Co‐evolutionary patterns in congeneric monogeneans: a review of Dactylogyrus species and their cyprinid hosts

Patterns associated with the evolution of parasite diversity, speciation and diversification were analysed using Dactylogyrus species (gill monogeneans) and their cyprinid hosts as a model. The aim of this study was to use this highly specific host–parasite systems to review: (1) the diversity and distribution of Dactylogyrus species, (2) the patterns of organization and structure of Dactylogyrus communities, (3) the evolution and determinants of host specificity and (4) the mode of Dactylogyrus speciation and co‐evolutionary patterns in this Dactylogyrus–cyprinid systems. Dactylogyrus are a highly diverse group of parasites, with their biogeography and distribution clearly linked to the evolutionary history of their cyprinid hosts. The coexistence of several Dactylogyrus species on one host is facilitated by increasing niche distances and the differing morphology of their reproductive organs. The positive interspecific and intraspecific interactions seem to be the most important factors determining the structure of Dactylogyrus communities. Host specificity is partially constrained by parasite phylogeny. Being a strict specialist is an ancestral character for Dactylogyrus, being the intermediate specialists or generalists are the derived characters. The evolution of attachment organ morphology is associated with both parasite phylogeny and host specificity. Considering larger and long‐lived hosts or hosts with several ecological characters as the measures of resource predictability, specialists with larger anchors occurred on larger or longer‐living fish species. Intra‐host speciation, a mode of speciation not often recorded in parasites, was observed in Dactylogyrus infecting sympatric cyprinids. Sister parasite species coexisting on the same host occupied niches that differed in at least one niche variable. Intra‐host speciation, however, was not observed in Dactylogyrus species of congeneric hosts from geographically isolated areas, which suggested association by descent and host‐switching events.     

Gene expression remodelling and immune response during adaptive divergence in an African cichlid fish

Variation in gene expression contributes to ecological speciation by facilitating population persistence in novel environments. Likewise, immune responses can be of relevance in speciation driven by adaptation to different environments. Previous studies examining gene expression differences between recently diverged ecotypes have often relied on only one pair of populations, targeted the expression of only a subset of genes or used wild‐caught individuals. Here, we investigated the contribution of habitat‐specific parasites and symbionts and the underlying immunological abilities of ecotype hosts to adaptive divergence in lake–river population pairs of the cichlid fish Astatotilapia burtoni. To shed light on the role of phenotypic plasticity in adaptive divergence, we compared parasite and microbiota communities, immune response, and gene expression patterns of fish from natural habitats and a lake‐like pond set‐up. In all investigated population pairs, lake fish were more heavily parasitized than river fish, in terms of both parasite taxon composition and infection abundance. The innate immune response in the wild was higher in lake than in river populations and was elevated in a river population exposed to lake parasites in the pond set‐up. Environmental differences between lake and river habitat and their distinct parasite communities have shaped differential gene expression, involving genes functioning in osmoregulation and immune response. Most changes in gene expression between lake and river samples in the wild and in the pond set‐up were based on a plastic response. Finally, gene expression and bacterial communities of wild‐caught individuals and individuals acclimatized to lake‐like pond conditions showed shifts underlying adaptive phenotypic plasticity.     

Environmental parasitology: stressor effects on aquatic parasites

Anthropogenic stressors are causing fundamental changes in aquatic habitats and to the organisms inhabiting these ecosystems. Yet, we are still far from understanding the diverse responses of parasites and their hosts to these environmental stressors and predicting how these stressors will affect host–parasite communities. Here, we provide an overview of the impacts of major stressors affecting aquatic ecosystems in the Anthropocene (habitat alteration, global warming, and pollution) and highlight their consequences for aquatic parasites at multiple levels of organisation, from the individual to the community level. We provide directions and ideas for future research to better understand responses to stressors in aquatic host–parasite systems.     

The association of feeding behaviour with the resistance and tolerance to parasites in recently diverged sticklebacks

Divergent natural selection regimes can contribute to adaptive population divergence, but can be sensitive to human‐mediated environmental change. Nutrient loading of aquatic ecosystems, for example, might modify selection pressures by altering the abundance and distribution of resources and the prevalence and infectivity of parasites. Here, we used a mesocosm experiment to test for interactive effects of nutrient loading and parasitism on host condition and feeding ecology. Specifically, we investigated whether the common fish parasite Gyrodactylus sp. differentially affected recently diverged lake and stream ecotypes of three‐spined stickleback (Gasterosteus aculeatus). We found that the stream ecotype had a higher resistance to Gyrodactylus sp. infections than the lake ecotype, and that both ecotypes experienced a cost of parasitism, indicated by negative relationships between parasite load and both stomach fullness and body condition. Overall, our results suggest that in the early stages of adaptive population divergence of hosts, parasites can affect host resistance, body condition and diet.     

Parasitism and the evolutionary ecology of animal personality

The ecological factors responsible for the evolution of individual differences in animal personality (consistent individual differences in the same behaviour across time and contexts) are currently the subject of intense debate. A limited number of ecological factors have been investigated to date, with most attention focusing on the roles of resource competition and predation. We suggest here that parasitism may play a potentially important, but largely overlooked, role in the evolution of animal personalities. We identify two major routes by which parasites might influence the evolution of animal personality. First, because the risk of acquiring parasites can be influenced by an individual's behavioural type, local parasite regimes may impose selection on personality traits and behavioural syndromes (correlations between personality traits). Second, because parasite infections have consequences for aspects of host 'state', parasites might induce the evolution of individual differences in certain types of host behaviour in populations with endemic infections. Also, because infection often leads to specific changes in axes of personality, parasite infections have the potential to decouple behavioural syndromes. Host-parasite systems therefore provide researchers with valuable tools to study personality variation and behavioural syndromes from a proximate and ultimate perspective.     

Sexual signalling in female crested macaques and the evolution of primate fertility signals

Background

Host-parasite coevolution can lead to local adaptation of either parasite or host if there is specificity (GxG interactions) and asymmetric evolutionary potential between host and parasite. This has been demonstrated both experimentally and in field studies, but a substantial proportion of studies fail to detect such clear-cut patterns. One explanation for this is that adaptation can be masked by counter-adaptation by the antagonist. Additionally, genetic architecture underlying the interaction is often highly complex thus preventing specific adaptive responses. Here, we have employed a reciprocal cross-infection experiment to unravel the adaptive responses of two components of fitness affecting both parties with different complexities of the underlying genetic architecture (i.e. mortality and spore load). Furthermore, our experimental coevolution of hosts (Tribolium castaneum) and parasites (Nosema whitei) included paired replicates of naive hosts from identical genetic backgrounds to allow separation between host- and parasite-specific responses.

Results

In hosts, coevolution led to higher resistance and altered resistance profiles compared to paired control lines. Host genotype × parasite genotype interactions (G_H × G_P) were observed for spore load (the trait of lower genetic complexity), but not for mortality. Overall parasite performance correlated with resistance of its matching host coevolution background reflecting a directional and unspecific response to strength of selection during coevolution. Despite high selective pressures exerted by the obligatory killing parasite, and host- and parasite-specific mortality profiles, no general pattern of local adaptation was observed, but one case of parasite maladaptation was consistently observed on both coevolved and control host populations. In addition, the use of replicate control host populations in the assay revealed one case of host maladaptation and one case of parasite adaptation that was masked by host counter-adaptation, suggesting the presence of complex and probably dynamically changing fitness landscapes.

Conclusions

Our results demonstrate that the use of replicate naive populations can be a useful tool to differentiate between host and parasite adaptation in complex and dynamic fitness landscapes. The absence of clear local adaptation patterns during coevolution with a sexual host showing a complex genetic architecture for resistance suggests that directional selection for generality may be more important attributes of host-parasite coevolution than commonly assumed.     

Phylogenetic signals in host–parasite associations for Neotropical bats and Nearctic desert rodents

Hosts and their parasites have strong ecological and evolutionary relationships, with hosts representing habitats and resources for parasites. In the present study, we use approaches developed to evaluate the statistical dependence of species trait values on phylogenetic relationships to determine whether host–parasite relationships (i.e. parasite infections) are contingent on host phylogeny. If host–parasite relationships are contingent on the ability of hosts to provide habitat or resources to parasites, and if host phylogeny is an effective surrogate for among‐host variation in habitat and resource quality, host–parasite relationships should evince phylogenetic signals (i.e. be contingent on host phylogeny). Because the strength of ecological relationships between parasites and their hosts may affect the likelihood of phylogenetic signals occurring in host–parasite relationships, we hypothesized that (1) host specificity would be positively correlated with the strength of phylogenetic signals and (2) the strength of phylogenetic signals will be greater for parasites that rely more on their host throughout their life cycle. Analyses were conducted for ectoparasites from tropical bats and for ectoparasites, helminths, and coccidians from desert rodents. Phylogenetic signals were evaluated for parasite presence and for parasite prevalence. The frequency of phylogenetic signal occurrence was similar for parasite presence and prevalence, with a signal detected in 24–27% of cases at the species level and in 67% and 15% of cases at the genus level for parasites of bats and rodents, respectively. No differences in signal strength or the likelihood of detecting a signal existed between groups of parasites. Phylogenetic signal strength was correlated with host specificity, suggesting that mechanisms increasing host specificity also increase the likelihood of a phylogenetic signal in host use by parasites. Differences in the transmission mode did not affect signal strength or the likelihood of detecting a signal, indicating that variation in host switching opportunities associated with the transmission mode does not affect signal strength.     

Ecological determinants of parasite acquisition by exotic fish species

Disease‐mediated threats posed by exotic species to native counterparts are not limited to introduced parasites alone, since exotic hosts frequently acquire native parasites with possible consequences for infection patterns in native hosts. Several biological and geographical factors are thought to explain both the richness of parasites in native hosts, and the invasion success of free‐living exotic species. However, the determinants of native parasite acquisition by exotic hosts remain unknown. Here, we investigated native parasite communities of exotic freshwater fish to determine which traits influence acquisition of native parasites by exotic hosts. Model selection suggested that five factors (total body length, time since introduction, phylogenetic relatedness to the native fish fauna, trophic level and native fish species richness) may be linked to native parasite acquisition by exotic fish, but 95% confidence intervals of coefficient estimates indicated these explained little of the variance in parasite richness. Based on R²‐values, weak positive relationships may exist only between the number of parasites acquired and either host size or time since introduction. Whilst our results suggest that factors influencing parasite richness in native host communities may be less important for exotic species, it seems that analyses of general ecological factors currently fail to adequately incorporate the physiological and immunological complexity of whether a given animal species will become a host for a new parasite.     

The relationship between biodiversity and ecosystem functioning in food webs

Recent theoretical and experimental work provides clear evidence that biodiversity loss can have profound impacts on functioning of natural and managed ecosystems and the ability of ecosystems to deliver ecological services to human societies. Work on simplified ecosystems in which the diversity of a single trophic level is manipulated shows that diversity can enhance ecosystem processes such as primary productivity and nutrient retention. Theory also strongly suggests that biodiversity can act as biological insurance against potential disruptions caused by environmental changes. However, these studies generally concern a single trophic level, primary producers for the most part. Changes in biodiversity also affect ecosystem functioning through trophic interactions. Here we review, through the analysis of a simple ecosystem model, several key aspects inherent in multitrophic systems that may strongly affect the relationship between diversity and ecosystem processes. Our analysis shows that trophic interactions have a strong impact on the relationships between diversity and ecosystem functioning, whether the ecosystem property considered is total biomass or temporal variability of biomass at the various trophic levels. In both cases, food-web structure and trade-offs that affect interaction strength have major effects on these relationships. Multitrophic interactions are expected to make biodiversity–ecosystem functioning relationships more complex and non-linear, in contrast to the monotonic changes predicted for simplified systems with a single trophic level.     

Genotype-Specific vs. Cross-Reactive Host Immunity against a Macroparasite

Vertebrate hosts often defend themselves against several co-infecting parasite genotypes simultaneously. This has important implications for the ecological dynamics and the evolution of host defence systems and parasite strategies. For example, it can drive the specificity of the adaptive immune system towards high genotype-specificity or cross-reactivity against several parasite genotypes depending on the sequence and probability of re-infections. However, to date, there is very little evidence on these interactions outside mammalian disease literature. In this study we asked whether genotype-specific or cross-reactive responses dominate in the adaptive immune system of a fish host towards a common macroparasite. In other words, we investigated if the infection success of a parasite genotype is influenced by the immunization genotype. We reciprocally immunized and re-exposed rainbow trout (Oncorhynchus mykiss) to a range of genotypes of the trematode eye fluke Diplostomum pseudospathaceum, and measured infection success of the parasite. We found that the infection success of the parasite genotypes in the re-exposure did not depend on the immunization genotype. While immunization reduced average infection success by 31%, the reduction was not larger against the initial immunization genotype. Our results suggest significant cross-reactivity, which may be advantageous for the host in genetically diverse re-exposures and have significant evolutionary implications for parasite strategies. Overall, our study is among the first to demonstrate cross-reactivity of adaptive immunity against genetically diverse macroparasites with complex life cycles.     

Aphids indirectly increase virulence and transmission potential of a monarch butterfly parasite by reducing defensive chemistry of a shared food plant

Parasites and hosts live in communities consisting of many interacting species, but few studies have examined how communities affect parasite virulence and transmission. We studied a food web consisting of two species of milkweed, two milkweed herbivores (monarch butterfly and oleander aphid) and a monarch butterfly-specific parasite. We found that the presence of aphids increased the virulence and transmission potential of the monarch butterfly's parasite on one milkweed species. These increases were associated with aphid-induced decreases in the defensive chemicals of milkweed plants. Our experiment suggests that aphids can indirectly increase the virulence and transmission potential of monarch butterfly parasites, probably by altering the chemical composition of a shared food plant. These results indicate that species that are far removed from host-parasite interactions can alter such interactions through cascading indirect effects in the food web. As such, indirect effects within ecological communities may drive the dynamics and evolution of parasites.     

Human impacts decouple a fundamental ecological relationship—The positive association between host diversity and parasite diversity

Human impacts on ecosystems can decouple the fundamental ecological relationships that create patterns of diversity in free‐living species. Despite the abundance, ubiquity, and ecological importance of parasites, it is unknown whether the same decoupling effects occur for parasitic species. We investigated the influence of fishing on the relationship between host diversity and parasite diversity for parasites of coral reef fishes on three fished and three unfished islands in the central equatorial Pacific. Fishing was associated with a shallowing of the positive host‐diversity–parasite‐diversity relationship. This occurred primarily through negative impacts of fishing on the presence of complex life‐cycle parasites, which created a biologically impoverished parasite fauna of directly transmitted parasites resilient to changes in host biodiversity. Parasite diversity appears to be decoupled from host diversity by fishing impacts in this coral reef ecosystem, which suggests that such decoupling might also occur for parasites in other ecosystems affected by environmental change.     

Natural insect host-parasite systems show immune priming and specificity: puzzles to be solved

Study of the multiplicity of interactions between invertebrate hosts and their parasites helps to define the aspects of the host immune systems that have ecological and evolutionary significance. Such study, however, reveals how much is yet unknown. For instance, the costs of mounting an immune response, the nature of the long-lasting protection sometimes attained, and the high degree of specificity observed in certain hosts are phenomena that still await full explanation. An additional puzzle is the high degree of specificity achieved in light of the apparent low degree of specificity in the recognition and effector mechanisms of insect immune systems. Furthermore, while protective immunity is typically associated with vertebrate adaptive immune systems, invertebrates may have analogous capacities, whose nature is still largely unknown. This review will illustrate how the traditional host-centred view of immune defence can be usefully extended by taking account of parasite immune evasion strategies and the variation that such strategies create in the observed outcomes of infection.     

Chance or choice? Understanding parasite selection and infection in multi-host communities

Ongoing debate over the relationship between biodiversity and disease risk underscores the need to develop a more mechanistic understanding of how changes in host community composition influence parasite transmission, particularly in complex communities with multiple hosts. A key challenge involves determining how motile parasites select among potential hosts and the degree to which this process shifts with community composition. Focusing on interactions between larval amphibians and the pathogenic trematode Ribeiroia ondatrae, we designed a novel, large-volume set of choice chambers to assess how the selectivity of free-swimming infectious parasites varied among five host species and in response to changes in assemblage composition (four different permutations). In a second set of trials, cercariae were allowed to contact and infect hosts, allowing comparison of host-parasite encounter rates (parasite choice) with infection outcomes (successful infections). Cercariae exhibited consistent preferences for specific host species that were independent of the community context; large-bodied amphibians, such as larval bullfrogs (Rana catesbeiana), exhibited the highest level of parasite attraction. However, because host attractiveness was decoupled from susceptibility to infection, assemblage composition sharply affected both per-host infection as well as total infection (summed among co-occurring hosts). Species such as the non-native R. catesbeiana functioned as epidemiological ‘sinks’ or dilution hosts, attracting a disproportionate fraction of parasites relative to the number that established successfully, whereas Taricha granulosa and especially Pseudacris regilla supported comparatively more metacercariae relative to cercariae selection. These findings provide a framework for integrating information on parasite preference in combination with more traditional factors such as host competence and density to forecast how changes within complex communities will affect parasite transmission.     

Biodiversity and land use change on the Causse Méjan, France

This paper argues that due to the co-evolution of biological and cultural diversity, a meaningful study of biodiversity must be positioned within complex social-ecological systems. A complex systems framework is proposed for conceptualising the study of social-ecological systems. A case study approach is adopted whereby changes in biodiversity on the Causse Méjan, France, are linked with changes in society, land use, agricultural practices and policies. We argue that ecological and social resilience is linked through the dependence on ecosystems of communities, and in turn by the influence of institutional structures, including market forces, on the use of natural resources. Within a non-equilibrium evolutionary perspective, we highlight the difficulty of choosing a landscape and biodiversity of reference and postulating that it is in equilibrium with a type of social organisation. We conclude by exploring an ‘adaptive management’ approach to the management of the biodiverse landscape studied.     

Investigating patterns may reveal processes: evolutionary ecology of ectoparasitic monogeneans.

We reviewed several published and ongoing studies concerning monogenean communities. Patterns of species richness, host specificity, community structure and host--parasite coevolutionary interaction were carefully analysed, and hypotheses of evolutionary processes are proposed. The structuring of monogenean communities seems to be related to both ecological and historical constraints. The database supports an absence of intra- and interspecific competition in monogeneans. Species richness seems to be more due to host characteristics than to parasite interactions. Monogeneans seem to specialise on large hosts, leading to greater species richness on those hosts. The morphometric evolution of attachment and copulatory organs support the hypothesis of a reproductive segregation among conspecifics parasitising the same host(s). It also suggests the existence of concurrent adaptive and non-adaptive processes. The general absence of a coevolutionary pattern between host and parasites also suggests the constraints of history without dismissing the influences of ecological factors in the structuring of the communities. More generally, we strengthen the need to study the structure of communities in a phylogenetic context.     

How parasite interaction strategies alter virulence evolution in multi‐parasite communities

The majority of organisms host multiple parasite species, each of which can interact with hosts and competitors through a diverse range of direct and indirect mechanisms. These within‐host interactions can directly alter the mortality rate of coinfected hosts and alter the evolution of virulence (parasite‐induced host mortality). Yet we still know little about how within‐host interactions affect the evolution of parasite virulence in multi‐parasite communities. Here, we modeled the virulence evolution of two coinfecting parasites in a host population in which parasites interacted through cross immunity, immune suppression, immunopathology, or spite. We show (1) that these within‐host interactions have different effects on virulence evolution when all parasites interact with each other in the same way versus when coinfecting parasites have unique interaction strategies, (2) that these interactions cause the evolution of lower virulence in some hosts, and higher virulence in other hosts, depending on the hosts infection status, and (3) that for cross immunity and spite, whether parasites increase or decrease the evolutionarily stable virulence in coinfected hosts depended on interaction strength. These results improve our understanding of virulence evolution in complex parasite communities, and show that virulence evolution must be understood at the community scale.     

Temperature and multiple parasites combine to alter host community structure

Predicting the effects of climate change requires understanding complex interactions among multiple abiotic and biotic factors. By influencing key interactions among host species, parasites can affect community and ecosystem structuring. Yet, our understanding of how multiple parasites and abiotic factors interact to alter ecosystem structure remains limited. To empirically test the role of temperature variation and parasites in shaping communities, we used a multigenerational mesocosm experiment composed of four sympatric freshwater crustacean species (isopods and amphipods) that share up to four parasite species. Mesocosms were assigned to one of four different treatments with contrasting seasonal temperatures (normal and elevated) and parasite exposure levels (continuous and arrested (presence or absence of parasite larvae in mesocosm)). We found that parasite exposure and water temperature had interactive effects on the host community. Continuous exposure to parasites altered the community structure and differences in water temperature altered species abundance. The abundance of the amphipod Paracalliope fluviatilis decreased substantially when experiencing continuous parasite exposure and elevated water temperatures. Elevated temperatures also led to parasite-induced mortality in another amphipod host, Paracorophium excavatum. Contrastingly, isopod hosts were affected much less, suggesting increasing temperatures in conjunction with higher parasite exposure might increase their relative abundance in the community. Changes in invertebrate host populations have implications for other species such as fish and birds that consume crustaceans as well as having impacts on ecosystem processes, such as aquatic primary production and nutrient cycling. In light of climate change predictions, parasite exposure and rise in average temperatures may have substantial impacts on communities and ecosystems, altering ecosystem structure and dynamics.     

Host traits associated with species roles in parasite sharing networks

The community of host species that a parasite infects is often explained by functional traits and phylogeny, predicting that closely related hosts or those with particular traits share more parasites with other hosts. Previous research has examined parasite community similarity by regressing pairwise parasite community dissimilarity between two host species against host phylogenetic distance. However, pairwise approaches cannot target specific host species responsible for disproportionate levels of parasite sharing. To better identify why some host species contribute differentially to parasite diversity patterns, we represent parasite sharing using ecological networks consisting of host species connected by instances of shared parasitism. These networks can help identify host species and traits associated with high levels of parasite sharing that may subsequently identify important hosts for parasite maintenance and transmission within communities. We used global‐scale parasite sharing networks of ungulates, carnivores, and primates to determine if host importance – encapsulated by the network measures degree, closeness, betweenness, and eigenvector centrality – was predictable based on host traits. Our findings suggest that host centrality in parasite sharing networks is a function of host population density and range size, with range size reflecting both species geographic range and the home range of those species. In the full network, host taxonomic family became an important predictor of centrality, suggesting a role for evolutionary relationships between host and parasite species. More broadly, these findings show that trait data predict key properties of ecological networks, thus highlighting a role for species traits in understanding network assembly, stability, and structure.