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Parasites, including pathogens, can adapt to better exploit their hosts on many scales, ranging from within an infection of a single individual to series of infections spanning multiple host species. However, little is known about how the genomes of parasites in natural communities evolve when they face diverse hosts. We investigated howBartonellabacteria that circulate in rodent communities in the dunes of the Negev Desert in Israel adapt to different species of rodent hosts. We propagated 15Bartonellapopulations through infections of either a single host species (Gerbillus andersoniorGerbillus pyramidum) or alternating between the two. After 20 rodent passages, strains withde novomutations replaced the ancestor in most populations. Mutations in two mononucleotide simple sequence repeats (SSRs) that caused frameshifts in the same adhesin gene dominated the evolutionary dynamics. They appeared exclusively in populations that encounteredG.andersoniand altered the dynamics of infections of this host. Similar SSRs in other genes are conserved and exhibit ON/OFF variation inBartonellaisolates from the Negev Desert dunes. Our results suggest that SSR-based contingency loci could be important not only for rapidly and reversibly generating antigenic variation to escape immune responses but that they may also mediate the evolution of host specificity. 

Determining the effects of parasites on host reproduction is key to understanding how parasites affect the underpinnings of selection on hosts. Although infection is expected to be costly, reducing mean fitness, infection could also increase variation in fitness costs among hosts, both of which determine the potential for selection on hosts. To test these ideas, we used a phylogenetically informed meta-analysis of 118 studies to examine how changes in the mean and variance in the outcome of reproduction differed between parasitized and non-parasitized hosts. We found that parasites had severe negative effects on mean fitness, with parasitized hosts suffering reductions in fecundity, viability and mating success. Parasite infection also increased variance in reproduction, particularly fecundity and offspring viability. Surprisingly, parasites had similar effects on viability when either the male or female was parasitized. These results not only provide the first synthetic, comparative, and quantitative summary of the strong deleterious effects of parasites on host reproductive fitness, but also reveal a consistent role for parasites in shaping the opportunity for selection. 

Abstract The extent and magnitude of parasitism often vary among closely related host species and across populations within species. Determining the ecological basis for this species and population‐level variation in parasitism is critical for understanding infection dynamics in multi‐host–parasite systems. To investigate such ecological underpinnings of variation in parasitism, we studiedEnallagmadamselfly host species and their water mite (Arrenurusspp.) ectoparasites in lakes.We first evaluated how host identity and density could shape parasitism. To test the effects of con‐ and heterospecific host density on parasitism, we used a field experiment withEnallagma basidensandE. signatum. We found that parasitism did not vary with con‐ or heterospecific density and was determined by host identity alone, with no spillover effects.We also evaluated the potential role of local adaptation and resource availability in shaping parasitism. To do so, we usedE. signatumin a reciprocal transplant experiment crossed with a prey resource‐level manipulation. This experiment revealed that parasitism declined sharply for one host population in its non‐local lake, but not the other source population, with no effects of prey levels. This asymmetry implies that damselflies express enhanced defences against parasitism that are neither population‐specific nor dependent on resource abundance, or that mites developed heightened local host specificity.The results of multivariate modeling from an observational study generally supported these experimental findings: neither host density nor resource abundance strongly explained among‐population variation in parasitism. Instead, local abiotic conditions (pH) had the strongest relationship with parasitism, with minimal associations with predator density, temperature and a measure of immune function.Collectively, our findings suggest a crucial role for the local environment in shaping host–parasite interactions within multi‐host–parasite systems. More generally, these results show that research at the intersection of community ecology and disease ecology is critical for understanding host–parasite dynamics within natural communities. 

Abstract Despite the ubiquitous nature of parasitism, how parasitism alters the outcome of host–species interactions such as competition, mutualism and predation remains unknown. Using a phylogenetically informed meta‐analysis of 154 studies, we examined how the mean and variance in the outcomes of species interactions differed between parasitized and non‐parasitized hosts. Overall, parasitism did not significantly affect the mean or variance of host–species interaction outcomes, nor did the shared evolutionary histories of hosts and parasites have an effect. Instead, there was considerable variation in outcomes, ranging from strongly detrimental to strongly beneficial for infected hosts. Trophically‐transmitted parasites increased the negative effects of predation, parasites increased and decreased the negative effects of interspecific competition for parasitized and non‐parasitized heterospecifics, respectively, and parasites had particularly strong negative effects on host species interactions in freshwater and marine habitats, yet were beneficial in terrestrial environments. Our results illuminate the diverse ways in which parasites modify critical linkages in ecological networks, implying that whether the cumulative effects of parasitism are considered detrimental depends not only on the interactions between hosts and their parasites but also on the many other interactions that hosts experience.