Co‐variation between the intensity of behavioural manipulation and parasite development time in an acanthocephalan–amphipod system

Pomphorhynchus laevis, a fish acanthocephalan parasite, manipulates the behaviour of its gammarid intermediate host to increase its trophic transmission to the definitive host. However, the intensity of behavioural manipulation is variable between individual gammarids and between parasite populations. To elucidate causes of this variability, we compared the level of phototaxis alteration induced by different parasite sibships from one population, using experimental infections of Gammarus pulex by P. laevis. We used a naive gammarid population, and we carried out our experiments in two steps, during spring and winter. Moreover, we also investigated co‐variation between phototaxis (at different stages of infection, ‘young’ and ‘old cystacanth stage’) and two other fitness‐related traits, infectivity and development time. Three main parameters could explain the parasite intra‐population variation in behavioural manipulation. The genetic variation, suggested by the differences between parasite families, was lower than the variation owing to an (unidentified) environmental factor. Moreover, a correlation was found between development rate and the intensity of behavioural change, the fastest growing parasites being unable to induce rapid phototaxis reversal. This suggests that parasites cannot optimize at the same time these two important parameters of their fitness, and this could explain a part of the variation observed in the wild.     

Alternative measures of response to Pseudomonas aeruginosa infection in Drosophila melanogaster

Studies of invertebrate immune defence often measure genetic variation either for the fitness cost of infection or for the ability of the host to clear the parasite. These studies assume that variation in measures of resistance is related to variation in fitness costs of infection. To test this assumption, we infected strains of the fruit fly, Drosophila melanogaster, with a pathogenic bacterium. We then measured the correlation between host bacterial load and the ability to survive infection. Despite the presence of genotypic variation for both traits, bacterial load and survival post-infection were not correlated. Our results support previous arguments that individual measures of immune function and the host's ability to survive infection may be decoupled. In light of these results, we suggest that the difference between tolerance and resistance to infection, a distinction commonly found in the plant literature, may also be of value in studies of invertebrate immunity.     

Resistance and tolerance in a host plant-holoparasitic plant interaction: genetic variation and costs

Host organisms are believed to evolve defense mechanisms (i.e., resistance and/or tolerance) under selective pressures exerted by natural enemies. A prerequisite for the evolution of resistance and tolerance is the existence of genetic variation in these traits for natural selection to act. However, selection for resistance and/or tolerance may be constrained by negative genetic correlations with other traits that affect host fitness. We studied genetic variation in resistance and tolerance against parasitic infection and the potential fitness costs associated with these traits using a novel study system, namely the interaction between a flowering plant and a parasitic plant. In this system, parasitic infection has significant negative effects on host growth and reproduction and may thus act as a selective agent. We conducted a greenhouse experiment in which we grew host plants, Urtica dioica, that originated from a single natural population and represented 20 maternal families either uninfected or infected with the holoparasitic dodder, Cuscuta europaea. that originated from the same site. We calculated correlations among resistance, tolerance, and host performance to test for costs of resistance and tolerance. We measured resistance as parasite performance (quantitative resistance) and tolerance as the slopes of regressions relating the vegetative and reproductive biomass of host plants to damage level (measured as parasite biomass). We observed significant differences among host families in parasite resistance and in parasite tolerance in terms of reproductive biomass, a result that suggests genetic variation in these traits. Furthermore, we found differences in resistance and tolerance between female and male host plants. In addition, the correlations indicate costs of resistance in terms of host growth and reproduction and costs of tolerance in terms of host reproduction. Our results thus indicate that host tolerance and resistance can evolve as a response to infection by a parasitic plant and that costs of resistance and tolerance may be one factor maintaining genetic variation in these traits.     

Genetic variation and covariation of aphid life-history traits across unrelated host plants

A central paradigm of life-history theory is the existence of resource mediated trade-offs among different traits that contribute to fitness, yet observations inconsistent with this tenet are not uncommon. We previously found a clonal population of the aphid Myzus persicae to exhibit positive genetic correlations among major components of fitness, resulting in strong heritable fitness differences on a common host. This raises the question of how this genetic variation is maintained. One hypothesis states that variation for resource acquisition on different hosts may override variation for allocation, predicting strong fitness differences within hosts as a rule, but changes in fitness hierarchies across hosts due to trade-offs. Therefore, we carried out a life-table experiment with 17 clones of M. persicae, reared on three unrelated host plants: radish, common lambsquarters and black nightshade. We estimated the broad-sense heritabilities of six life-history traits on each host, the genetic correlations among traits within hosts, and the genetic correlations among traits on different hosts (cross-environment genetic correlations). The three plants represented radically different environments with strong effects on performance of M. persicae, yet we detected little evidence for trade-offs. Fitness components were positively correlated within hosts but also between the two more benign hosts (radish and lambsquarters), as well as between those and another host tested earlier. The comparison with the most stressful host, nightshade, was hampered by low survival. Survival on nightshade also exhibited genetic variation but was unrelated to fitness on other hosts. Acknowledging that the number of environments was necessarily limited in a quantitative genetic experiment, we suggest that the rather consistent fitness hierarchies across very different plants provided little evidence to support the idea that the clonal variation for life-history traits and their covariance structure are maintained by strong genotypexenvironment interactions with respect to hosts. Alternative explanations are discussed.     

Epidemiological, evolutionary, and coevolutionary implications of context-dependent parasitism

Abstract Victims of infection are expected to suffer increasingly as parasite population growth increases. Yet, under some conditions, faster-growing parasites do not appear to cause more damage, and infections can be quite tolerable. We studied these conditions by assessing how the relationship between parasite population growth and host health is sensitive to environmental variation. In experimental infections of the crustacean Daphnia magna and its bacterial parasite Pasteuria ramosa, we show how easily an interaction can shift from a severe interaction, that is, when host fitness declines substantially with each unit of parasite growth, to a tolerable relationship by changing only simple environmental variables: temperature and food availability. We explored the evolutionary and epidemiological implications of such a shift by modeling pathogen evolution and disease spread under different levels of infection severity and found that environmental shifts that promote tolerance ultimately result in populations harboring more parasitized individuals. We also find that the opportunity for selection, as indicated by the variance around traits, varied considerably with the environmental treatment. Thus, our results suggest two mechanisms that could underlie coevolutionary hotspots and coldspots: spatial variation in tolerance and spatial variation in the opportunity for selection.     

Host dispersal as the driver of parasite genetic structure: a paradigm lost?

Understanding traits influencing the distribution of genetic diversity has major ecological and evolutionary implications for host–parasite interactions. The genetic structure of parasites is expected to conform to that of their hosts, because host dispersal is generally assumed to drive parasite dispersal. Here, we used a meta‐analysis to test this paradigm and determine whether traits related to host dispersal correctly predict the spatial co‐distribution of host and parasite genetic variation. We compiled data from empirical work on local adaptation and host–parasite population genetic structure from a wide range of taxonomic groups. We found that genetic differentiation was significantly lower in parasites than in hosts, suggesting that dispersal may often be higher for parasites. A significant correlation in the pairwise genetic differentiation of hosts and parasites was evident, but surprisingly weak. These results were largely explained by parasite reproductive mode, the proportion of free‐living stages in the parasite life cycle and the geographical extent of the study; variables related to host dispersal were poor predictors of genetic patterns. Our results do not dispel the paradigm that parasite population genetic structure depends on host dispersal. Rather, we highlight that alternative factors are also important in driving the co‐distribution of host and parasite genetic variation.     

MAINTENANCE OF GENETIC VARIATION IN IMMUNE DEFENSE OF A FRESHWATER SNAIL: ROLE OF ENVIRONMENTAL HETEROGENEITY

Natural populations often show genetic variation in pathogen resistance, which is paradoxal because natural selection is expected to erode genetic variation in fitness‐related traits. Several different factors have been suggested to maintain such variation, but their relative importance is still poorly understood. Here we examined if environmental heterogeneity and genetic trade‐offs could contribute to the maintenance of genetic variation in immune function of a freshwater snail Lymnaea stagnalis. We assessed the immunocompetence of snails originating from different families and maintained in different feeding treatments (ad libitum feeding, no food) by measuring the density of circulating hemocytes, phenoloxidase activity, and antibacterial activity of snail hemolymph. Food limitation reduced snail immune function, and we found significant among‐family variation in hemocyte concentration and PO activity, but not in antibacterial activity. Interestingly, food availability modified the family‐level variation observed in PO activity so that the relative immunocompetence of different snail families changed over environmental conditions (G × E interaction). We found no evidence for genetic trade‐offs between snail growth and immune defense nor among immune traits. Thus, our findings support the idea that environmental heterogeneity may promote maintenance of genetic variation in immune defense, but also suggest that different immune traits might not respond similarly to environmental variation.     

A field study on the influence of food and immune priming on a bumblebee–gut parasite system

Laboratory experiments are often preferred over field experiments because they allow the control of confounding factors that would otherwise influence the causal effect of a particular focal experimental factor. These confounding factors can, however, significantly alter the response of an organism confronted with a particular situation, which can have great implications. In a field experiment with a bumblebee host–parasite system, we looked at the influence of additional food supply and immune challenge on various colony fitness values and parasite traits. We could confirm the importance of food on the colony fitness, but not on parasite infection probability or parasite genetic diversity. In contrast to the findings of laboratory experiments of this system, challenge of the immune system had no significant effect on colony fitness or parasite infections. These results likely reflect an overriding effect of environmental variation without disproving the concept of a cost of defence per se. But the results also demonstrate that confounding factors purposely controlled for in the laboratory have to be weighed against their ecological relevance, and stress the need for careful analysis before any direct transfer is made of laboratory results to field situations.     

Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa

Genetic variation among hosts for resistance to parasites is an important assumption underlying evolutionary theory of host and parasite evolution. Using the castrating bacterial parasite Pasteuria ramosa and its cladoceran host Daphnia magna, we examined both within- and between-population genetic variation for resistance. First, we tested hosts from four populations for genetic variation for resistance to three parasite isolates. Allozyme analysis revealed significant host population divergence and that genetic distance corresponds to geographic distance. Host and parasite fitness components showed strong genetic differences between parasite isolates for host population by parasite interactions and for clones within populations, whereas host population effects were significant for only a few traits. In a second experiment we tested explicitly for within-population differences in variation for resistance by challenging nine host clones from a single population with four different parasite spore doses. Strong clone and dose effects were evident. More susceptible clones also suffered higher costs once infected. The results indicate that within-population variation for resistance is high relative to between-population variation. We speculate that P. ramosa adapts to individual host clones rather than to its host population.     

Temperature effects on parasite prevalence in a natural hybrid complex

Both host susceptibility and parasite infectivity commonly have a genetic basis, and can therefore be shaped by coevolution. However, these traits are often sensitive to environmental variation, resulting in genotype-by-environment interactions. We tested the influence of temperature on host–parasite genetic specificity in the Daphnia longispina hybrid complex, exposed to the protozoan parasite Caullerya mesnili. Infection rates were higher at low temperature. Furthermore, significant differences between host clones, but not between host taxa, and a host genotype-by-temperature interaction were observed.     

Specialization and local adaptation of a fungal parasite on two host plant species as revealed by two fitness traits

We investigate the geographic pattern of adaptation of a fungal parasite, Colletotrichum lindemuthianum, on two host species, Phaseolus vulgaris and P. coccineus for two parasite fitness traits: infectivity (ability to attack a host individual) and aggressivity (degree of sporulation and leaf surface damage). Using a cross-inoculation experiment, we show specialization of the fungus on its host species of origin for both traits even when fungi, which originated from hosts growing in sympatry, were tested on sympatric host populations. Within the two host species, we compared infectivity and aggressivity on local versus allopatric plant-fungus combinations. We found evidence for local adaptation for the two traits on P. vulgaris but not on P. coccineus. There was no significant correlation between the degrees of local adaptation for infectivity and aggressivity, indicating that the genetic basis and the effect of selection may differ between these two traits. For the two fitness traits, a positive correlation between the degree of specialization and the degree of local adaptation was found, suggesting that specialization can be reinforced by local adaptation.     

Heritable variation in host tolerance and resistance inferred from a wild host–parasite system

Hosts have evolved two distinct defence strategies against parasites: resistance (which prevents infection or limit parasite growth) and tolerance (which alleviates the fitness consequences of infection). However, heritable variation in resistance and tolerance and the genetic correlation between these two traits have rarely been characterized in wild host populations. Here, we estimate these parameters for both traits in Leuciscus burdigalensis, a freshwater fish parasitized by Tracheliastes polycolpus. We used a genetic database to construct a full-sib pedigree in a wild L. burdigalensis population. We then used univariate animal models to estimate inclusive heritability (i.e. all forms of genetic and non-genetic inheritance) in resistance and tolerance. Finally, we assessed the genetic correlation between these two traits using a bivariate animal model. We found significant heritability for resistance (H = 17.6%; 95% CI: 7.2–32.2%) and tolerance (H = 18.8%; 95% CI: 4.4–36.1%), whereas we found no evidence for the existence of a genetic correlation between these traits. Furthermore, we confirm that resistance and tolerance are strongly affected by environmental effects. Our results demonstrate that (i) heritable variation exists for parasite resistance and tolerance in wild host populations, and (ii) these traits can evolve independently in populations.     

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.     

Specific interactions between host and parasite genotypes do not act as a constraint on the evolution of antiviral resistance in Drosophila

Genetic correlations between parasite resistance and other traits can act as an evolutionary constraint and prevent a population from evolving increased resistance. For example, previous studies have found negative genetic correlations between host resistance and life-history traits. In invertebrates, the level of resistance often depends on the combination of the host and parasite genotypes, and in this study, we have investigated whether such specific resistance also acts as an evolutionary constraint. We measured the resistance of different genotypes of the fruit fly Drosophila melanogaster to different genotypes of a naturally occurring pathogen, the sigma virus. Using a multitrait analysis, we examine whether genetic covariances alter the potential to select for general resistance against all of the different viral genotypes. We found large amounts of heritable variation in resistance, and evidence for specific interactions between host and parasite, but these interactions resulted in little constraint on Drosophila evolving greater resistance.     

Parasite‐mediated selection in a natural metapopulation of Daphnia magna

Parasite‐mediated selection varying across time and space in metapopulations is expected to result in host local adaptation and the maintenance of genetic diversity in disease‐related traits. However, nonadaptive processes like migration and extinction‐(re)colonization dynamics might interfere with adaptive evolution. Understanding how adaptive and nonadaptive processes interact to shape genetic variability in life‐history and disease‐related traits can provide important insights into their evolution in subdivided populations. Here we investigate signatures of spatially fluctuating, parasite‐mediated selection in a natural metapopulation of Daphnia magna. Host genotypes from infected and uninfected populations were genotyped at microsatellite markers, and phenotyped for life‐history and disease traits in common garden experiments. Combining phenotypic and genotypic data a Q_ST–F_ST‐like analysis was conducted to test for signatures of parasite mediated selection. We observed high variation within and among populations for phenotypic traits, but neither an indication of host local adaptation nor a cost of resistance. Infected populations have a higher gene diversity (Hs) than uninfected populations and Hs is strongly positively correlated with fitness. These results suggest a strong parasite effect on reducing population level inbreeding. We discuss how stochastic processes related to frequent extinction‐(re)colonization dynamics as well as host and parasite migration impede the evolution of resistance in the infected populations. We suggest that the genetic and phenotypic patterns of variation are a product of dynamic changes in the host gene pool caused by the interaction of colonization bottlenecks, inbreeding, immigration, hybrid vigor, rare host genotype advantage and parasitism. Our study highlights the effect of the parasite in ameliorating the negative fitness consequences caused by the high drift load in this metapopulation.     

POSITIVE GENETIC CORRELATION BETWEEN PARASITE RESISTANCE AND BODY SIZE IN A FREE-LIVING UNGULATE POPULATION

Abstract Parasite resistance and body size are subject to directional natural selection in a population of feral Soay sheep (Ovis aries) on the island of St. Kilda, Scotland. Classical evolutionary theory predicts that directional selection should erode additive genetic variation and favor the maintenance of alleles that have negative pleiotropic effects on other traits associated with fitness. Contrary to these predictions, in this study we show that there is considerable additive genetic variation for both parasite resistance, measured as fecal egg count (FEC), and body size, measured as weight and hindleg length, and that there are positive genetic correlations between parasite resistance and body size in both sexes. Body size traits had higher heritabilities than parasite resistance. This was not due to low levels of additive genetic variation for parasite resistance, but was a consequence of high levels of residual variance in FEC. Measured as coefficients of variation, levels of additive genetic variation for FEC were actually higher than for weight or hindleg length. High levels of additive genetic variation for parasite resistance may be maintained by a number of mechanisms including high mutational input, balancing selection, antagonistic pleiotropy, and host‐parasite coevolution. The positive genetic correlation between parasite resistance and body size, a trait also subject to sexual selection in males, suggests that parasite resistance and growth are not traded off in Soay sheep, but rather that genetically resistant individuals also experience superior growth.     

Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal

Parasites detrimentally affect host fitness, leading to expectations of positive selection on host parasite resistance. However, as immunity is costly, host fitness may be maximized at low, but nonzero, parasite infection intensities. These hypotheses are rarely tested on natural variation in free-living populations. We investigated selection on a measure of host parasite resistance in a naturally regulated Soay sheep population using a longitudinal data set and found negative correlations between parasite infection intensity and annual fitness in lambs, male yearlings and adult females. However, having accounted for confounding effects of body weight, the effect was only significant in lambs. Associations between fitness and parasite resistance were environment-dependent, being strong during low-mortality winters, but negligible during harsher high-mortality winters. There was no evidence for stabilizing selection. Our findings reveal processes that may shape variation in parasite resistance in natural populations and illustrate the importance of accounting for correlated traits in selection analysis.     

Genetic structure and host–parasite co‐divergence: evidence for trait‐specific local adaptation

Host–parasite co‐evolution can lead to genetic differentiation among isolated host–parasite populations and local adaptation between parasites and their hosts. However, tests of local adaptation rarely consider multiple fitness‐related traits although focus on a single component of fitness can be misleading. Here, we concomitantly examined genetic structure and co‐divergence patterns of the trematode Coitocaecum parvum and its crustacean host Paracalliope fluviatilis among isolated populations using the mitochondrial cytochrome oxidase I gene (COI). We then performed experimental cross‐infections between two genetically divergent host–parasite populations. Both hosts and parasites displayed genetic differentiation among populations, although genetic structure was less pronounced in the parasite. Data also supported a co‐divergence scenario between C. parvum and P. fluviatilis potentially related to local co‐adaptation. Results from cross‐infections indicated that some parasite lineages seemed to be locally adapted to their sympatric (home) hosts in which they achieved higher infection and survival rates than in allopatric (away) amphipods. However, local, intrinsic host and parasite characteristics (host behavioural or immunological resistance to infections, parasite infectivity or growth rate) also influenced patterns of host–parasite interactions. For example, overall host vulnerability to C. parvum varied between populations, regardless of parasite origin (local vs. foreign), potentially swamping apparent local co‐adaptation effects. Furthermore, local adaptation effects seemed trait specific; different components of parasite fitness (infection and survival rates, growth) responded differently to cross‐infections. Overall, data show that genetic differentiation is not inevitably coupled with local adaptation, and that the latter must be interpreted with caution in a multi‐trait context.     

Immunity in a variable world

Immune function is likely to be a critical determinant of an organism's fitness, yet most natural animal and plant populations exhibit tremendous genetic variation for immune traits. Accumulating evidence suggests that environmental heterogeneity may retard the long-term efficiency of natural selection and even maintain polymorphism, provided alternative host genotypes are favoured under different environmental conditions. 'Environment' in this context refers to abiotic factors such as ambient temperature or availability of nutrient resources, genetic diversity of pathogens or competing physiological demands on the host. These factors are generally controlled in laboratory experiments measuring immune performance, but variation in them is likely to be very important in the evolution of resistance to infection. Here, we review some of the literature emphasizing the complexity of natural selection on immunity. Our aim is to describe how environmental and genetic heterogeneities, often excluded from experimentation as 'noise', may determine the evolutionary potential of populations or the potential for interacting species to coevolve.     

Vertebrate defense against parasites: Interactions between avoidance,resistance, and tolerance

Hosts can utilize different types of defense against the effects of parasitism, including avoidance, resistance, and tolerance. Typically, there is tremendous heterogeneity among hosts in these defense mechanisms that may be rooted in the costs associated with defense and lead to trade‐offs with other life‐history traits. Trade‐offs may also exist between the defense mechanisms, but the relationships between avoidance, resistance, and tolerance have rarely been studied. Here, we assessed these three defense traits under common garden conditions in a natural host–parasite system, the trematode eye‐fluke Diplostomum pseudospathaceum and its second intermediate fish host. We looked at host individuals originating from four genetically distinct populations of two closely related salmonid species (Atlantic salmon, Salmo salar and sea trout, Salmo trutta trutta) to estimate the magnitude of variation in these defense traits and the relationships among them. We show species‐specific variation in resistance and tolerance and population‐specific variation in resistance. Further, we demonstrate evidence for a trade‐off between resistance and tolerance. Our results suggest that the variation in host defense can at least partly result from a compromise between different interacting defense traits, the relative importance of which is likely to be shaped by environmental components. Overall, this study emphasizes the importance of considering different components of the host defense system when making predictions on the outcome of host–parasite interactions.