Temperature Alters Host Genotype-Specific Susceptibility to Chytrid Infection

The cost of parasitism often depends on environmental conditions and host identity. Therefore, variation in the biotic and abiotic environment can have repercussions on both, species-level host-parasite interaction patterns but also on host genotype-specific susceptibility to disease. We exposed seven genetically different but concurrent strains of the diatom Asterionella formosa to one genotype of its naturally co-occurring chytrid parasite Zygorhizidium planktonicum across five environmentally relevant temperatures. We found that the thermal tolerance range of the tested parasite genotype was narrower than that of its host, providing the host with a “cold” and “hot” thermal refuge of very low or no infection. Susceptibility to disease was host genotype-specific and varied with temperature level so that no genotype was most or least resistant across all temperatures. This suggests a role of thermal variation in the maintenance of diversity in disease related traits in this phytoplankton host. The duration and intensity of chytrid parasite pressure on host populations is likely to be affected by the projected changes in temperature patterns due to climate warming both through altering temperature dependent disease susceptibility of the host and, potentially, through en- or disabling thermal host refugia. This, in turn may affect the selective strength of the parasite on the genetic architecture of the host population.     

EVOLUTION OF HOST-PARASITE DIVERSITY

Hosts and parasites often have extensive genetic diversity for resistance and virulence (host range). Qualitative diversity occurs when the success of attack is an all-or-nothing response that varies according to the genotypes of the host and parasite. Quantitative diversity occurs when the success of attack is a graded response that depends on additive genetic variation in the host and parasite. Community diversity occurs when parasites vary in the success with which they can attack different host species, leading to a mixture of specialists and generalists. I developed a series of models that classify components of host-parasite interactions according to whether they cause stabilizing or disruptive selection for resistance and virulence. Stabilizing selection reduces diversity by favoring a single optimal phenotype. Disruptive selection creates diversity by favoring a mixture of widely separated phenotypes. The evolution of maximal resistance and virulence are opposed by one of three forces: metabolic costs, frequency dependence, or negative genetic correlations among beneficial traits. The models predict that qualitatively inherited resistance and virulence traits typically cause greater diversity than quantitatively inherited traits. However, each natural system is composed of many stabilizing factors that reduce diversity and disruptive factors that promote diversity. I advocate a style of modeling in which families of related assumptions are compared by their equilibrium properties, and general conclusions from equilibrium properties are tested by complete dynamical analysis. The comparison among models highlights the need for empirical studies that compare levels of diversity among related host-parasite systems.     

Food-environment mediates the outcome of specific interactions between a bumblebee and its trypanosome parasite

Specific host-parasite interactions, where the outcome of exposure to a parasite depends upon the genotypic identity of both parties, have implications for understanding host-parasite coevolution and patterns of genetic diversity. Thus, grasping the extent to which these interactions are mediated by environmental changes in a spatially and temporally heterogeneous world is vital. In this study, it is shown that the environment can influence specific host-parasite interactions in the well-studied system of the bumblebee Bombus terrestris and its trypanosome parasite Crithidia bombi. Naturally relevant variation in the quality of the food environment formed a three-way interaction with both host and parasite identity in determining the outcome of infection, with regard to the resistance of the host and the transmission of the parasite. The demonstration of such a host-genotype by parasite-genotype by environment interaction (G(H) x G(P) x E) shows the importance of considering environmental variation when investigating host-parasite interactions. Moreover, such interactions may to some extent explain levels of genetic diversity in natural host-parasite systems owing to the fact that they will create selection mosaics when environments are heterogeneous.     

THE EFFECTS OF HOST GENOTYPE AND SPATIAL DISTRIBUTION ON TREMATODE PARASITISM IN A BIVALVE POPULATION

A basic assumption underlying models of host-parasite coevolution is the existence of additive genetic variation among hosts for resistance to parasites. However, estimates of additive genetic variation are lacking for natural populations of invertebrates. Testing this assumption is especially important in view of current models that suggest parasites may be responsible for the evolution of sex, such as the Red Queen hypothesis. This hypothesis suggests that the twofold reproductive disadvantage of sex relative to parthenogenesis can be overcome by the more rapid production of rare genotypes resistant to parasites. Here I present evidence of significant levels of additive genetic variance in parasite resistance for an invertebrate host-parasite system in nature. Using families of the bivalve mollusc, Transennella tantilla, cultured in the laboratory, then exposed to parasites in the field, I quantified heritable variation in parasite resistance under natural conditions. The spatial distribution of outplanted hosts was also varied to determine environmental contributions to levels of parasite infection and to estimate potential interactions of host genotype with environment. The results show moderate but significant levels of heritability for resistance to parasites (h² = 0.36). The spatial distribution of hosts also significantly influenced parasite prevalence such that increased host aggregation resulted in decreased levels of parasite infection. Family mean correlations across environments were positive, indicating no genotype-environment interaction. Therefore, these results provide support for important assumptions underlying coevolutionary models of host-parasite systems.     

Disentangling the influence of parasite genotype, host genotype and maternal environment on different stages of bacterial infection in Daphnia magna

Individuals naturally vary in the severity of infectious disease when exposed to a parasite. Dissecting this variation into genetic and environmental components can reveal whether or not this variation depends on the host genotype, parasite genotype or a range of environmental conditions. Complicating this task, however, is that the symptoms of disease result from the combined effect of a series of events, from the initial encounter between a host and parasite, through to the activation of the host immune system and the exploitation of host resources. Here, we use the crustacean Daphnia magna and its parasite Pasteuria ramosa to show how disentangling genetic and environmental factors at different stages of infection improves our understanding of the processes shaping infectious disease. Using compatible host-parasite combinations, we experimentally exclude variation in the ability of a parasite to penetrate the host, from measures of parasite clearance, the reduction in host fecundity and the proliferation of the parasite. We show how parasite resistance consists of two components that vary in environmental sensitivity, how the maternal environment influences all measured aspects of the within-host infection process and how host-parasite interactions following the penetration of the parasite into the host have a distinct temporal component.     

Metazoan parasite species richness and genetic variation among freshwater fish species: cause or consequence?

The factors responsible for the maintenance of genetic variation among natural populations remain a mystery. Recent models of host-parasite co-evolution assume that parasites exert frequency-dependent selection on their hosts by favouring rare alleles that may confer resistance against infection. We tested this prediction in a comparative analysis that sought relationships between levels of genetic variation and the number of metazoan parasite species exploiting each host species. We used data on 40 species of North American freshwater fishes. After controlling for sampling effort and phylogenetic influences, we found no relationship between genetic polymorphism and parasite species richness among fish species. However, we found a marginal negative correlation between parasite species richness and heterozygosity. This result goes against the prediction that increased selective pressure by parasites should be associated with higher levels of genetic variation. Instead, it suggests that parasites may be colonising host species showing low levels of genetic variation with greater success than genetically more variable host species.     

Reciprocal Interaction Matrix Reveals Complex Genetic and Dose-Dependent Specificity among Coinfecting Parasites

Abstract Understanding genetic specificity in factors determining the outcome of host-parasite interactions is especially important as it contributes to parasite epidemiology, virulence, and maintenance of genetic variation. Such specificity, however, is still generally poorly understood. We examined genetic specificity in interactions among coinfecting parasites. In natural populations, individual hosts are often simultaneously infected by multiple parasite species and genotypes that interact. Such interactions could maintain genetic variation in parasite populations if they are genetically specific so that the relative fitness of parasite genotypes varies across host individuals depending on (1) the presence/absence of coinfections and/or (2) the genetic composition of the coinfecting parasite community. We tested these predictions using clones of fish eye flukes Diplostomum pseudospathaceum and Diplostomum gasterostei. We found that interactions among parasites had a strong genetic basis and that this modified genetic variation in infection success of D. pseudospathaceum between single and multiple infections as well as across multiply infected host individuals depending on the genetic identity of the coinfecting D. gasterostei. The relative magnitude of these effects, however, depended on the exposure dose, suggesting that ecological factors can modify genetic interactions between parasites.     

A bit of sex stabilizes host-parasite dynamics

To date, only a few studies have focused on the effects of sex on population dynamics. Previous models have typically found that sexual reproduction dampens population fluctuations. Although asexual and sexual reproduction are just the two endpoints along a continuum of varying rates of sex, previous work has ignored the effects of intermediate degrees of sex on population dynamics. Here we study the effects of partial sexual reproduction (i.e. sex occurs only every few generations or with small probability in each generation) on the coupled population dynamics of a Nicholson-Bailey host-parasite model. We show that complex dynamics are simplified for high host population growth rates if the frequency of sex is sufficiently high in both host and parasite: sex decreases fluctuations in population density, and leads to non-chaotic dynamics for population growth rates that would result in chaotic dynamics in the absence of sexual reproduction. However, the simplification does not increase gradually with an increasing frequency of sex but appears abruptly at low-to-intermediate frequencies of sex. For some parameter settings, intermediate frequencies of sexual reproduction can simplify the dynamics more than lower or higher frequencies. Thus, in agreement with earlier results, sexual reproduction typically stabilizes complex population dynamics in our models. Additionally, our results suggest that low-to-intermediate frequencies of sex may often be as (or even more) stabilizing as high frequencies.     

A quantitative genetic analysis of nuclear-cytoplasmic male sterility in structured populations of Silene vulgaris

Gynodioecy, the coexistence of functionally female and hermaphroditic morphs within plant populations, often has a complicated genetic basis involving several cytoplasmic male-sterility factors and nuclear restorers. This complexity has made it difficult to study the genetics and evolution of gynodioecy in natural populations. We use a quantitative genetic analysis of crosses within and among populations of Silene vulgaris to partition genetic variance for sex expression into nuclear and cytoplasmic components. We also use mitochondrial markers to determine whether cytoplasmic effects on sex expression can be traced to mitochondrial variance. Cytoplasmic variation and epistatic interactions between nuclear and cytoplasmic loci accounted for a significant portion of the variation in sex expression among the crosses. Source population also accounted for a significant portion of the sex ratio variation. Crosses among populations greatly enhanced the dam (cytoplasmic) effect, indicating that most among-population variance was at cytoplasmic loci. This is supported by the large among-population variance in the frequency of mitochondrial haplotypes, which also accounted for a significant portion of the sex ratio variance in our data. We discuss the similarities between the population structure we observed at loci that influence sex expression and previous work on putatively neutral loci, as well as the implications this has for what mechanisms may create and maintain population structure at loci that are influenced by natural selection.     

Genetic and environmental effects on secondary sex traits in guppies (Poecilia reticulata)

Male guppies (Poecilia reticulata) exhibit extreme phenotypic and genetic variability for several traits that are important to male fitness, and several lines of evidence suggest that resource level affects phenotypic expression of these traits in nature. We tested the hypothesis that genetic variation for male secondary sex traits could be maintained by genotype-specific effects of variable resource levels (genotype-environment interaction). To do this, we measured genetic variation and covariation under two environmental conditions--relatively low and relatively high food availability. We found high levels of genetic variation for most traits, but we only found a significant G x E interaction across food levels for one trait (body size) for one population. The across-environment correlations for size were large and positive, indicating that the reaction norms for size did not cross. We also found that male colour pattern elements had nearly an order of magnitude more genetic variation than did male size. Heritability estimates indicated that Y-linked genes are responsible for some of the genetic variation in male size and colour traits. We discuss implications of these results for theories of the maintenance of genetic variation in male secondary sexual traits in guppies.     

Pathogen fitness components and genotypes differ in their sensitivity to nutrient and temperature variation in a wild plant-pathogen association

Understanding processes maintaining variation in pathogen life-history stages affecting infectivity and reproduction is a key challenge in evolutionary ecology. Models of host-parasite coevolution are based on the assumption that genetic variation for host-parasite interactions is a significant cause of variation in infection, and that variation in environmental conditions does not overwhelm the genetic basis. However, surprisingly little is known about the stability of genotype-genotype interactions under variable environmental conditions. Here, using a naturally occurring plant-pathogen interaction, I tested whether the two distinct aspects of the infection process - infectivity and transmission potential - vary over realistic nutrient and temperature gradients. I show that the initial pathogen infectivity and host resistance responses are robust over the environmental gradients. However, for compatible responses there were striking differences in how different pathogen life-history stages and host and pathogen genotypes responded to environmental variation. For some pathogen genotypes even slight changes in temperature arrested spore production, rendering the developing infection ineffectual. The response of pathogen genotypes to environmental gradients varied in magnitude and even direction, so that their rankings changed across the abiotic gradients. Hence, the variable environment of spatially structured host-parasite interactions may strongly influence the maintenance of polymorphism in pathogen life-history stages governing transmission, whereas evolutionary trajectories of infectivity may be unaffected by the surrounding environment.     

Maternal influences on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination

Maternal and environmental factors are important sources of phenotypic variation because both factors influence offspring traits in ways that impact offspring and maternal fitness. The present study explored the effects of maternal factors (maternal body size, egg size, yolk‐steroid allocation, and oviposition‐site choice) and seasonally‐variable environmental factors on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination (Amphibolurus muricatus). Maternal identity had strong effects on offspring morphology, but the nature of maternal effects differed among successive clutches produced by females throughout the reproductive season (i.e. maternal identity by environment interactions). The among‐female and among‐clutch variation in offspring traits (including sex ratios) was not mediated through maternal body size, egg size, or variation in yolk steroid hormones. This lack of nongenetic maternal effects suggests that phenotypic variation may be generated by gene by environment interactions. These results demonstrate a significant genetic component to variation in offspring phenotypes, including sex ratios, even in species with environmental sex determination. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 256–266.     

Comparative landscape genetics reveals differential effects of environment on host and pathogen genetic structure in Tasmanian devils (Sarcophilus harrisii) and their transmissible tumour

Genetic structure in host species is often used to predict disease spread. However, host and pathogen genetic variation may be incongruent. Understanding landscape factors that have either concordant or divergent influence on host and pathogen genetic structure is crucial for wildlife disease management. Devil facial tumour disease (DFTD) was first observed in 1996 and has spread throughout almost the entire Tasmanian devil geographic range, causing dramatic population declines. Whereas DFTD is predominantly spread via biting among adults, devils typically disperse as juveniles, which experience low DFTD prevalence. Thus, we predicted little association between devil and tumour population structure and that environmental factors influencing gene flow differ between devils and tumours. We employed a comparative landscape genetics framework to test the influence of environmental factors on patterns of isolation by resistance (IBR) and isolation by environment (IBE) in devils and DFTD. Although we found evidence for broad‐scale costructuring between devils and tumours, we found no relationship between host and tumour individual genetic distances. Further, the factors driving the spatial distribution of genetic variation differed for each. Devils exhibited a strong IBR pattern driven by major roads, with no evidence of IBE. By contrast, tumours showed little evidence for IBR and a weak IBE pattern with respect to elevation in one of two tumour clusters we identify herein. Our results warrant caution when inferring pathogen spread using host population genetic structure and suggest that reliance on environmental barriers to host connectivity may be ineffective for managing the spread of wildlife diseases. Our findings demonstrate the utility of comparative landscape genetics for identifying differential factors driving host dispersal and pathogen transmission.     

Sex against virulence: the coevolution of parasitic diseases

Reciprocal selection is the underlying mechanism for host-parasite coevolutionary arms races. Its driving force is the reduction of host lifespan or fecundity that is caused by a parasite. Parasites evolve to optimize host exploitation, while hosts evolve to minimize the 'parasite-induced' loss of fitness (virulence). Research on the evolution of virulence has mostly emphasized the role of parasite evolution in determining virulence. However, host evolution, accelerated by sexual recombination, contributes to the evolution and expression of virulence as well. The Red Queen hypothesis predicts that genetic variation among host offspring facilitates selection for reduced virulence. Here, we outline a synthesis between current thinking about the evolution of virulence and the evolution of sex.     

Parasites, sex, and clonal diversity in natural snail populations

Under the Red Queen hypothesis, host-parasite coevolution selects against common host genotypes. Although this mechanism might underlie the persistence of sexual reproduction, it might also maintain high clonal diversity. Alternatively, clonal diversity might be maintained by multiple origins of parthenogens from conspecific sexuals, a feature in many animal groups. Herein, we addressed the maintenance of overall genetic diversity by coevolving parasites, as predicted by the Red Queen hypothesis. We specifically examined the contribution of parasites to host clonal diversity and the frequency of sexually reproducing individuals in natural stream populations of Potamopyrgus antipodarum snails. We also tested the alternative hypothesis that clonal diversity is maintained by the input of clones by mutation from sympatric sexuals. Clonal diversity and the frequency of sexual individuals were both positively related to infection frequency. Surprisingly, although clones are derived by mutation from sexual snails, parasites explained more of the genotypic variation among parthenogenetic subpopulations. Our findings thus highlight the importance of parasites as drivers of clonal diversity, as well as sex.     

Sex-specific response of a mosquito to parasites and crowding

Host-parasite interactions are significantly influenced by the sex of the host and the environment in which the host is found. Sex-specific responses to parasite infection, however, may change according to the host environment. I examine the combined effect of parasite infection and crowding on males and females of the mosquito Aedes albopictus. At a high larval density, infected males experienced a greater relative reduction in body size than did infected females, whereas the pattern was reversed at low density. This experiment demonstrates the importance of the environment on sex-specific responses to parasites and contributes to a growing body of work examining sources of variation in host-parasite interactions.     

Temporal and spatial variation of larval parasitism in non-outbreaking populations of a folivorous moth

In order to assess the role of parasitoids in the regulation of non-outbreaking populations of Epirrita autumnata, a geometrid lepidopteran with outbreaking populations in northern Europe, we examined the temporal and spatial variation of larval parasitism in southwestern Finland during 6 successive years. The study was carried out on two spatial scales, among trees within sites of about 1 ha and among sites separated by distances of 2–10 km, using experimental and observational approaches respectively. The overall percent parasitism was independent of host density on both spatial scales, while temporally it fluctuated only little. Of the two main parasitoids, the commoner one, Protapanteles immunis, showed a variable response to host density on the larger spatial scale and negative density dependence on the smaller scale. Temporally, parasitism caused by this species was independent of host density. Another parasitoid, Phobocampe bicingulata, showed positive density dependence on the smaller spatial scale and had a variable response on the larger scale, but exhibited negative density dependence over time. The results of this study caution against drawing conclusions concerning population regulation on the grounds of spatial density dependence alone. Larval parasitoids apparently do not maintain low densities in the E. autumnata populations studied. However, they may suppress E. autumnata densities to a level low enough for density-dependent mortality factor(s) to become regulating. Among other mortality factors of E. autumnata, pupal predation has been found to be temporally positively density-dependent. Received: 19 October 1999 / Accepted: 10 January 2000     

Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen

Parasite-mediated selection is potentially of great importance in modulating genetic diversity. Genetic variation for resistance, the fuel for natural selection, appears to be common in host-parasite interactions, but responses to selection are rarely observed. In the present study, we tested whether environmental variation could mediate infection and determine evolutionary outcomes. Temperature was shown to dramatically alter the potential for parasite-mediated selection in two independent laboratory infection experiments at four temperatures. The bacterial parasite, Pasteuria ramosa, was extremely virulent at 20 degrees C and 25 degrees C, sterilizing its host, Daphnia magna, so that females often never produced a single brood. However, at 10 degrees C and 15 degrees C, the host-parasite interaction was much more benign, as nearly all females produced broods before becoming sterile. This association between virulence and temperature alone could stabilize coexistence and lead to the maintenance of diversity, because it would weaken parasite-mediated selection during parts of the season. Additionally, highly significant genotype-by-environment interactions were found, with changes in clone rank order for infection rates at different temperatures. Our results clearly show that the outcome of parasite-mediated selection in this system is strongly context dependent.     

From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions

In most host-parasite systems, variation in parasite burden among hosts drives transmission dynamics. Heavily infected individuals introduce disproportionate numbers of infective stages into host populations or surrounding environments, causing sharp increases in frequency of infection. Parasite aggregation within host populations may result from variation among hosts in exposure to infective propagules and probability of subsequent establishment of parasites in the host. This is because individual host heterogeneities contribute to a pattern of parasite overdispersion that emerges at the population level. We quantified relative roles of host exposure and parasite establishment in producing variation in parasite burdens, to predict which hosts are more likely to bear heavy burdens, using big brown bats (Eptesicus fuscus) and their helminths as a model system. We captured bats from seven colonies in Michigan and Indiana, USA, assessed their helminth burdens, and collected data on intrinsic and extrinsic variables related to exposure, establishment, or both. Digenetic trematodes had the highest prevalence and mean abundance while cestodes and nematodes had much lower prevalence and mean abundance. Structural equation modeling revealed that best-fitting models to explain variations in parasite burden included genetic heterozygosity and immunocompetence as well as distance to the nearest water source and the year of host capture. Thus, both differential host exposure and differential parasite establishment significantly influence heterogeneous helminth burdens, thus driving population-level patterns of parasite aggregation.     

Demographic response to perturbations: the role of compensatory density dependence in a North American duck under variable harvest regulations and changing habitat

1. Most wild animal populations are subjected to many perturbations, including environmental forcing and anthropogenic mortality. How population size varies in response to these perturbations largely depends on life-history strategy and density regulation. 2. Using the mid-continent population of redhead Aythya americana (a North American diving duck), we investigated the population response to two major perturbations, changes in breeding habitat availability (number of ponds in the study landscape) and changes in harvest regulations directed at managing mortality patterns (bag limit). We used three types of data collected at the continental scale (capture-recovery, population surveys and age- and sex ratios in the harvest) and combined them into integrated population models to assess the interaction between density dependence and the effect of perturbations. 3. We observed a two-way interaction between the effects on fecundity of pond number and population density. Hatch-year female survival was also density dependent. Matrix modelling showed that population booms could occur after especially wet years. However, the effect of moderate variation in pond number was generally offset by density dependence the following year. 4. Mortality patterns were insensitive to changes in harvest regulations and, in males at least, insensitive to density dependence as well. We discuss potential mechanisms for compensation of hunting mortality as well as possible confounding factors. 5. Our results illustrate the interplay of density dependence and environmental variation both shaping population dynamics in a harvested species, which could be generalized to help guide the dual management of habitat and harvest regulations.