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.     

Identifying hotspots of parasite diversity from species–area relationships: host phylogeny versus host ecology

Interspecific variation in parasite species richness among host species has generated much empirical research. As in comparisons among geographical areas, controlling for variation in host body size is crucial because host size determines resource availability. Recent developments in the use of species–area relationships (SARs) to detect hotspots of biodiversity provide a powerful way to control for host body size, and to identify ‘hot’ and ‘cold hosts’ of parasite diversity, i.e. hosts with more or fewer parasites than expected from their size. Applying SAR modelling to six large datasets on parasite species richness in vertebrates, we search for hot and cold hosts and assess the effect of other ecological variables on the probability that a host species is hot/cold taking body size (and sampling effort) into account. Five non‐sigmoid SAR models were fitted to the data by optimisation; their relative likelihood was evaluated using the Bayesian information criterion, before deriving an averaged SAR function. Overall, the fit between the five SAR models and the actual data was poor; there was substantial uncertainty surrounding the fitted models, and the best model differed among the six datasets. These results show that host body size is not a strong or consistent determinant of parasite species richness across taxa. Hotspots were defined as host species lying above the upper limit of the 80% confidence interval of the averaged SAR, and coldspots as species lying below its lower limit. Our analyses revealed (1) no apparent effect of specific ecological factors (i.e. water temperature, mean depth range, latitude or population density) on the likelihood of a host species being a hot or coldspot; (2) evidence of phylogenetic clustering, i.e. hosts from certain families are more likely to be hotspots (or coldspots) than other species, independently of body size. These findings suggest that host phylogeny may sometimes outweigh specific host ecological traits as a predictor of whether or not a host species harbours more (or fewer) parasite species than expected for its size.     

Sediments,not plants,offer the preferred refuge for Daphnia against fish predation in Mediterranean shallow lakes: an experimental demonstration

1. Different behavioural responses of planktonic animals to their main predators, fish, have been reported from shallow lakes. In north temperate lakes, large‐bodied zooplankton may seek refuge from predation among macrophytes, whereas in subtropical lakes, avoidance of macrophytes has been observed. The prevalent behaviour probably depends on the characteristics of the fish community, which in Mediterranean lakes is typically dispersed in both the open water zone and in the littoral, as in temperate lakes, and is dominated by small size classes, as in subtropical lakes. 2. We performed ‘habitat choice’ experiments to test the response of Daphnia magna to predation cues at both the horizontal and vertical level by mimicking a ‘shallow littoral’ zone with plants and a ‘deeper pelagic’ zone with sediments. 3. Initial separate response experiments showed that natural plants, artificial plants and predation cues all repelled D. magna in the absence of other stimuli, while sediments alone did not trigger any significant response by D. magna. 4. The habitat choice experiments showed that, in the presence of predation cues and absence of plants, Daphnia moved towards areas with sediment. In the presence of both plants and sediments, Daphnia moved away from the plants towards the sediments under both shallow and deep water treatment conditions. 5. Based on these results, we suggest that Daphnia in Mediterranean shallow lakes avoid submerged macrophytes and instead prefer to hide near the sediment when exposed to predation risk, as also observed in subtropical shallow lakes. This pattern is not likely to change with water level alterations, a common feature of lakes in the region, even if the effectiveness of the refuge may be reduced.     

Hydroperiod,predators and the distribution of physid snails across the freshwater habitat gradient

1. Studies of species distributions across environmental gradients further our understanding of mechanisms regulating species diversity at the landscape scale. For some freshwater taxa the habitat gradient from small, shallow and temporary ponds to large, deep and permanent lakes has been shown to be an important environmental axis. Freshwater snails are key players in freshwater ecosystems, but there are no comprehensive studies of their distributions across the entire freshwater habitat gradient. Here we test the hypothesis that snail species in the family Physidae are distributed in a non‐random manner across the habitat gradient. We sampled the snails, their predators and the abiotic environment of 61 ponds and lakes, spanning a wide range in depth and hydroperiod. 2. Temporary habitats had the lowest biomass of predators. Shallow permanent ponds had the highest biomass of invertebrate predators but an intermediate fish biomass. Deep ponds and lakes had the highest fish biomass and intermediate invertebrate biomass. Five species of physids occurred in the regional species pool and 60 of the 61 ponds and lakes surveyed contained physid snails. Each pond and lake contained an average of just 1.2 physid species, illustrating limited membership in local communities and substantial among‐site heterogeneity in species composition. 3. Physids showed strong sorting along the habitat gradient, with Physa vernalis found in the shortest hydroperiod ponds and Aplexa elongata, P. gyrina, P. acuta and P. ancillaria found in habitats of successively greater permanence. When organised into a site‐by‐species incidence matrix with sites ordered according to their hydroperiods, we found the pattern of incidence to be highly coherent, showing that much of the heterogeneity in species composition from one pond to another is explained by hydroperiod. We also found that the number of species replacements along this gradient was higher than random, showing that replacement is more important than nesting in describing species composition in ponds of different hydroperiod. 4. Discriminant analysis showed that pond depth, invertebrate biomass and fish biomass were the best predictors of species composition. Analysis of these niche dimensions showed that P. vernalis and A. elongata were most successful in shallow, temporary ponds with few predators. P. gyrina and P. acuta were typically found in ponds of intermediate depth and high predator abundance. P. ancillaria was found in the deepest lakes, which had abundant fish predators but few invertebrate predators. Of the five species considered, P. ancillaria, P. vernalis and A. elongata were relatively specialised with regard to key habitat characteristics, P. gyrina was moderately generalised and P. acuta was remarkably generalised, since it alone occurred across the entire freshwater habitat gradient. The exceptional habitat breadth of P. acuta stands in contrast to distributional studies of other freshwater taxa and deserves further attention.     

Genetic variation in sexual and clonal lineages of a freshwater snail

Sexual reproduction within natural populations of most plants and animals continues to remain an enigma in evolutionary biology. That the enigma persists is not for lack of testable hypotheses but rather because of the lack of suitable study systems in which sexual and asexual females coexist. Here we review our studies on one such organism, the freshwater snail Potamopyrgus antipodarum (Gray). We also present new data that bear on hypotheses for the maintenance of sex and its relationship to clonal diversity. We have found that sexual populations of the snail are composed of diploid females and males, while clonal populations are composed of a high diversity of triploid apomictic females. Sexual and asexual individuals coexist in stable frequencies in many ‘mixed’ populations; genetic data indicate that clones from these mixed populations originated from the local population of sexual individuals without interspecific hybridization. Field data show that clonal and sexual snails have completely overlapping life histories, but individual clonal genotypes are less variable than individuals from the sympatric sexual population. Field data also show segregation of clones among depth‐specific habitat zones within a lake, but clonal diversity remains high even within habitats. A new laboratory experiment revealed extensive clonal variation in reproductive rate, a result which suggests that clonal diversity would be low in nature without some form of frequency‐dependent selection. New results from a long‐term field study of a natural, asexual population reveal that clonal diversity remained nearly constant over a 10‐year period. Nonetheless, clonal turnover occurs, and it occurs in a manner that is consistent with parasite‐mediated, frequency‐dependent selection. Reciprocal cross‐infection experiments have further shown that parasites are more infective to sympatric host snails than to allopatric snails, and that they are also more infective to common clones than rare clones within asexual host populations. Hence we suggest that sexual reproduction in these snails may be maintained, at least in part, by locally adapted parasites. Parasite‐mediated selection possibly also contributes to the maintenance of local clonal diversity within habitats, while clonal selection may be responsible for the distribution of clones among habitats. © 2003 The Linnean Society of London. Biological Journal of the Linnean Society 2003, 79 , 165–181.     

Local adaptation and maladaptation to pollinators in a generalist geographic mosaic

The Geographic Mosaic Theory of Coevolution predicts the occurrence of mosaics of interaction-mediated local adaptations and maladaptations. Empirical support to this prediction has come mostly from specialist interactions. In contrast, local adaptation is considered highly unlikely in generalist interactions. In this study, we experimentally test local adaptation in a generalist plant-pollinator geographic mosaic, by means of a transplant experiment in which plants coming from two evolutionary hotspots and two coldspots were offered to pollinators at the same four localities. Plants produced in the hotspots attracted more pollinators in all populations, whereas coldspot plants attracted fewer pollinators in all populations. Differences in adaptation were not related to genetic similarity between populations, suggesting that it was mainly due to spatial variation in previous selective regimes. Our experiment provides the first strong support for a spatially structured pattern of adaptation and maladaptation generated by a generalist free-living mutualism.     

THE GEOGRAPHY OF COEVOLUTION: COMPARATIVE POPULATION STRUCTURES FOR A SNAIL AND ITS TREMATODE PARASITE

Gene flow and the genetic structure of host and parasite populations are critical to the coevolutionary process, including the conditions under which antagonistic coevolution favors sexual reproduction. Here we compare the genetic structures of different populations of a freshwater New Zealand snail (Potamopyrgus antipodarum) with its trematode parasite (Microphallus sp.) using allozyme frequency data. Allozyme variation among snail populations was found to be highly structured among lakes; but for the parasite there was little allozyme structure among lake populations, suggesting much higher levels of parasite gene flow. The overall pattern of variation was confirmed with principal component analysis, which also showed that the organization of genetic differentiation for the snail (but not the parasite) was strongly related to the geographic arrangement of lakes. Some snail populations from different sides of the Alps near mountain passes were more similar to each other than to other snail populations on the same side of the Alps. Furthermore, genetic distances among parasite populations were correlated with the genetic distances among host populations, and genetic distances among both host and parasite populations were correlated with “stepping-stone” distances among lakes. Hence, the host snail and its trematode parasite seem to be dispersing to adjacent lakes in a stepping-stone fashion, although parasite dispersal among lakes is clearly greater. High parasite gene flow should help to continuously reintroduce genetic diversity within local populations where strong selection might otherwise isolate “host races.” Parasite gene flow can thereby facilitate the coevolutionary (Red Queen) dynamics that confer an advantage to sexual reproduction by restoring lost genetic variation.     

Evolution of spatially structured host–parasite interactions

Spatial structure has dramatic effects on the demography and the evolution of species. A large variety of theoretical models have attempted to understand how local dispersal may shape the coevolution of interacting species such as host–parasite interactions. The lack of a unifying framework is a serious impediment for anyone willing to understand current theory. Here, we review previous theoretical studies in the light of a single epidemiological model that allows us to explore the effects of both host and parasite migration rates on the evolution and coevolution of various life‐history traits. We discuss the impact of local dispersal on parasite virulence, various host defence strategies and local adaptation. Our analysis shows that evolutionary and coevolutionary outcomes crucially depend on the details of the host–parasite life cycle and on which life‐history trait is involved in the interaction. We also discuss experimental studies that support the effects of spatial structure on the evolution of host–parasite interactions. This review highlights major similarities between some theoretical results, but it also reveals an important gap between evolutionary and coevolutionary models. We discuss possible ways to bridge this gap within a more unified framework that would reconcile spatial epidemiology, evolution and coevolution.     

Migration highways and migration barriers created by host–parasite interactions

Co‐evolving parasites may play a key role in host migration and population structure. Using co‐evolving bacteria and viruses, we test general hypotheses as to how co‐evolving parasites affect the success of passive host migration between habitats that can support different intensities of host–parasite interactions. First, we show that parasites aid migration from areas of intense to weak co‐evolutionary interactions and impede migration in the opposite direction, as a result of intraspecific apparent competition mediated via parasites. Second, when habitats show qualitative difference such that some environments support parasite persistence while others do not, different population regulation forces (either parasitism or competitive exclusion) will reduce the success of migration in both directions. Our study shows that co‐evolution with parasites can predictably homogenises or isolates host populations, depending on heterogeneity of abiotic conditions, with the second scenario constituting a novel type of ‘isolation by adaptation’.     

Faster clonal turnover in high‐infection habitats provides evidence for parasite‐mediated selection

According to the Red Queen hypothesis for sex, parasite‐mediated selection against common clones counterbalances the reproductive advantage of asexual lineages, which would otherwise outcompete sexual conspecifics. Such selection on the clonal population is expected to lead to a faster clonal turnover in habitats where selection by parasites is stronger. We tested this prediction by comparing the genetic structure of clonal and sexual populations of freshwater snail Potamopyrgus antipodarum between years 2003 and 2007 in three depth‐specific habitats in Lake Alexandrina (South Island, New Zealand). These habitats differ in the risk of infection by castrating trematodes and in the relative proportion of sexual individuals. As predicted, we found that the clonal structure changed significantly in shallow and mid‐water habitats, where prevalence of infection was high, but not in the deep habitat, where parasite prevalence was low. Additionally, we found that both clonal diversity and evenness of the asexual population declined in the shallow habitat. In contrast, the genetic structure (based on F–statistics) of the coexisting sexual population did not change, which suggests that the change in the clonal structure cannot be related to genetic changes in the sexual population. Finally, the frequency of sexuals had no effect on the diversity of the sympatric clonal population. Taken together, our results show a more rapid clonal turnover in high‐infection habitats, which gives support for the Red Queen hypothesis for sex.     

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.     

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.     

Local adaptation and the geometry of host–parasite coevolution

Metapopulation dynamics can strongly affect the ecological and evolutionary processes involved in host–parasite interactions. Here, I analyse a deterministic host–parasite coevolutionary model and derive analytic approximations for the level of local adaptation as a function of (1) host migration rate, (2) parasite migration rate, (3) parasite specificity and (4) parasite virulence. This analysis confirms the results of previous simulation studies: the difference between host and parasite migration rates may explain the level of local adaptation of both species. I also show that both higher specificity and higher virulence generally lead to higher levels of local adaptation of the species which is already ahead in the coevolutionary arms race. The present analysis also provides a simple geometric interpretation for local adaptation which captures the complexity of the temporal dynamics of host–parasite coevolution.     

Identifying coevolving loci using interspecific genetic correlations

Evaluating the importance of coevolution for a wide range of evolutionary questions, such as the role parasites play in the evolution of sexual reproduction, requires that we understand the genetic basis of coevolutionary interactions. Despite its importance, little progress has been made identifying the genetic basis of coevolution, largely because we lack tools designed specifically for this purpose. Instead, coevolutionary studies are often forced to re‐purpose single species techniques. Here, we propose a novel approach for identifying the genes mediating locally adapted coevolutionary interactions that relies on spatial correlations between genetic marker frequencies in the interacting species. Using individual‐based multi‐locus simulations, we quantify the performance of our approach across a range of coevolutionary genetic models. Our results show that when one species is strongly locally adapted to the other and a sufficient number of populations can be sampled, our approach accurately identifies functionally coupled host and parasite genes. Although not a panacea, the approach we outline here could help to focus the search for coevolving genes in a wide variety of well‐studied systems for which substantial local adaptation has been demonstrated.     

Experimental evolution of local parasite maladaptation

Sign and magnitude of local adaptation in host–parasite systems may vary with ecological, epidemiological or genetic parameters. To investigate the role of host genetic background, we established long‐term experimental populations of different genotypes of the protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. We observed the evolution of an overall pattern of parasite local maladaptation for infectivity, indicating a general coevolutionary disadvantage of this parasite. Maladaptation extended to host populations with the same genetic background, similar to extending from the local to a higher regional level in natural populations. Patterns for virulence were qualitatively similar, but with less statistical support. A nonsignificant correlation with levels of (mal)adaptation for infectivity suggests independent evolution of these traits. Our results indicate similar (co)evolutionary trajectories in populations with different genetic backgrounds. Nonetheless, the correlated clines of genetic distance and parasite performance illustrate how genetic background can shape spatial gradients of local adaptation.     

Some like it deep: Intraspecific niche segregation in ruffe (Gymnocephalus cernua)

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Should ‘wetlands’ cover all aquatic ecosystems and do macrophytes make a difference to their ecosystem services?

The Ramsar Convention has gradually expanded the scope of the term ‘wetland’ to bring under its umbrella all kinds of inland freshwater (and saline) ecosystems as well as many marine ecosystems. It is not possible to develop a common framework for the study, management or policy of such a large and divergent assemblage of habitats with water being a single shared feature. In this paper, I argue that wetlands are distinct from deep open water systems such as rivers, lakes and reservoirs. The restriction of macrophytes (except the free floating plants like salvinia and water hyacinth) to shallow water habitats helps distinguish between wetlands and deep water systems. Following an ecosystem service approach, I discuss that wetlands are generally characterized by the occurrence of macrophytes, which critically contribute to their provisioning, regulating, supporting and cultural ecosystem services that differ significantly from those of the microphyte (phytoplankton)-dominated deep water habitats. I argue that wetlands do lie adjacent to deep and open water systems (including large rivers), which interact with them regularly and influence their biodiversity, hydrology, water quality and functioning, depending upon their relative areal extent and characteristics of the macrophyte community, but that only the littoral zones between the mean highest and lowest water levels (and stream banks and the floodplains beyond them in the case of rivers) should be treated as wetlands. Shallow lakes devoid of macrophytes because of eutrophication are degraded wetlands that need to be restored.     

Effect of spatial connectivity on host resistance in a highly fragmented natural pathosystem

Both theory and experimental evolution studies predict migration to influence the outcome of antagonistic coevolution between hosts and their parasites, with higher migration rates leading to increased diversity and evolutionary potential. Migration rates are expected to vary in spatially structured natural pathosystems, yet how spatial structure generates variation in coevolutionary trajectories across populations occupying the same landscape has not been tested. Here, we studied the effect of spatial connectivity on host evolutionary potential in a natural pathosystem characterized by a stable Plantago lanceolata host network and a highly dynamic Podosphaera plantaginis parasite metapopulation. We designed a large inoculation experiment to test resistance of five isolated and five well‐connected host populations against sympatric and allopatric pathogen strains, over 4 years. Contrary to our expectations, we did not find consistently higher resistance against sympatric pathogen strains in the well‐connected populations. Instead, host local adaptation varied considerably among populations and through time with greater fluctuations observed in the well‐connected populations. Jointly, our results suggest that in populations where pathogens have successfully established, they have the upper hand in the coevolutionary arms race, but hosts may be better able to respond to pathogen‐imposed selection in the well‐connected than in the isolated populations. Hence, the ongoing and extensive fragmentation of natural habitats may increase vulnerability to diseases.     

Developmental effects of visual environment on species‐assortative mating preferences in Lake Victoria cichlid fish

Local adaptation can be a potent force in speciation, with environmental heterogeneity leading to niche specialization and population divergence. However, local adaption often requires nonrandom mating to generate reproductive isolation. Population divergence in sensory properties can be particularly consequential in speciation, affecting both ecological adaptation and sexual communication. Pundamilia pundamila and Pundamilia nyererei are two closely related African cichlid species that differ in male coloration, blue vs. red. They co‐occur at rocky islands in southern Lake Victoria, but inhabit different depth ranges with different light environments. The species differ in colour vision properties, and females exert species‐specific preferences for blue vs. red males. Here, we investigated the mechanistic link between colour vision and preference, which could provide a rapid route to reproductive isolation. We tested the behavioural components of this link by experimentally manipulating colour perception – we raised both species and their hybrids under light conditions mimicking shallow and deep habitats – and tested female preference for blue and red males under both conditions. We found that rearing light significantly affected female preference: shallow‐reared females responded more strongly to P. pundamilia males and deep‐reared females favoured P. nyererei males – implying that visual development causally affects mate choice. These results are consistent with sensory drive predictions, suggesting that the visual environment is key to behavioural isolation of these species. However, the observed plasticity could also make the species barrier vulnerable to environmental change: species‐assortative preferences were weaker in females that were reared in the other species’ light condition.     

Evaluating the role of regional and local processes in structuring a larval trematode metacommunity of Helisoma trivolvis

Metacommunity theory has advanced our understanding of how local and regional processes affect the structure of ecological communities. While parasites have largely been omitted from metacommunity research, parasite communities can provide the large sample sizes and discrete boundaries often required for evaluating metacommunity patterns. Here, we used assemblages of flatworm parasites that infect freshwater snails (Helisoma trivolvis) to evaluate three questions: 1) what factors affect individual host infections within ponds? 2) Is the parasite metacommunity structured among ponds? And 3) what is the relative role of local versus regional processes in determining metacommunity structure and species richness among ponds? We examined 10 821 snails from 96 sites in five park complexes in the San Francisco Bay area, California, and found 953 infections from six parasite groups. At the within‐pond level, infection status of host snails correlated positively with individual snail size and pond infection prevalence for all six parasite groups. Using an ordination method to test for metacommunity structure, we found that the parasite metacommunity was organized in a non‐random pattern with species responding individually along an environmental gradient. Based on a model selection approach involving local and regional predictors, parasite species richness and metacommunity structure correlated with both local abiotic (pH and total dissolved nitrogen) and biotic (non‐host mollusk density, and H. trivolvis biomass) factors, with little support for regional predictors. Overall, this trematode metacommunity most closely followed the predictions from the species sorting or mass effects metacommunity paradigm, in which community diversity is filtered by local site characteristics.