Organisms that can resist parasitic infection often have lower fitness in the absence of parasites. These costs of resistance can mediate host evolution during parasite epidemics. For example, large epidemics will select for increased host resistance. In contrast, small epidemics (or no disease) can select for increased host susceptibility when costly resistance allows more susceptible hosts to outcompete their resistant counterparts. Despite their importance for evolution in host populations, costs of resistance (which are also known as resistance trade-offs) have mainly been examined in laboratory-based host-parasite systems. Very few examples come from fieldcollected hosts. Furthermore, little is known about how resistance trade-offs vary across natural populations. We addressed these gaps using the freshwater crustacean Daphnia dentifera and its natural yeast parasite, Metschnikowia bicuspidata. We found a cost of resistance in two of the five populations we studied -those with the most genetic variation in resistance and the smallest epidemics in the previous year. However, yeast epidemics in the current year did not alter slopes of these trade-offs before and after epidemics. In contrast, the no-cost populations showed little variation in resistance, possibly because large yeast epidemics eroded that variation in the previous year. Consequently, our results demonstrate variation in costs of resistance in wild host populations. This variation has important implications for host evolution during epidemics in nature.
Generalist parasites can strongly influence interactions between native and invasive species. Host competence can be used to predict how an invasive species will affect community disease dynamics; the addition of a highly competent, invasive host is predicted to increase disease. However, densities of invasive and native species can also influence the impacts of invasive species on community disease dynamics. We examined whether information on host competence alone could be used to accurately predict the effects of an invasive host on disease in native hosts. We first characterized the relative competence of an invasive species and a native host species to a native parasite. Next, we manipulated species composition in mesocosms and found that host competence results did not accurately predict community dynamics. While the invasive host was more competent than the native, the presence of the native (lower competence) host increased disease in the invasive (higher competence) host. To identify potential mechanisms driving these patterns, we analyzed a two-host, one-parasite model parameterized for our system. Our results demonstrate that patterns of disease were primarily driven by relative population densities, mediated by asymmetry in intra- and interspecific competition. Thus, information on host competence alone may not accurately predict how an invasive species will influence disease in native species.
Habitat disturbance and anthropogenic change are globally associated with extinctions and invasive species introductions. Less understood is the impact of environmental change on the parasites harbored by endangered, extinct, and introduced species. To improve our understanding of the impacts of anthropogenic disturbance on such host-parasite interactions, we investigated an invasive trypanosome (Trypanosoma lewisi). We screened 348 individual small mammals, representing 26 species, from both forested and non-forested habitats in rural Uganda. Using microscopy and PCR, we identified 18% of individuals (order Rodentia) as positive for trypanosomes. Further phylogenetic analyses revealed two trypanosomes circulating-T. lewisi and T. varani. T. lewisi was found in seven species both native and invasive, while T. varani was identified in only three native forest species. The lack of T. varani in non-forested habitats suggests that it is a natural parasite of forest-dwelling rodents. Our findings suggest that anthropogenic disturbance may lead to spillover of an invasive parasite (T. lewisi) from non-native to native species, and lead to local co-extinction of a native parasite (T. varani) and native forest-dwelling hosts.
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