relevant divergence in gene expression during adaptive diversification.

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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.

Engraulicypris sardella is an endemic and economically important cyprinid species in Lake Nyasa/Malawi which has recently been infected by the tapeworm Ligula intestinalis. This parasite is known to induce severe pathological and behavioural effects on other cyprinids, including castration, followed by a collapse of infected populations. As a first step to understanding the dynamics between this parasite and E. sardella, we studied the spatial and temporal variation in prevalence over a period of 1 year. Overall prevalence was about 15%, but we observed a consistently higher prevalence in the littoral compared to the pelagic zone. Fish in the upper water levels showed the highest prevalence, with a marked decline with increasing water depth down to 150 m. The proportion of infected fish varied over time, with a significantly higher prevalence in the rainy season. In a huge lake like the Nyasa, with a surface area of 29,000 km2 and a maximum depth of 785 m, the transmission success of the parasite appears to show large variations in time and space. We suggest that these conditions could lead the parasite to become persistent within the lake, rather than the typical epidemic situation as observed in smaller bodies of water.

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Life history theory assumes that there are trade-offs between different traits in organisms, such as growth, reproduction, and survival (Roff, 2002). These traits cannot be simultaneously maximized within the same individual because the available amount of nutrients and other resources are in limited supply (Stearns, 1989). Increased resource allocation into one trait will, therefore, come at the cost of reduced allocation into other traits (Agnew et al., 2000). In each given environment, the optimal way to resolve these trade-offs (i.e., the optimal strategy for maximizing fitness) is the one achieving the highest possible reproductive success (