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Parasite-driven and immunogenetic diversification in Lake Tanganyika cichlid fishes

Final Report Summary - CICHLIDWORMS (Parasite-driven and immunogenetic diversification in Lake Tanganyika cichlid fishes)

In this project, we were interested in the mechanisms underlying adaptation to distinct environments and, consequently, how new species might form, in an enigmatic model system in evolutionary biology, the East African cichlid fishes. In particular, we were interested in the question how the exposure to different parasite communities in different habitats might contribute to speciation, e.g. via immunity-based mate choice. We also intended to test the hypothesis that cichlid diversification could be ‘parasite-driven’ and that the combined effect of natural and sexual selection on a trait (in this case the immune system) has the potential to accelerate speciation. We primarily focused on one group of cichlid fishes from Lake Tanganyika, the Tropheini, but extended our genomic analysis to the entire cichlid species-flock from this lake. Our strategy was to explore these questions at two levels: (i) the micro-evolutionary scale by comparing populations of the same species (primarily Tropheus moorii) in allopatry and across different sampling periods; and (ii) the macro-evolutionary scale by comparing different members of an entire cichlid lineage, the Tropheini, and by studying the diversity of immune-related genes across the entire species flock. To this end, we combined field studies and laboratory experiments. The field studies aimed at characterizing the parasite communities of cichlid fishes in East African Lake Tanganyika in detail, both at the intra- and inter-species level, and across different sampling years. The laboratory experiments aimed at characterizing molecular differences in immune gene composition (primarily the genes of the major histocompatibility complex (MHC) class IIB) using classical and next-generation sequencing technologies. At the micro-evolutionary scale, we found by screening through different populations of a single cichlid species (Tropheus moorii) that there is seasonal variation with respect to infections with acanthocephalans, nematodes, monogeneans and copepods, and that parasite communities differ between allopatric and genetically isolated Tropheus populations. This suggests that local differences in parasites might indeed facilitate speciation. We then showed that MHC allelic diversity correlates with body condition as measured by the amount of perivisceral fat reserves in T. moorii, while there was no correlation between parasite infection and number of MHC length variants or perivisceral fat deposits. This suggests that male individuals with an intermediate number of alleles might be able to use their fat reserves more efficiently. A comparison across two species suggests that there is a link between host dispersal and parasite diversity in two sympatric cichlids of Lake Tanganyika. The analysis of full-length coding sequences of the MCH class IIB genes in cichlids revealed a common origin of the b family of this gene. In addition, we found that the more diversified lineages of cichlid MHC class IIB b genes show higher levels of recombination and selection. By integrating across field survey data and MHC class II diversity across a phylogenetic representative set of cichlids from Lake Tanganyika, we further show that the different cichlid tribes feature partially non-overlapping parasite communities as well as partially non-overlapping MHC diversities. The trophic-morphological axis of diversification in Lake Tanganyika cichlids appears to be strongly correlated with infection levels of metazoan macro-parasites, suggesting that parasitism and immunogenetic contribute to trigger adaptive radiation. In summary, we provide evidence that the adaptation to divergent parasite communities might indeed facilitate diversification in the adaptive radiations of cichlid fishes in East Africa. This aspect of cichlid evolution has been largely overlooked so far, so that our results provide important baseline data for future research in this important model system and role-model in evolutionary biology.