Parasite infections are a product of both ecological processes affecting host-parasite encounter rates and evolutionary dynamics affecting host susceptibility. However, few studies examine natural infection variation from both ecological and evolutionary perspectives. Here, we describe the ecological and evolutionary factors generating variation in infection rates by a tapeworm (Schistocephalus solidus) in a vertebrate host, the threespine stickleback (Gasterosteus aculeatus). To explore ecological aspects of infection, we measured tapeworm prevalence in Canadian stickleback inhabiting two distinct environments: marine and freshwater. Consistent with ecological control of infection, the tapeworm is very rare in marine environments, even though marine fish are highly susceptible. Conversely, commonly infected freshwater stickleback exhibit substantial resistance in controlled laboratory trials, suggesting that high exposure risk overwhelms their recently evolved resistance. We also tested for parasite adaptation to its host by performing transcontinental reciprocal infections, using stickleback and tapeworm populations from Europe and western Canada. More infections occurred in same-continent host-parasite combinations, indicating parasite "local" adaptation, at least on the scale of continents. However, the recently evolved immunity of freshwater hosts applies to both local and foreign parasites. The pattern of adaptation described here is not wholly compatible with either of the common models of host-parasite coevolution (i.e., matching infection or targeted recognition). Instead, we propose a hybrid, eco-evolutionary model to explain the remarkable pattern of global host resistance and local parasite infectivity.
Parasites can be a major cause of natural selection on hosts, which consequently evolve a variety of strategies to avoid, eliminate, or tolerate infection. When ecologically similar host populations present disparate infection loads, this natural variation can reveal immunological strategies underlying adaptation to infection and population divergence. For instance, the tapeworm persistently infects 0-80% of threespine stickleback () in lakes on Vancouver Island. To test whether these heterogeneous infection rates result from evolved differences in immunity, we experimentally exposed laboratory-reared fish from ecologically similar high-infection and no-infection populations to controlled doses of We observed heritable between-population differences in several immune traits: Fish from the naturally uninfected population initiated a stronger granulocyte response to infection, and their granulocytes constitutively generate threefold more reactive oxygen species in cell culture. Despite these immunological differences, was equally successful at establishing initial infections in both host populations. However, the no-infection fish dramatically suppressed tapeworm growth relative to high-infection fish, and parasite size was intermediate in F1 hybrid hosts. Our results show that stickleback recently evolved heritable variation in their capacity to suppress helminth growth by two orders of magnitude. Data from many natural populations indicate that growth suppression is widespread but not universal and, when present, is associated with reduced infection prevalence. Host suppression of helminth somatic growth may be an important immune strategy that aids in parasite clearance or in mitigating the fitness costs of persistent infection.
Parasites can be a major cause of natural selection on hosts, which consequently evolve a variety of strategies to avoid, eliminate, or tolerate infection. When ecologically similar host populations present disparate infection loads, this natural variation can reveal immunological strategies underlying adaptation to infection and population divergence. For instance, the tapeworm Schistocephalus solidus persistently infects between 0% to 80% of threespine stickleback (Gasterosteus aculeatus) in lakes on Vancouver Island. To test whether these heterogeneous infection rates are due to evolved differences in immunity, we experimentally exposed lab-reared fish from high-and low-infection populations, which are not known to differ in natural exposure risk, to controlled doses of Schistocephalus. We observed heritable between-population differences in several immune traits: fish from the naturally uninfected population initiated a stronger granulocyte response to Schistocephalus infection, and their granulocytes constitutively generated threefold more reactive oxygen species (ROS). Despite these immunological differences, Schistocephalus was equally successful at establishing initial infections in both host populations. However, the low-infection fish dramatically suppressed tapeworm growth relative to high-infection fish, and parasite size was intermediate in F1hybrid hosts. Our results show that stickleback recently evolved heritable variation in their capacity to suppress helminth growth. Comparative data from many from natural populations indicate that growth suppression is widespread but not universal and, when present, is associated with reduced infection prevalence. Host suppression of helminth somatic growth may be an important immune strategy that aids in parasite clearance, or in mitigating the fitness costs of persistent infection.Significance: Large parasites remain a persistent source of morbidity and mortality in humans, domesticated animals, and wildlife. Hosts are subject to strong natural selection to eliminate or tolerate these parasite infections. Here, we document the recent evolution of a striking form of resistance by a vertebrate host (threespine stickleback) against its cestode parasite (Schistocephalus solidus). After Pleistocene glacial retreat, marine stickleback colonized freshwater lakes, encountered Schistocephalus, and evolved varying levels of resistance to it. We show that a heavily-and a rarely-infected population of stickleback have similar resistance to Schistocephalus colonization, but rarely-infected fish suppress parasite growth by orders of magnitude. These populations represent ends of a natural continuum of cestode growth suppression, which is associated with reduced infection prevalence.
In spatially structured host metapopulations (subdivided into isolated populations), this process of immune adaptation may lead to disparate phenotypic solutions, and population divergence (Brunner et al., 2013;Meihls et al., 2013;Weber, Kalbe, et al., 2017). Two populations may evolve to recognize different parasite antigens (e.g., a geographic mosaic of coevolution; Dodds & Thrall, 2009), use different facets of the immune system to achieve the same form of
Parasites impose fitness costs on their hosts. Biologists therefore tend to assume that natural selection favors infection-resistant hosts. Yet, when the immune response itself is costly, theory suggests selection may instead favor loss of resistance. Immune costs are rarely documented in nature, and there are few examples of adaptive loss of resistance. Here, we show that when marine threespine stickleback colonized freshwater lakes they gained resistance to the freshwater-associated tapeworm, Schistocephalus solidus. Extensive peritoneal fibrosis and inflammation contribute to suppression of cestode growth and viability, but also impose a substantial cost of reduced fecundity. Combining genetic mapping and population genomics, we find that the immune differences between tolerant and resistant populations arise from opposing selection in both populations acting, respectively, to reduce and increase resistance consistent with divergent optimization.One Sentence SummaryRecently-evolved freshwater populations of stickleback frequently evolve increased resistance to tapeworms, involving extensive fibrosis that suppresses parasite growth; because this fibrosis greatly reduces fish fecundity, in some freshwater populations selection has favored an infection-tolerant strategy with fibrosis suppression.
Parasites impose fitness costs on their hosts. Biologists often assume that natural selection favors infection-resistant hosts. Yet, when the immune response itself is costly, theory suggests that selection may sometimes favor loss of resistance, which may result in alternative stable states where some populations are resistant and others are tolerant. Intraspecific variation in immune costs is rarely surveyed in a manner that tests evolutionary patterns, and there are few examples of adaptive loss of resistance. Here, we show that when marine threespine stickleback colonized freshwater lakes, they gained resistance to the freshwater-associated cestode Schistocephalus solidus . Extensive peritoneal fibrosis and inflammation are a commonly observed phenotype that contributes to suppression of cestode growth and viability but also imposes a substantial cost on fecundity. Combining genetic mapping and population genomics, we find that opposing selection generates immune system differences between tolerant and resistant populations, consistent with divergent optimization.
Multiple biological processes can generate sexual selection on male visual signals such as color. For example, females may prefer colorful males because those males are more readily detected (perceptual bias), or because male color conveys information about male quality and associated direct or indirect benefits to females. For example, male threespine stickleback often exhibit red throat coloration, which females prefer both because red is more visible in certain environments, and red color is correlated with male immune function and parasite load. However, not all light environments favor red nuptial coloration: more tannin-stained water tends to favor the evolution of a melanic male phenotype. Do such population differences in stickleback male color, driven by divergent light environments, lead to changes in the relationship between color and immunity? Here, we show that, within stickleback populations, multiple components of male color (brightness and hue of four body parts) are correlated with multiple immune variables (ROS production, phagocytosis rates, and lymphocyte:leukocyte ratios). Some of these color-immune associations persist across stickleback populations with very different male color patterns, whereas other color-immune associations are population-specific. Overall, lakes with red males exhibit stronger color-immune covariance while melanic male populations exhibit weak if any color-immune associations. Our finding that color-immunity relationships are labile implies that any evolution of male color traits (e.g., due to female perceptual bias in a given light environment), can alter the utility of color as an indicator of male quality.
Despite the significant effect of host-parasite interactions on both ecological systems and organism health, there is still limited understanding of the mechanisms driving evolution of host resistance to parasites. One model of rapid evolution, the Baldwin Effect, describes the role of plasticity in adaptation to novel conditions, and subsequent canalization of associated traits. While mostly applied in the context of environmental conditions, this theory may be relevant to the evolution of host resistance to novel parasites. Here we test the applicability of the Baldwin Effect to the evolution of resistance in a natural system using threespine stickleback fish (Gasterosteus aculeatus) and their cestode parasite Schistochephalus solidus. We leverage a large transcriptomic data set to describe the response to S. solidus infection by three different genetic crosses of stickleback, from a resistant and a tolerant population. Hosts mount a multigenic response to the parasite that is similar among host genotypes. In addition, we document extensive constitutive variation in gene expression among host genotypes. However, although many genes are both infection-induced and differentially expressed between genotypes, this overlap is not more extensive than expected by chance. We also see little evidence of canalization of infection-induced gene expression in the derived resistant population. These patterns do not support the Baldwin Effect, though they illustrate the importance of variation in both constitutive expression and induced responses to parasites. Finally, our results improve understanding of the cellular mechanisms underlying a putative resistance phenotype (fibrosis). Combined, our results highlight the importance of both constitutive and inducible variation in the evolution of resistance to parasites, and identify new target genes contributing to fibrosis. These findings advance understanding of host-parasite interactions and co-evolutionary relationships in natural systems.
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