Parasite Local Adaptation Research Articles

Do biological control agents adapt to local pest genotypes? A multiyear test across geographic scales.

Parasite local adaptation has been a major focus of (co)evolutionary research on host-parasite interactions. Studies of wild host-parasite systems frequently find that parasites paired with local, sympatric host genotypes perform better than parasites paired with allopatric host genotypes. In contrast, there are few such tests in biological control systems to establish whether biological control parasites commonly perform better on sympatric pest genotypes. This knowledge gap prevents the optimal design of biological control programs: strong local adaptation could argue for the use of sympatric parasites to achieve consistent pest control. To address this gap, we tested for local adaptation of the biological control bacterium Pasteuria penetrans to the root-knot nematode Meloidogyne arenaria, a global threat to a wide range of crops. We measured the probability and intensity of P. penetrans infection on sympatric and allopatric M. arenaria over the course of 4 years. Our design accounted for variation in adaptation across scales by conducting tests within and across fields, and we isolated the signature of parasite adaptation by comparing parasites collected over the course of the growing season. Our results are largely inconsistent with local adaptation of P. penetrans to M. arenaria: in 3 of 4 years, parasites performed similarly well in sympatric and allopatric combinations. In 1 year, however, infection probability was 28% higher for parasites paired with hosts from their sympatric plot, relative to parasites paired with hosts from other plots within the same field. These mixed results argue for population genetic data to characterize the scale of gene flow and genetic divergence in this system. Overall, our findings do not provide strong support for using P. penetrans from local fields to enhance biological control of Meloidogyne.

Host-Parasite Coevolution in Continuous Space Leads to Variation in Local Adaptation across Spatial Scales.

AbstractPrevious host-parasite coevolutionary theory has focused on understanding the determinants of local adaptation using spatially discrete models. However, these studies fall short of describing patterns of host-parasite local adaptation across spatial scales. In contrast, empirical work demonstrates that patterns of adaptation depend on the scale at which they are measured. Here, we propose a mathematical model of host-parasite coevolution in continuous space that naturally leads to a scale-dependent definition of local adaptation. In agreement with empirical research, we find that patterns of adaptation vary across spatial scales. In some cases, not only the magnitude of local adaptation but also the identity of the locally adapted species will depend on the spatial scale at which measurements are taken. Building on our results, we suggest a way to consistently measure parasite local adaptation when continuous space is the driver of cross-scale variation. We also describe a way to test whether continuous space is driving cross-scale variation. Taken together, our results provide a new perspective that can be used to understand empirical observations previously unexplained by theoretical expectations and deepens our understanding of the mechanics of host-parasite local adaptation.

The roles of environmental variation and parasite survival in virulence-transmission relationships.

Disease outbreaks are a consequence of interactions among the three components of a host–parasite system: the infectious agent, the host and the environment. While virulence and transmission are widely investigated, most studies of parasite life-history trade-offs are conducted with theoretical models or tractable experimental systems where transmission is standardized and the environment controlled. Yet, biotic and abiotic environmental factors can strongly affect disease dynamics, and ultimately, host–parasite coevolution. Here, we review research on how environmental context alters virulence–transmission relationships, focusing on the off-host portion of the parasite life cycle, and how variation in parasite survival affects the evolution of virulence and transmission. We review three inter-related ‘approaches’ that have dominated the study of the evolution of virulence and transmission for different host–parasite systems: (i) evolutionary trade-off theory, (ii) parasite local adaptation and (iii) parasite phylodynamics. These approaches consider the role of the environment in virulence and transmission evolution from different angles, which entail different advantages and potential biases. We suggest improvements to how to investigate virulence–transmission relationships, through conceptual and methodological developments and taking environmental context into consideration. By combining developments in life-history evolution, phylogenetics, adaptive dynamics and comparative genomics, we can improve our understanding of virulence–transmission relationships across a diversity of host–parasite systems that have eluded experimental study of parasite life history.

The geography of parasite local adaptation to host communities

Fitness responses to environment can shape species distributions, though opposing eco‐evolutionary processes can obscure environmental effects. For example, host specificity influences parasite dynamics, but is unclear how adaptation of parasites to local host communities may scale up to continental distributions. Here, we develop a macroecological framework to determine how host community structure affects the distribution of specialist and generalist populations of Striga hermonthica, an African parasitic plant of cereal crops. Combining data from global crop production and parasite experimental trials, we find that parasites perform best on the host species that is most common in their location of origin. Moreover, niche model contrasts predict parasite specialization on two hosts that evolved alongside Striga during domestication (pearl millet and sorghum), indicating that specialist parasites may be most likely to occur where host niches differ most in multivariate environmental space. Our study demonstrates that patterns of parasite local adaptation to host communities can emerge at continental scales and that differential environmental tolerances of hosts indirectly shape the distribution of specialist and generalist parasites. By predicting spatial dynamics of parasite specialization versus generalization directly from environmental data, our approach may help inform current and future management of pests and disease.

Among-Strain Variation in Resistance of Paramecium caudatum to the Endonuclear Parasite Holospora undulata: Geographic and Lineage-Specific Patterns.

Resistance is a key determinant in interactions between hosts and their parasites. Understanding the amount and distribution of variation in this trait between strains can provide insights into (co)evolutionary processes and their potential to shape patterns of diversity in natural populations. Using controlled inoculation in experimental mass cultures, we investigated the quantitative variation in resistance to the bacterial parasite Holospora undulata across a worldwide collection of strains of its ciliate host Paramecium caudatum. We combined the observed variation with available information on the phylogeny and biogeography of the strains. We found substantial variation in resistance among strains, with upper-bound values of broad-sense heritability >0.5 (intraclass correlation coefficients). Strain estimates of resistance were repeatable between laboratories and ranged from total resistance to near-complete susceptibility. Early (1 week post inoculation) measurements provided higher estimates of resistance heritability than did later measurements (2–3 weeks), possibly due to diverging epidemiological dynamics in replicate cultures of the same strains. Genetic distance (based on a neutral marker) was positively correlated with the difference in resistance phenotype between strains (r = 0.45), essentially reflecting differences between highly divergent clades (haplogroups) within the host species. Haplogroup A strains, mostly European, were less resistant to the parasite (49% infection prevalence) than non-European haplogroup B strains (28%). At a smaller geographical scale (within Europe), strains that are geographically closer to the parasite origin (Southern Germany) were more susceptible to infection than those from further away. These patterns are consistent with a picture of local parasite adaptation. Our study demonstrates ample natural variation in resistance on which selection can act and hints at symbiont adaptation producing signatures in geographic and lineage-specific patterns of resistance in this model system.

Local adaptation of a parasite to solar radiation impacts disease transmission potential, spore yield, and host fecundity.

Environmentally transmitted parasites spend time in the abiotic environment, where they are subjected to a variety of stressors. Learning how they face this challenge is essential if we are to understand how host-parasite interactions may vary across environmental gradients. We used a zooplankton-bacteria host-parasite system where availability of sunlight (solar radiation) influences disease dynamics to look for evidence of parasite local adaptation to sunlight exposure. We also examined how variation in sunlight tolerance among parasite strains impacted host reproduction. Parasite strains collected from clearer lakes (with greater sunlight penetration) were most tolerant of the negative impacts of sunlight exposure, suggesting local adaptation to sunlight conditions. This adaptation came with both a cost and a benefit for parasites: parasite strains from clearer lakes produced relatively fewer transmission stages (spores) but these strains were more infective. After experimental sunlight exposure, the most sunlight-tolerant parasite strains reduced host fecundity just as much as spores that were never exposed to sunlight. Sunlight availability varies greatly among lakes around the world. Our results suggest that the selective pressure sunlight exposure exerts on parasites may impact both parasite and host fitness, potentially driving variation in disease epidemics and host population dynamics across sunlight availability gradients.

Gene flow and adaptive potential in a generalist ectoparasite

BackgroundIn host-parasite systems, relative dispersal rates condition genetic novelty within populations and thus their adaptive potential. Knowledge of host and parasite dispersal rates can therefore help us to understand current interaction patterns in wild populations and why these patterns shift over time and space. For generalist parasites however, estimates of dispersal rates depend on both host range and the considered spatial scale. Here, we assess the relative contribution of these factors by studying the population genetic structure of a common avian ectoparasite, the hen flea Ceratophyllus gallinae, exploiting two hosts that are sympatric in our study population, the great tit Parus major and the collared flycatcher Ficedula albicollis. Previous experimental studies have indicated that the hen flea is both locally maladapted to great tit populations and composed of subpopulations specialized on the two host species, suggesting limited parasite dispersal in space and among hosts, and a potential interaction between these two structuring factors.ResultsC. gallinae fleas were sampled from old nests of the two passerine species in three replicate wood patches and were genotyped at microsatellite markers to assess population genetic structure at different scales (among individuals within a nest, among nests and between host species within a patch and among patches). As expected, significant structure was found at all spatial scales and between host species, supporting the hypothesis of limited dispersal in this parasite. Clustering analyses and estimates of relatedness further suggested that inbreeding regularly occurs within nests. Patterns of isolation by distance within wood patches indicated that flea dispersal likely occurs in a stepwise manner among neighboring nests. From these data, we estimated that gene flow in the hen flea is approximately half that previously described for its great tit hosts.ConclusionOur results fall in line with predictions based on observed patterns of adaptation in this host-parasite system, suggesting that parasite dispersal is limited and impacts its adaptive potential with respect to its hosts. More generally, this study sheds light on the complex interaction between parasite gene flow, local adaptation and host specialization within a single host-parasite system.

Habitat Heterogeneity, Host Population Structure, and Parasite Local Adaptation.

Reciprocal-transplant experiments have proven to be a powerful tool for detecting local adaptation (LA). More recently, reciprocal cross-inoculation experiments have been used to evaluate adaptation by parasites to their local host populations. These experiments are conceptually similar to reciprocal-transplant experiments, except that the "environment" (the host population) may have evolved in response to changes in the parasite population. Here, I use analytical tools and computer simulations to determine when parasites would be expected to be more infective to their local host populations than to allopatric host populations. The models assume that parasites have to genetically "match" their hosts in order to infect. I also assumed that different host clones were favored in different populations. When parasite virulence was low, clonal selection outweighed parasite-mediated selection, leading to low host diversity within populations and strong LA by parasites. At intermediate levels of virulence, parasite-mediated selection maintained high levels of host diversity within populations, which reduced or eliminated parasite LA. The loss of parasite LA was not associated with increased infectivity by parasites on allopatric hosts. Instead, the loss of LA was due to a reduction in infectivity of parasites on sympatric hosts. Finally, at high levels of parasite virulence, parasite-mediated selection led to oscillatory host dynamics and weak local adaption by parasites. Across all levels of virulence, the strength of parasite LA closely tracked the degree of host population structure (GST).

Rethinking Conventional Wisdom: Are Locally Adapted Parasites Ahead in the Coevolutionary Race?

The metaphors of the Red Queen and the arms race have inspired a large amount of research aimed at understanding the process of antagonistic coevolution between hosts and parasites. One approach that has been heavily used is to estimate the strength of parasite local adaptation using a reciprocal cross infection or transplant study. These studies frequently conclude that the locally adapted species is ahead in the coevolutionary race. Here, I use mathematical models to decompose parasite infectivity into components attributable to local versus global adaptation and to develop a robust index of which species is ahead in the coevolutionary race, which I term coevolutionary advantage. Computer simulations of coevolving host-parasite interactions demonstrate that because the magnitudes of local and global adaptation are largely independent, the link between the sign of local adaptation and coevolutionary advantage is tenuous. A consequence of the weak coupling between local adaptation and coevolutionary advantage is that the bulk of existing empirical studies do not sample enough populations for any reliable conclusions to be drawn. Together, these results suggest that the long-standing conventional wisdom holding that locally adapted parasites are ahead in the coevolutionary race should be reconsidered.

Parasite transmission among relatives halts Red Queen dynamics.

The theory that coevolving hosts and parasites create a fluctuating selective environment for one another (i.e., produce Red Queen dynamics) has deep roots in evolutionary biology; yet empirical evidence for Red Queen dynamics remains scarce. Fluctuating coevolutionary dynamics underpin the Red Queen hypothesis for the evolution of sex, as well as hypotheses explaining the persistence of genetic variation under sexual selection, local parasite adaptation, the evolution of mutation rate, and the evolution of nonrandom mating. Coevolutionary models that exhibit Red Queen dynamics typically assume that hosts and parasites encounter one another randomly. However, if related individuals aggregate into family groups or are clustered spatially, related hosts will be more likely to encounter parasites transmitted by genetically similar individuals. Using a model that incorporates familial parasite transmission, we show that a slight degree of familial parasite transmission is sufficient to halt coevolutionary fluctuations. Our results predict that evidence for Red Queen dynamics, and its evolutionary consequences, are most likely to be found in biological systems in which hosts and parasites mix mainly at random, and are less likely to be found in systems with familial aggregation. This presents a challenge to the Red Queen hypothesis and other hypotheses that depend on coevolutionary cycling.

Parasite genetic distance and local adaptation in co-evolving bacteria-bacteriophage populations.

Antagonistic co-evolution between hosts and parasites can lead to local adaptation (LA) such that parasite fitness is greatest in sympatric hosts (or vice versa). The magnitude of LA typically increases with geographical distance, which is assumed to be because genetic (and hence phenotypic) distance increases with geographical distance. Here, we explicitly test the relationships between parasite genetic and phenotypic distance and LA using isolates of co-evolved viral parasites (lytic bacteriophage ϕ2) and the host bacterium Pseudomonas fluorescens SBW25. We find positive relationships between parasite genotype and infectivity phenotype, but the strength of the relationship was greater when infectivity was defined by the identity of hosts that could be infected rather than the actual number of hosts infected (host range), and when measurements were compared within rather than among populations. Crucially, we find a monotonic relationship between LA and genetic distance across phage isolates from different populations, although in contrast to many geographical studies, parasite LA decreased with genetic distance. These results can be explained by the fact that bacteria can rapidly adapt to phage infectivity mutations, but that evolved resistance has a degree of specificity to the local phage population. Our results show that antagonistic co-evolution alone can result in predictable links between genetic distance and host-parasite local adaptation.

Adaptation to abiotic conditions drives local adaptation in bacteria and viruses coevolving in heterogeneous environments.

Parasite local adaptation, the greater performance of parasites on their local compared with foreign hosts, has important consequences for the maintenance of diversity and epidemiology. While the abiotic environment may significantly affect local adaptation, most studies to date have failed either to incorporate the effects of the abiotic environment, or to separate them from those of the biotic environment. Here, we tease apart biotic and abiotic components of local adaptation using the bacterium Pseudomonas fluorescens and its viral parasite bacteriophage Φ2. We coevolved replicate populations of bacteria and phages at three different temperatures, and determined their performance against coevolutionary partners from the same and different temperatures. Crucially, we measured performance at different assay temperatures, which allowed us to disentangle adaptation to biotic and abiotic habitat components. Our results show that bacteria and phages are more resistant and infectious, respectively, at the temperature at which they previously coevolved, confirming that local adaptation to abiotic conditions can play a crucial role in determining parasite infectivity and host resistance. Our work underlines the need to assess host–parasite interactions across multiple relevant abiotic environments, and suggests that microbial adaption to local temperatures can create ecological barriers to dispersal across temperature gradients.

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 fitnessrelated 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. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2016, 118, 344–358.

Bacteria-phage interactions across time and space: merging local adaptation and time-shift experiments to understand phage evolution.

The study of parasite local adaptation to host populations offers important insight into the spatial scale of host-parasite interactions. For parasites adapting to local hosts, the process is continually driven by change in the host population, in response to either the parasite or alternative selection pressures. In the case of reciprocal coevolutionary change, this adaptation should generate a pattern whereby parasites are most fit against hosts from the recent past (which have not yet responded to parasite-mediated selection) and least fit against future host populations (with increased resistance). I argue that combining data on local adaptation across space with data on evolutionary responses over time can offer novel insight into the process of adaptation. Using bacteriophages from horse chestnut trees, I compare infectivity on bacterial hosts isolated from either the same tree or different trees over multiple months of the growing season and find that phage adaptation to local hosts is most pronounced on bacterial hosts from the recent past. These results confirm that phages are well adapted to bacterial populations living within eukaryotes and more broadly suggest that local adaptation studies may underestimate the magnitude of parasite evolution, as host and parasite adaptation are confounded within contemporary time points.

Life-history traits indicate local adaptation of the schistosome parasite, Schistosoma mansoni, to its snail host, Biomphalaria pfeifferi

The digenean trematode Schistosoma mansoni causes schistosomiasis (Bilharziasis), a significant human disease especially in sub-Saharan Africa. We tested local adaptation of this parasite to its intermediate host, the freshwater snail Biomphalaria pfeifferi, by exposure of S. mansoni to B. pfeifferi from one sympatric and four allopatric populations and measurement of life-history traits of both species over time. The pre-patent period, infection rate, and cercarial production of the parasite were determined, and the shell diameter, fecundity, and survival of the snail host were determined. The results provide evidence for local adaptation of S. mansoni to its sympatric snail host: the pre-patent period was the shortest, the cercarial production was moderate and accompanied by a higher survival rate, the growth was greater during the pre-patent period, and the fecundity was greater during the pre-patent period. The greater growth and fecundity of sympatric B. pfeifferi suggests the presence of growth and fecundity compensation. These fitness traits are relevant to energy allocation of the snail host and to the transmission strategy of the schistosome parasite.

Varying herbivore population structure correlates with lack of local adaptation in a geographic variable plant-herbivore interaction.

Local adaptation of parasites to their hosts due to coevolution is a central prediction of many theories in evolutionary biology. However, empirical studies looking for parasite local adaptation show great variation in outcomes, and the reasons for such variation are largely unknown. In a previous study, we showed adaptive differentiation in the arctiid moth Utetheisa ornatrix to its host plant, the pyrrolizidine alkaloid-bearing legume Crotalaria pallida, at the continental scale, but found no differentiation at the regional scale. In the present study, we sampled the same sites to investigate factors that may contribute to the lack of differentiation at the regional scale. We performed field observations that show that specialist and non-specialist polyphagous herbivore incidence varies among populations at both scales. With a series of common-garden experiments we show that some plant traits that may affect herbivory (pyrrolizidine alkaloids and extrafloral nectaries) vary at the regional scale, while other traits (trichomes and nitrogen content) just vary at the continental scale. These results, combined with our previous evidence for plant population differentiation based on larval performance on fresh fruits, suggest that U. ornatrix is subjected to divergent selection even at the regional scale. Finally, with a microsatellite study we investigated population structure of U. ornatrix. We found that population structure is not stable over time: we found population differentiation at the regional scale in the first year of sampling, but not in the second year. Unstable population structure of the herbivore is the most likely cause of the lack of regional adaptation.

On the Equivalence of Host Local Adaptation and Parasite Maladaptation: An Experimental Test

In spatiotemporally varying environments, host-parasite coevolution may lead to either host or parasite local adaptation. Using reciprocal infestations over 11 pairs of plots, we tested local adaptation in the hen flea and its main host, the great tit. Flea reproductive success (number of adults at host fledging) was lower on host individuals from the same plot compared with foreign hosts (from another plot), revealing flea local maladaptation. Host reproductive success (number of fledged young) for nests infested by foreign fleas was lower compared with the reproductive success of controls, with an intermediate success for nests infested by local fleas. This suggests host local adaptation although the absence of local adaptation could not be excluded. However, fledglings were heavier and larger when reared with foreign fleas than when reared with local fleas, which could also indicate host local maladaptation if the fitness gain in offspring size offsets the potential cost in offspring number. Our results therefore challenge the traditional view that parasite local maladaptation is equivalent to host local adaptation. The differences in fledgling morphology between nests infested with local fleas and those with foreign fleas suggest that flea origin affects host resource allocation strategy between nestling growth and defense against parasites. Therefore, determining the mechanisms that underlie these local adaptation patterns requires the identification of the relevant fitness measures and life-history trade-offs in both species.

Meta-analysis and research on host–parasite interactions: past and future

Host–parasite interactions are characterised by a lack of stable species-specific traits that limits generalisations one can make even about particular host or parasite species. For instance, the virulence, life history traits or transmission mode of a given parasite species can depend on which of its suitable hosts it infects. In the search for general rules or patterns, meta-analysis provides a possible solution to the challenges posed by the highly variable outcomes of host–parasite interactions. It allows an estimate of the overall association between any factor and its biological response that transcends the particulars of given host and parasite taxonomic combinations. In this review, we begin with a historical overview of the use of meta-analysis in research on the ecology and evolution of host–parasite interactions. We then identify several key conceptual advances that were made possible only through meta-analytical synthesis. For example, meta-analysis revealed the predominant association between rates of host and parasite gene flow and local adaptation, as well as an unexpected latitudinal gradient in parasite virulence, or parasite-induced host mortality. Finally, we propose some areas of research on host–parasite interactions that are based on a mature theoretical foundation and for which there now exist sufficient primary results to make them ripe for meta-analysis. The search for the processes causing variability in parasite species richness among host species, and the link between the expression of host resistance and the specificity of parasites, are two such research areas. The main objective of this review is to promote meta-analysis as a synthetic tool overriding the idiosyncrasies of specific host–parasite combinations and capable of uncovering the universal trends, if any, in the evolutionary ecology of parasitism.

Abiotic heterogeneity drives parasite local adaptation in coevolving bacteria and phages

Spatial abiotic heterogeneity can result in divergent selection, hence might increase the magnitude of host-parasite local adaptation (the mean difference in fitness of sympatric vs. allopatric host-parasite combinations). We explicitly tested this hypothesis by measuring local adaptation in experimentally coevolved populations of bacteria and viruses evolved in the same or different nutrient media. Consistent with previous work, we found that mean levels of evolved phage infectivity and bacteria resistance varied with nutrient concentration, with maximal levels at nutrient concentrations that supported the greatest densities of bacteria. Despite this variation in evolved mean infectivity and resistance between treatments, we found that parasite local adaptation was greatly increased when measured between populations evolved in different, compared with the same, media. This pattern is likely to have resulted from different media imposing divergent selection on bacterial hosts, and phages in turn adapting to their local hosts. These results demonstrate that the abiotic environment can play a strong and predictable role in driving patterns of local adaptation.

Coevolutionary hotspots and coldspots for host sex and parasite local adaptation in a snail–trematode interaction

Reciprocal adaptation between interacting species may occur in some regions (coevolutionary ‘hotspots’) and not others (‘coldspots’). In a previous study, we found hotspots and coldspots along a continuous depth gradient in two different New Zealand lakes. Specifically, we found that Microphallus sp. trematodes were locally adapted to Potamopyrgus antipodarum snails collected from shallow‐water margins of the lakes, but not to snails collected from deep‐water habitats. As sexual snails were more common in the shallow water, and asexual snails more common in the deep water, the results were also consistent with the Red Queen hypothesis, which predicts that sex should be favored in environments with coevolving parasites. Here, we repeated our earlier experiment to determine whether the results are robust over time (two years) and space (three lakes). We also tested whether our measure of parasite local adaptation was sensitive to parasite dose. Our results suggest that shallow‐water habitats are temporally stable coevolutionary hotspots, and that the pattern is spatially robust over three lake populations. We also found that, while parasite dose affects the magnitude of local adaptation, it does not obscure the signature of local adaptation in this snail–trematode system.