BackgroundAdaptation to different ecological environments is thought to drive ecological speciation. This phenomenon culminates in the radiations of cichlid fishes in the African Great Lakes. Multiple characteristic traits of cichlids, targeted by natural or sexual selection, are considered among the driving factors of these radiations. Parasites and pathogens have been suggested to initiate or accelerate speciation by triggering both natural and sexual selection. Three prerequisites for parasite-driven speciation can be inferred from ecological speciation theory. The first prerequisite is that different populations experience divergent infection levels. The second prerequisite is that these infection levels cause divergent selection and facilitate adaptive divergence. The third prerequisite is that parasite-driven adaptive divergence facilitates the evolution of reproductive isolation. Here we investigate the first and the second prerequisite in allopatric chromatically differentiated lineages of the rock-dwelling cichlid Tropheus spp. from southern Lake Tanganyika (Central Africa). Macroparasite communities were screened in eight populations belonging to five different colour morphs.ResultsParasite communities were mainly composed of acanthocephalans, nematodes, monogeneans, copepods, branchiurans, and digeneans. In two consecutive years (2011 and 2012), we observed significant variation across populations for infection with acanthocephalans, nematodes, monogeneans of the genera Gyrodactylus and Cichlidogyrus, and the copepod Ergasilus spp. Overall, parasite community composition differed significantly between populations of different colour morphs. Differences in parasite community composition were stable in time. The genetic structure of Tropheus populations was strong and showed a significant isolation-by-distance pattern, confirming that spatial isolation is limiting host dispersal. Correlations between parasite community composition and Tropheus genetic differentiation were not significant, suggesting that host dispersal does not influence parasite community diversification.ConclusionsSubject to alternating episodes of isolation and secondary contact because of lake level fluctuations, Tropheus colour morphs are believed to accumulate and maintain genetic differentiation through a combination of vicariance, philopatric behaviour and mate discrimination. Provided that the observed contrasts in parasitism facilitate adaptive divergence among populations in allopatry (which is the current situation), and promote the evolution of reproductive isolation during episodes of sympatry, parasites might facilitate speciation in this genus.

24In adaptive radiations species diversify rapidly to occupy an array of ecological niches. In these 25 different niches, species might be exposed to parasites through different routes and at different 26 levels. If this is the case, adaptive radiations should be accompanied by a turnover in parasite 27 communities. How the adaptive radiation of host species might be entangled with such a turnover of 28 parasite communities is poorly documented in nature. In the present study, we examined the 29 intestinal parasite faunas of eleven species belonging to the tribe Tropheini, one of several adaptive 30 radiations of cichlid fishes in Lake Tanganyika. The most parsimonious ancestral foraging strategy 31 among Tropheini is relatively unselective substrate ingestion by browsing of aufwuchs. Certain 32 lineages however evolved more specialized foraging strategies, such as selective combing of 33 microscopic diatoms or picking of macro-invertebrates. We found that representatives of such 34 specialized lineages bear reduced infection with intestinal acanthocephalan helminths. Possibly, the 35 evolution of selective foraging strategies entailed reduced ingestion of intermediate invertebrate 36hosts of these food-web transmitted parasites. In Tropheini, trophic specialization is therefore 37 intertwined with divergence in parasite infection. We conclude that the study of parasite 38 communities could improve our understanding of host evolution, ecological speciation and the origin 39 of adaptive radiations. 40 41

24In adaptive radiations species diversify rapidly to occupy an array of ecological niches. In these 25 different niches, species might be exposed to parasites through different routes and at different 26 levels. If this is the case, adaptive radiations should be accompanied by a turnover in parasite 27 communities. How the adaptive radiation of host species might be entangled with such a turnover of 28 parasite communities is poorly documented in nature. In the present study, we examined the 29 intestinal parasite faunas of eleven species belonging to the tribe Tropheini, one of several adaptive 30 radiations of cichlid fishes in Lake Tanganyika. The most parsimonious ancestral foraging strategy 31 among Tropheini is relatively unselective substrate ingestion by browsing of aufwuchs. Certain 32 lineages however evolved more specialized foraging strategies, such as selective combing of 33 microscopic diatoms or picking of macro-invertebrates. We found that representatives of such 34 specialized lineages bear reduced infection with intestinal acanthocephalan helminths. Possibly, the 35 evolution of selective foraging strategies entailed reduced ingestion of intermediate invertebrate 36hosts of these food-web transmitted parasites. In Tropheini, trophic specialization is therefore 37 intertwined with divergence in parasite infection. We conclude that the study of parasite 38 communities could improve our understanding of host evolution, ecological speciation and the origin 39 of adaptive radiations. 40 41

Differences in habitat and diet between species are often associated with morphological differences. Habitat and trophic adaptation have therefore been proposed as important drivers of speciation and adaptive radiation. Importantly, habitat and diet shifts likely impose changes in exposure to different parasites and infection risk. As strong selective agents influencing survival and mate choice, parasites might play an important role in host diversification. We explore this possibility for the adaptive radiation of Lake Tanganyika (LT) cichlids. We first compare metazoan macroparasites infection levels between cichlid tribes. We then describe the cichlids’ genetic diversity at the major histocompatibility complex (MHC), which plays a key role in vertebrate immunity. Finally, we evaluate to what extent trophic ecology and morphology explain variation in infection levels and MHC, accounting for phylogenetic relationships. We show that different cichlid tribes in LT feature partially non-overlapping parasite communities and partially non-overlapping MHC diversity. While morphology explained 15% of the variation in mean parasite abundance, trophic ecology accounted for 16% and 22% of the MHC variation at the nucleotide and at the amino acid level, respectively. Parasitism and immunogenetic adaptation may thus add additional dimensions to the LT cichlid radiation. Electronic supplementary material The online version of this article (10.1007/s10750-018-3798-2) contains supplementary material, which is available to authorized users.

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