Parasite escape through trophic specialization in a species flock

Abstract

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

Divergent parasite infections in sympatric cichlid species in Lake Victoria

“…'nyererei-like'. This may be related to the habitat specialization of the former, being confined to crevices in both islands, which may provide a refuge from infections (see also Hablutzel et al (2017)). Alternatively, it could be related to the more insectivorous feeding habits, which could limit exposure to limnetic parasites compared to the more planktivorous P. nyererei and P. sp.…”

“…The first prerequisite of parasite-mediated divergent selection in natural populations is that infections differ between diverging host populations. Currently, there is a growing body of literature describing differentiated parasite infections in ecotypes or closely related species particularly in freshwater fishes (Knudsen et al, 1997(Knudsen et al, , 2003MacColl, 2009;Eizaguirre et al, 2011;Natsopoulou et al, 2012;Karvonen et al, 2013aKarvonen et al, ,b, 2015 including cichlid fishes (Blais et al, 2007;Maan et al, 2008;Raeymaekers et al, 2013;Hablutzel et al, 2016Hablutzel et al, , 2017. Overall, these studies suggest that conditions for parasite-mediated divergent selection between ecological niches are not uncommon.…”

An exploration of the links between parasites, trophic ecology, morphology, and immunogenetics in the Lake Tanganyika cichlid radiation

“…Overall, there are thus substantial indications that habitat and diet influence both the bacterial microbiota as well as parasitic macrobiota with the LT cichlid radiation. Previously, Hablützel et al (2017) demonstrated that trophic divergence can also lead to divergence in parasite communities at younger branches of the LT radiation. Within the Tropheini, one of the tribes included in this study, species evolved from relatively unselective substrate browsing of aufwuchs to more specialized foraging strategies, such as selective combing of microscopic diatoms or picking of macro-invertebrates.…”

“…Parasite-induced speciation requires divergent parasite communities, adaptation to these parasite communities, and evolution of reproductive isolation (Karvonen & Seehausen, 2012). Specialization in habitat use has been shown to significantly affect exposure to parasites (Johnson et al, 2009; Matthews et al, 2010; Karvonen et al, 2013, 2018), and shifts in trophic niche may lead to changes in parasite transmission (Knudsen et al, 2010; Hablützel et al, 2017; Karvonen et al, 2018). Following adaptive divergence in allopatry, exposure of migrants to novel parasite communities may lead to reduced fitness and promote the evolution of prezygotic barriers (Nosil et al, 2005; MacColl & Chapman, 2010).…”

“…We first evaluated macroevolutionary relationships between trophic morphology, trophic ecology, and parasitism within LT cichlids. We expected different macroparasite communities among species, possibly between algae and invertebrate feeders (i.e., species that shifted in diet), or between generalists and sand and rock dwelling species (i.e., species that shifted in habitat) (Hablützel et al, 2017; Hayward et al, 2017). Second, we tested whether the species evolved immunogenetic differences by screening several loci of teleost MHC class II B genes.…”