Examining the role of parasites in limiting unidirectional gene flow between lake and river sticklebacks.

Parasites are important selective agents with the potential to limit gene flow between host populations by shaping local host immunocompetence. We report on a contact zone between lake and river three-spined sticklebacks (Gasterosteus aculeatus) that offers the ideal biogeographic setting to explore the role of parasite-mediated selection on reproductive isolation. A waterfall acts as a natural barrier and enforces unidirectional migration from the upstream river stickleback population to the downstream river and lake populations. We assessed population genetic structure and parasite communities over four years. In a set of controlled experimental infections, we compared parasite susceptibility of upstream and downstream fish by exposing laboratory-bred upstream river and lake fish, as well as hybrids, to two common lake parasite species: a generalist trematode parasite, Diplostomum pseudospathaceum, and a host-specific cestode, Schistocephalus solidus. We found consistent genetic differentiation between upstream and downstream populations across four sampling years, even though the downstream river consisted of ~10% first-generation migrants from the upstream population as detected by parentage analysis. Fish in the upstream population had lower genetic diversity and were strikingly devoid of macroparasites. Through experimental infections, we demonstrated that upstream fish and their hybrids had higher susceptibility to parasite infections than downstream fish. Despite this, naturally sampled upstream migrants were less infected than downstream residents. Thus, migrants coming from a parasite-free environment may enjoy an initial fitness advantage, but their descendants seem likely to suffer from higher parasite loads. Our results suggest that adaptation to distinct parasite communities can influence stickleback invasion success and may represent a barrier to gene flow, even between close and connected populations.

Virulence in the three-spined stickleback specific parasite Schistocephalus solidus is inherited additively.

Parasite virulence is a key trait in host-parasite interactions and plays a crucial role in infection dynamics. Our study system offers the rare opportunity to study the virulence of an individual macroparasite (Schistocephalus solidus) in its vertebrate fish host (Gasterosteus aculeatus). The size of the tapeworm in the fish can be regarded as a good proxy for individual parasite virulence, as parasite size correlates negatively with fitness traits of the stickleback host (i.e. the bigger the parasite, the lower the host's reproductive success) as well as directly with the number of parasite offspring to be expected. To investigate how virulence is inherited, laboratory bred, parasite-naïve stickleback were infected with a cross of two S. solidus populations of either high or low virulence, as well as one hybrid cross between the two. The relative weight of the parasite as expressed in the parasite index served as a measure of virulence. Furthermore, we measured several condition and immune related traits in the fish host to assess parasite impact on the stickleback. We hypothesized that parasite virulence is to a large extent genetically determined and correlated with several fitness traits in the stickleback host. We found that virulence is inherited additively in S. solidus, with hybrids of high and low virulence parasites displaying intermediate levels. However, contrary to expectation, infection rate of S. solidus in three-spined stickleback is not related to virulence. Even though the presence of the parasite caused differences in host condition, these were indistinguishable between the different levels of virulence in this experiment. Fish immune traits also showed a response to infection but had no correlation with level of parasite virulence. With this experiment we have taken the first step towards understanding how virulence is inherited and how it is driven in the Schistocephalus-stickleback system, even though virulence, as measured here, does not directly translate into cost for the host. A better understanding of the costs inflicted on the host by S. solidus infection is needed to understand this interaction in greater detail.

The role of prezygotic isolation mechanisms in the divergence of two parasite species.

BACKGROUND: The formation of reproductive barriers in diverging lineages is a prerequisite to complete speciation according to the biological species concept. In parasites with complex life cycles, speciation may be driven by adaptation to different intermediate hosts, yet diverging lineages can still share the same definitive host where reproduction takes place. In these cases, prezygotic isolation mechanisms should evolve very early and be particularly strong, preventing costly unfavourable matings. In this study, we investigated the importance of prezygotic barriers to reproduction in two cestode species that diverged 20-25mya and show an extraordinary degree of specificity to different intermediate hosts. Both species share the same definitive hosts and hybridize in the laboratory. Yet, natural hybrids have so far not been detected. METHODS: We used a combination of different experiments to investigate the role of prezygotic barriers to reproduction in the speciation of these parasites. First, we investigated whether hybridization is possible under natural conditions by exposing lab-reared herring gulls (Larus argentatus, the definitive hosts) to both parasites of either sympatric or allopatric combinations. In a second experiment, we tested whether the parasites prefer conspecifics over parasites from a different species in dichotomous mate choice trials. RESULTS: Our results show that the two species hybridize under natural conditions with parasites originating either from sympatric or allopatric populations producing hybrid offspring. Surprisingly, the mate choice experiment indicated that both parasite species prefer mates of the different species to conspecifics. CONCLUSIONS: Neither fundamental constraints against hybridization in a natural host nor assortative mate choice sufficiently explain the persistent segregation of the two tapeworm species in nature. Hence, postzygotic ecological selection against hybrids is presumably the more important driving force limiting gene flow between the two parasite sister species.

Hybridization between two cestode species and its consequences for intermediate host range.

BACKGROUND: Many parasites show an extraordinary degree of host specificity, even though a narrow range of host species reduces the likelihood of successful transmission. In this study, we evaluate the genetic basis of host specificity and transmission success of experimental F(1) hybrids from two closely related tapeworm species (Schistocephalus solidus and S. pungitii), both highly specific to their respective vertebrate second intermediate hosts (three- and nine-spined sticklebacks, respectively). METHODS: We used an in vitro breeding system to hybridize Schistocephalus solidus and S. pungitii; hybridization rate was quantified using microsatellite markers. We measured several fitness relevant traits in pure lines of the parental parasite species as well as in their hybrids: hatching rates, infection rates in the copepod first host, and infection rates and growth in the two species of stickleback second hosts. RESULTS: We show that the parasites can hybridize in the in vitro system, although the proportion of self-fertilized offspring was higher in the heterospecific breeding pairs than in the control pure parental species. Hybrids have a lower hatching rate, but do not show any disadvantages in infection of copepods. In fish, hybrids were able to infect both stickleback species with equal frequency, whereas the pure lines were only able to infect their normal host species. CONCLUSIONS: Although not yet documented in nature, our study shows that hybridization in Schistocephalus spp. is in principle possible and that, in respect to their expanded host range, the hybrids are fitter. Further studies are needed to find the reason for the maintenance of the species boundaries in wild populations.