Strong neutral genetic differentiation in a host, but not in its parasite.

The genetic diversity and population structure of a parasite with a complex life cycle generally depends on the dispersal by its most motile host. Given that high gene flow is assumed to hinder local adaptation, this can impose significant constraints on a parasite's potential to adapt to local environmental conditions, intermediate host populations, and ultimately to host-parasite coevolution. Here, we aimed to examine the population genetic basis for local host-parasite interactions between the eye fluke Diplostomum lineage 6, a digenean trematode with a multi-host life cycle (including a snail, a fish, and a bird) and its second intermediate host, the three-spined stickleback Gasterosteus aculeatus L. We developed the first microsatellite primers for D. lineage 6 and used them together with published stickleback markers to analyse host and parasite population structures in 19 freshwater lakes, which differ in their local environmental characteristics regarding water chemistry and Diplostomum abundance. Our analyses suggest that one parasite population successfully infects a range of genetically differentiated stickleback populations. The lack of neutral genetic differentiation in D. lineage 6, which could be attributed to the motility of the parasite's definitive host as well as its life cycle characteristics, makes local host-parasite co-adaptations seem more likely on a larger geographical scale than among the lakes of our study site. Our study provides a suitable background for future studies in this system and the first microsatellite primers for a widespread fish parasite.

Distribution of common stickleback parasites on North Uist, Scotland, in relation to ecology and host traits.

Analysing spatial differences among macroparasite communities is an important tool in the study of host-parasite interactions. Identifying patterns can shed light on the underlying causes of heterogeneity of parasite distribution and help to better understand ecological constraints and the relative importance of host and parasite adaptations. In the present study, we aimed to find correlational evidence that the macroparasite distribution patterns on the Scottish island of North Uist, which had been described by de Roij and MacColl (2012), are indicative of local processes rather than an unspecific influence of habitat characteristics. We therefore reinvestigated parasite abundances and tested for associations with habitat characteristics and host traits. Distribution patterns of the most common parasites were largely consistent with the observations of de Roij and MacColl (2012). In accordance with the published results, we found that the most obvious abiotic habitat characteristic varying among the lakes on the island, pH, did not statistically explain parasite abundances (except for eye fluke species inside the lens). Instead, we found that genetic differentiation between host populations, measured as pairwise FST values based on available microsatellite data, was significantly correlated with dissimilarity in parasite community composition. Our results indicate that individual lake characteristics rather than physicochemical variables shape parasite distribution on this island, making it an ideal place to study host-parasite interactions. Furthermore, additionally to geographic distance measures taken from maps, we suggest taking into account connectivity among freshwater habitats, indirectly measured via fish population structure, to analyse spatial distribution patterns.

Sperm quality but not relatedness predicts sperm competition success in threespine sticklebacks (Gasterosteus aculeatus).

BACKGROUND: Mating between close relatives often leads to a reduction of an individual's fitness, due to an increased expression of deleterious alleles. Thus, in many animal taxa pre- as well as postcopulatory inbreeding avoidance mechanisms have evolved. An increased risk of inbreeding and hence a loss of genetic variation may occur during founder events as in most cases only few individuals establish a new population. The threespine stickleback (Gasterosteus aculeatus) is a small externally fertilizing fish species subject to strong sperm competition. Sticklebacks inhabit both marine and freshwater environments and anadromous populations have repeatedly established new genetically less diverse freshwater populations. Previous studies showed that anadromous sticklebacks strongly suffer from inbreeding depression and when given the choice females prefer to mate with unrelated males. RESULTS: The present study aimed to address whether there exists a postcopulatory inbreeding avoidance mechanism solely based on sperm-egg interactions in sperm competition experiments. We used F1 individuals that originated either from a large, genetically heterogeneous anadromous population or from a small, genetically less diverse freshwater population. For each population, eggs of two different females were in vitro fertilized by the same two males' sperm in a paired study design. In the main experiment one male was the female's full-sib brother and in the control experiment all individuals were unrelated. The results revealed that fertilization success was independent of relatedness in both populations suggesting a general lack of a postcopulatory inbreeding avoidance mechanism. Instead, male quality (i.e. sperm morphology) predicted paternity success during competitive fertilization trials. CONCLUSION: In sticklebacks, there is no evidence for postcopulatory inbreeding avoidance. Sperm morphology predicted paternity instead, thus sperm quality traits are under strong sexual selection, presumably driven by the high risk of sperm competition under natural conditions.

In vitro leukocyte response of three-spined sticklebacks (Gasterosteus aculeatus) to helminth parasite antigens.

Helminth parasites of teleost fish have evolved strategies to evade and manipulate the immune responses of their hosts. Responsiveness of fish host immunity to helminth antigens may therefore vary depending on the degree of host-parasite counter-adaptation. Generalist parasites, infective for a number of host species, might be unable to adapt optimally to the immune system of a certain host species, while specialist parasites might display high levels of adaptation to a particular host species. The degree of adaptations may further differ between sympatric and allopatric host-parasite combinations. Here, we test these hypotheses by in vitro exposure of head kidney leukocytes from three-spined sticklebacks (Gasterosteus aculeatus) to antigens from parasites with a broad fish host range (Diplostomum pseudospathaceum, Triaenophorus nodulosus), a specific fish parasite of cyprinids (Ligula intestinalis) and parasites highly specific only to a single fish species as second intermediate host (Schistocephalus pungitii, which does not infect G. aculeatus, and Schistocephalus solidus, infecting G. aculeatus). In vitro responses of stickleback leukocytes to S. solidus antigens from six European populations, with S. solidus prevalence from <1% to 66% were tested in a fully crossed experimental design. Leukocyte cultures were analysed by means of flow cytometry and a chemiluminescence assay to quantify respiratory burst activity. We detected decreasing magnitudes of in vitro responses to antigens from generalist to specialist parasites and among specialists, from parasites that do not infect G. aculeatus to a G. aculeatus-infecting species. Generalist parasites seem to maintain their ability to infect different host species at the costs of relatively higher immunogenicity compared to specialist parasites. In a comparison of sympatric and allopatric combinations of stickleback leukocytes and antigens from S. solidus, magnitudes of in vitro responses were dependent on the prevalence of the parasite in the population of origin, rather than on sympatry. Antigens from Norwegian (prevalence 30-50%) and Spanish (40-66%) S. solidus induced generally higher in vitro responses compared to S. solidus from two German (<1%) populations. Likewise, leukocytes from stickleback populations with a high S. solidus prevalence showed higher in vitro responses to S. solidus antigens compared to populations with low S. solidus prevalence. This suggests a rather low degree of local adaptation in S. solidus populations, which might be due to high gene flow among populations because of their extremely mobile final hosts, fish-eating birds.