Divergent parasite infections in sympatric cichlid species in Lake Victoria

Abstract

Parasitism has been proposed as a factor in host speciation, as an agent affecting coexistence of host species in species-rich communities and as a driver of post-speciation diversification. Young adaptive radiations of closely related host species of varying ecological and genomic differentiation provide interesting opportunities to explore interactions between patterns of parasitism, divergence and coexistence of sympatric host species. Here, we explored patterns in ectoparasitism in a community of 16 fully sympatric cichlid species at Makobe Island in Lake Victoria, a model system of vertebrate adaptive radiation. We asked whether host niche, host abundance or host genetic differentiation explains variation in infection patterns. We found significant differences in infections, the magnitude of which was weakly correlated with the extent of genomic divergence between the host species, but more strongly with the main ecological gradient, water depth. These effects were most evident with infections of Cichlidogyrus monogeneans, whereas the only host species with a strictly crevice-dwelling niche, Pundamilia pundamilia, deviated from the general negative relationship between depth and parasitism. In accordance with the Janzen-Connell hypothesis, we also found that host abundance tended to be positively associated with infections in some parasite taxa. Data on the Pundamilia sister species pairs from three other islands with variable degrees of habitat (crevice) specialization suggested that the lower parasite abundance of P. pundamilia at Makobe could result from both habitat specialization and the evolution of specific resistance. Our results support influences of host genetic differentiation and host ecology in determining infections in this diverse community of sympatric cichlid species.

Patterns of ectoparasite infection in wild-caught and laboratory-bred cichlid fish, and their hybrids, implicate extrinsic rather than intrinsic causes of species differences in infection

“…In our previous studies, we found that populations of Pundamilia with intermediate differentiation, inhabiting Kissenda and Python Islands, showed some infection divergence (Gobbin et al in prep.). In the wild, P. nye are more frequently infected, and in higher numbers, with L. monodi and E. lamellifer than P. pun (Maan et al, 2008;Karvonen et al, 2018;Gobbin et al, 2020). Here, we report that these differences were absent in fish raised in the laboratory, where the expression of species-specific depth and diet Fig.…”

“…In nature, these two species are sympatric but differ in their average depth distribution and diet. Previous studies in this species pair, as well as in closely related populations inhabiting other locations in Lake Victoria, revealed that they differ in parasite infection (Maan et al, 2008;Karvonen et al, 2018;Gobbin et al in prep.). They mate assortatively, mediated by species-specific female preferences for male coloration (blue vs. red; Seehausen & van Alphen, 1998.…”

“…Among islands, sympatric pairs vary in the level of reproductive isolation and in the extent of differentiation in ecological traits, such as water depth and diet (Seehausen, 1996;Seehausen et al, 2008;Meier et al, 2017b;van Rijssel et al, 2018;Wright et al, 2019). At Makobe Island, where these two sympatric species are strongly differentiated, they differ in their parasite abundances, in a way that is consistent with species differences in diet and microhabitat: P. pun harbour more intestinal nematodes and P. nye more gill copepods (Maan et al, 2008;Karvonen et al, 2018;Gobbin et al in prep.). Less pronounced differences in parasite infection were found in populations inhabiting Kissenda and Python Islands (Gobbin et al in prep.…”

“…A large number of species has rapidly diverged through niche partitioning (Turner, 2007) resulting in a large diversity of macro-habitat, micro-habitat and trophic specializations (Sturmbauer & Meyer, 1992;Bouton et al, 1997;Genner et al, 1999). In several African cichlid lineages, species differences in ecology are associated with differences in the community composition of the parasites infecting them (Hablützel et al, 2017;Hayward et al, 2017;Karvonen et al, 2018), suggesting that variation in exposure contributes to variation in infection. Variation in immune response may have evolved as well: among closely related and sympatric cichlid species of Lake Malawi, differentiation in parasite community composition is correlated with differentiation at the MHC locus (Major Histocompatibility Complex, coding for proteins that recognize pathogens) (Blais et al, 2007).…”

Diversity in rest-activity patterns among Lake Malawi cichlid fishes suggests novel axis of habitat partitioning

“…In Lake Malawi alone, there are over 500 species of cichlids, inhabiting a diversity of environmental and feeding niches. Cichlid species exhibit a high degree of habitat fidelity and partition their environment along discrete ecological axes, including distinct biotic (food availability, predation, and parasites) and abiotic (light, water chemistry) environments that play a critical role in the origins and maintenance of cichlid biodiversity [12][13][14][15][16][17]. Predation on Malawi cichlids is considered to be relatively low, which is thought to have contributed to their evolutionary and ecological success [18].…”