Genomic evidence for population‐specific responses to co‐evolving parasites in a New Zealand freshwater snail

Reciprocal co‐evolving interactions between hosts and parasites are a primary source of strong selection that can promote rapid and often population‐ or genotype‐specific evolutionary change. These host–parasite interactions are also a major source of disease. Despite their importance, very little is known about the genomic basis of co‐evolving host–parasite interactions in natural populations, especially in animals. Here, we use gene expression and sequence evolution approaches to take critical steps towards characterizing the genomic basis of interactions between the freshwater snail Potamopyrgus antipodarum and its co‐evolving sterilizing trematode parasite, Microphallus sp., a textbook example of natural coevolution. We found that Microphallus‐infected P. antipodarum exhibit systematic downregulation of genes relative to uninfected P. antipodarum. The specific genes involved in parasite response differ markedly across lakes, consistent with a scenario where population‐level co‐evolution is leading to population‐specific host–parasite interactions and evolutionary trajectories. We also used an F_ST‐based approach to identify a set of loci that represent promising candidates for targets of parasite‐mediated selection across lakes as well as within each lake population. These results constitute the first genomic evidence for population‐specific responses to co‐evolving infection in the P. antipodarum‐Microphallus interaction and provide new insights into the genomic basis of co‐evolutionary interactions in nature.     

Comparative morphology of Van der Vecht's organ in Polistes social parasites: host ecology and adaptation of the parasite

Camouflage strategies are common in insect social parasites. Being accepted into an alien colony as a dominant nestmate favours behavioural and morphological adaptations to mimic a specific odour. In Polistes social parasites, abdominal tegumental glands are involved in this camouflage strategy. These glands secreting cuticular hydrocarbons are connected with a modified cuticular area of the last gastral sternite of female wasps, named Van der Vecht's organ, whose secretion is involved in rank and dominance recognition. The size of this exocrine area has been demonstrated to be under selective pressure in Polistes, as a response to an efficient dominance recognition. Because chemical and behavioural integration differs between parasitic species, we carried out a comparison of Van der Vecht's organ size between the three Polistes social parasites and their respective hosts. The parasites Polistes sulcifer and Polistes semenowi, capable of a rapid chemical mimicry and specialized to exploit a lowland host, also show an enlarged Van der Vecht's organ. Conversely, the parasite Polistes atrimandibularis, specialized on a mountain species and showing a slow chemical integration, has a smaller organ. The time available for the parasite to tune up its chemical mimicry, before the emergence of workers to be accepted as a dominant nestmate, appears to be the most important selective pressure acting on the size of this abdominal organ. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013 , 109 , 313–319.     

Conflicts over host manipulation between different parasites and pathogens: Investigating the ecological and medical consequences

When parasites have different interests in regard to how their host should behave this can result in a conflict over host manipulation, i.e. parasite induced changes in host behaviour that enhance parasite fitness. Such a conflict can result in the alteration, or even complete suppression, of one parasite's host manipulation. Many parasites, and probably also symbionts and commensals, have the ability to manipulate the behaviour of their host. Non‐manipulating parasites should also have an interest in host behaviour. Given the frequency of multiple parasite infections in nature, potential conflicts of interest over host behaviour and manipulation may be common. This review summarizes the evidence on how parasites can alter other parasite's host manipulation. Host manipulation can have important ecological and medical consequences. I speculate on how a conflict over host manipulation could alter these consequences and potentially offer a new avenue of research to ameliorate harmful consequences of host manipulation.     

The relationship between species replacement,dissimilarity derived from nestedness,and nestedness

Aim Beta diversity can be partitioned into two components: dissimilarity due to species replacement and dissimilarity due to nestedness ( Baselga, 2010 , Global Ecology and Biogeography, 19 , 134–143). Several contributions have challenged this approach or proposed alternative frameworks. Here, I review the concepts and methods used in these recent contributions, with the aim of clarifying: (1) the rationale behind the partitioning of beta diversity into species replacement and nestedness‐resultant dissimilarity, (2) how, based on this rationale, numerators and denominators of indices have to match, and (3) how nestedness and nestedness‐resultant dissimilarity are related but different concepts. Innovation The rationale behind measures of species replacement (turnover) dictates that the number of species that are replaced between sites (numerator of the index) has to be relativized with respect to the total number of species that could potentially be replaced (denominator). However, a recently proposed partition of Jaccard dissimilarity fails to do this. In consequence, this partition underestimates the contribution of species replacement and overestimates the contribution of richness differences to total dissimilarity. I show how Jaccard dissimilarity can be partitioned into meaningful turnover and nestedness components, and extend these new indices to multiple‐site situations. Finally the concepts of nestedness and nestedness‐resultant dissimilarity are discussed. Main conclusions Nestedness should be assessed using consistent measures that depend both on paired overlap and matrix filling, e.g. NODF, whereas beta‐diversity patterns should be examined using measures that allow the total dissimilarity to be separated into the components of dissimilarity due to species replacement and dissimilarity due to nestedness. In the case of multiple‐site dissimilarity patterns, averaged pairwise indices should never be used because the mean of the pairwise values is unable to accurately reflect the multiple‐site attributes of dissimilarity.     

The changing ecology of tropical forests

The threat to tropical forests is often gauged in terms of deforestation rates and the total area remaining. Recently, however, there has been a growing realization that forest can appear intact on a satellite image yet be biologically degraded or vulnerable to degradation. The array of direct threats to humid tropical forest biodiversity, in addition to deforestation, includes: selective extraction of plants; selective extraction of animals; biological invasion; fragmentation; climate change; changing atmospheric composition; and increasing tree turnover rates. The threats are linked to one another by a poorly understood network of causality and feedback effects. Moreover, their potential impacts on forest biodiversity are hard to assess because each threat is as likely to precipitate indirect effects as direct effects, and because several threats are likely to interact synergistically with one another. In spite of the uncertainties, it is clear that the biological health of tropical forests can become seriously degraded as a result of these threats, and it is unlikely that any tropical forest will escape significant ecological changes. Some groups of plants and animals are likely to benefit at the expense of others. Species diversity is expected to decline as a consequence of the changes in forest ecology. In the 21st century scientists and conservationists will be increasingly challenged to monitor, understand, prevent and head off these threats.     

Pollinator parasites and the evolution of floral traits

The main selective force driving floral evolution and diversity is plant–pollinator interactions. Pollinators use floral signals and indirect cues to assess flower reward, and the ensuing flower choice has major implications for plant fitness. While many pollinator behaviors have been described, the impact of parasites on pollinator foraging decisions and plant–pollinator interactions have been largely overlooked. Growing evidence of the transmission of parasites through the shared‐use of flowers by pollinators demonstrate the importance of behavioral immunity (altered behaviors that enhance parasite resistance) to pollinator health. During foraging bouts, pollinators can protect themselves against parasites through self‐medication, disease avoidance, and grooming. Recent studies have documented immune behaviors in foraging pollinators, as well as the impacts of such behaviors on flower visitation. Because pollinator parasites can affect flower choice and pollen dispersal, they may ultimately impact flower fitness. Here, we discuss how pollinator immune behaviors and floral traits may affect the presence and transmission of pollinator parasites, as well as how pollinator parasites, through these immune behaviors, can impact plant–pollinator interactions. We further discuss how pollinator immune behaviors can impact plant fitness, and how floral traits may adapt to optimize plant fitness in response to pollinator parasites. We propose future research directions to assess the role of pollinator parasites in plant–pollinator interactions and evolution, and we propose better integration of the role of pollinator parasites into research related to pollinator optimal foraging theory, floral diversity and agricultural practices.     

Ecology of malaria parasites infecting Southeast Asian macaques: evidence from cytochrome b sequences

Although malaria parasites infecting non‐human primates are important models for human malaria, little is known of the ecology of infection by these parasites in the wild. We extensively sequenced cytochrome b (cytb) of malaria parasites (Apicomplexa: Haemosporida) from free‐living southeast Asian monkeys Macaca nemestrina and Macaca fascicularis. The two most commonly observed taxa were Plasmodium inui and Hepatocystis sp., but certain other sequences did not cluster closely with any previously sequenced species. Most of the major clades of parasites were found in both Macaca species, and the two most commonly occurring parasite infected the two Macaca species at approximately equal levels. However, P. inui showed evidence of genetic differentiation between the populations infecting the two Macaca species, suggesting limited movement of this parasite among hosts. Moreover, coinfection with Plasmodium and Hepatocystis species occurred significantly less frequently than expected on the basis of the rates of infection with either taxon alone, suggesting the possibility of competitive exclusion. The results revealed unexpectedly complex communities of Plasmodium and Hepatocystis taxa infecting wild southeast Asian monkeys. Parasite taxa differed with respect to both the frequency of between‐host movement and their frequency of coinfection.     

Beta‐diversity gradients of butterflies along productivity axes

Aim Several lines of evidence suggest that beta diversity, or dissimilarity in species composition, should increase with productivity: (1) the latitudinal species richness gradient is most closely related to productivity and associated latitudinal beta‐diversity relationships have been described, and (2) the scale dependence of the productivity–diversity relationship implies that there should be a positive productivity–beta‐diversity relationship. However, such a pattern has not yet been demonstrated at broad scales. We test if there is a gradient of increasing beta diversity with productivity. Location Canada. Methods Canada was clustered into regions of similar productivity regimes along three remotely sensed productivity axes (minimum and integrated annual productivity, seasonality of productivity) and elevation. The overall (β_j), turnover (β_sim) and nestedness (β_nes) components of beta diversity within each productivity regime were estimated with pairwise dissimilarity metrics and related to cluster productivity with partial linear regression and with spatial autoregression. Tests were performed for all species, productivity breadth‐based subsets (e.g. species occurring in many and a moderate number of productivity regimes), and pre‐ and post‐1970 butterfly records. Beta diversity between adjacent clusters along the productivity gradients was also evaluated. Results Within‐cluster β_j and β_sim increased with productivity and decreased with seasonality. The converse was true for β_nes. All species subsets responded similarly; however, productivity–beta‐diversity relationships were weaker for the post‐1970 temporal subset and strongest for species of moderate breadth. Between‐cluster beta diversity (β_j) and nestedness (β_nes) declined with productivity. Main conclusions As predicted, beta diversity of communities within productivity regimes was observed to increase with productivity. This pattern was driven largely by a gradient of species turnover. Therefore, beta diversity may make an important contribution to the broad‐scale gradient of species richness with productivity. However, this species richness gradient dominates regional beta diversity between productivity regimes, resulting in decreasing between‐productivity dissimilarity with productivity driven by a concurrent decline in nestedness.     

Spatial structure,host heterogeneity and parasite virulence: implications for vaccine‐driven evolution

Natural host‐parasite interactions exhibit considerable variation in host quality, with profound consequences for disease ecology and evolution. For instance, treatments (such as vaccination) may select for more transmissible or virulent strains. Previous theory has addressed the ecological and evolutionary impact of host heterogeneity under the assumption that hosts and parasites disperse globally. Here, we investigate the joint effects of host heterogeneity and local dispersal on the evolution of parasite life‐history traits. We first formalise a general theoretical framework combining variation in host quality and spatial structure. We then apply this model to the specific problem of parasite evolution following vaccination. We show that, depending on the type of vaccine, spatial structure may select for higher or lower virulence compared to the predictions of non‐spatial theory. We discuss the implications of our results for disease management, and their broader fundamental relevance for other causes of host heterogeneity in nature.     

Epidemiology of a tick‐borne viral infection: theoretical insights and practical implications for public health

The morbidity of tick‐borne encephalitis (TBE) varies yearly by as much as 10‐fold among the people of Western Siberia. This long‐term variation is dependent on many factors such as the density of the tick populations, the prevalence of TBE virus (TBEV) among sub‐adult ticks, the yearly virulence of the TBEV, and prophylactic measures. Here we highlight the role of small mammal hosts in the circulation of TBEV through the ecosystem. Refining classical models of non‐viremic horizontal transmission, we emphasize the recently understood fact that the physiological and immunological status of the small mammal hosts affects the tick and virus‐host interactions. In addition to its theoretical interest, our approach may lead to some practical improvements in the precision of epidemiological forecasts and perhaps in forestalling the severity of outbreaks of TBE, or, at least, in forewarning medical authorities and the general public of impending TBE outbreaks.     

Population structure of a vector‐borne plant parasite

Parasites are among the most diverse groups of life on Earth, yet complex natural histories often preclude studies of their speciation processes. The biology of parasitic plants facilitates in situ collection of data on both genetic structure and the mechanisms responsible for that structure. Here, we studied the role of mating, dispersal and establishment in host race formation of a parasitic plant. We investigated the population genetics of a vector‐borne desert mistletoe (Phoradendron californicum) across two legume host tree species (Senegalia greggii and Prosopis velutina) in the Sonoran desert using microsatellites. Consistent with host race formation, we found strong host‐associated genetic structure in sympatry, little genetic variation due to geographic site and weak isolation by distance. We hypothesize that genetic differentiation results from differences in the timing of mistletoe flowering by host species, as we found initial flowering date of individual mistletoes correlated with genetic ancestry. Hybrids with intermediate ancestry were detected genetically. Individuals likely resulting from recent, successful establishment events following dispersal between the host species were detected at frequencies similar to hybrids between host races. Therefore, barriers to gene flow between the host races may have been stronger at mating than at dispersal. We also found higher inbreeding and within‐host individual relatedness values for mistletoes on the more rare and isolated host species (S. greggii). Our study spanned spatial scales to address how interactions with both vectors and hosts influence parasitic plant structure with implications for parasite virulence evolution and speciation.     

Host‐specific variation in off‐host performance of a temperate ectoparasite

Antagonistic host–parasite interactions are rarely considered from an ecological perspective of the parasite. We used a blood‐feeding ectoparasite of boreal cervids, the deer ked (Lipoptena cervi L., Hippoboscidae), to study host‐dependent variation in a parasite's ability to cope with an abiotic environment during the free‐living stage(s) in two allopatric Fennoscandian populations. We found that a strongly host‐specific deer ked population in eastern Fennoscandia, exploiting only moose (Alces alces), produced the largest offspring that were the most cold‐tolerant and emerged the earliest as adults, when compared with the western Fennoscandian population that exploited two hosts efficiently. Within the western population, however, offspring produced on roe deer (Capreolus capreolus) were significantly larger, more cold‐tolerant, and had higher survival than those produced on moose in the same area. We discuss potential causes for both host‐specific and geographical differences in off‐host performance: (1) maternal host directly affects the offspring survival prospects; (2) divergent co‐evolution with local main host(s) has shaped the parasite's life history; and/or (3) off‐host performance is shaped by adaptation to the local abiotic environment. In conclusion, this study increases our understanding of the evolution of host–parasite interactions by demonstrating how geographical differences in host exploitation may result in differences in survival prospects outside the host.     

Coevolutionary interactions with parasites constrain the spread of self‐fertilization into outcrossing host populations

Given the cost of sex, outcrossing populations should be susceptible to invasion and replacement by self‐fertilization or parthenogenesis. However, biparental sex is common in nature, suggesting that cross‐fertilization has substantial short‐term benefits. The Red Queen hypothesis (RQH) suggests that coevolution with parasites can generate persistent selection favoring both recombination and outcrossing in host populations. We tested the prediction that coevolving parasites can constrain the spread of self‐fertilization relative to outcrossing. We introduced wild‐type Caenorhabditis elegans hermaphrodites, capable of both self‐fertilization, and outcrossing, into C. elegans populations that were fixed for a mutant allele conferring obligate outcrossing. Replicate C. elegans populations were exposed to the parasite Serratia marcescens for 33 generations under three treatments: a control (avirulent) parasite treatment, a fixed (nonevolving) parasite treatment, and a copassaged (potentially coevolving) parasite treatment. Self‐fertilization rapidly invaded C. elegans host populations in the control and the fixed‐parasite treatments, but remained rare throughout the entire experiment in the copassaged treatment. Further, the frequency of the wild‐type allele (which permits selfing) was strongly positively correlated with the frequency of self‐fertilization across host populations at the end of the experiment. Hence, consistent with the RQH, coevolving parasites can limit the spread of self‐fertilization in outcrossing populations.     

Towards an eco‐phylogenetic framework for infectious disease ecology

Identifying patterns and drivers of infectious disease dynamics across multiple scales is a fundamental challenge for modern science. There is growing awareness that it is necessary to incorporate multi‐host and/or multi‐parasite interactions to understand and predict current and future disease threats better, and new tools are needed to help address this task. Eco‐phylogenetics (phylogenetic community ecology) provides one avenue for exploring multi‐host multi‐parasite systems, yet the incorporation of eco‐phylogenetic concepts and methods into studies of host pathogen dynamics has lagged behind. Eco‐phylogenetics is a transformative approach that uses evolutionary history to infer present‐day dynamics. Here, we present an eco‐phylogenetic framework to reveal insights into parasite communities and infectious disease dynamics across spatial and temporal scales. We illustrate how eco‐phylogenetic methods can help untangle the mechanisms of host–parasite dynamics from individual (e.g. co‐infection) to landscape scales (e.g. parasite/host community structure). An improved ecological understanding of multi‐host and multi‐pathogen dynamics across scales will increase our ability to predict disease threats.     

The sound of a blood meal: Acoustic ecology of frog‐biting midges (Corethrella) in lowland Pacific Costa Rica

Animal communication systems are often exploited by eavesdropping antagonists, especially predators and ectoparasites. Female frog‐biting midges (Diptera: Corethrellidae) are known to use male anuran advertisement calls to locate their blood hosts, frogs. Here, we use acoustic midge traps broadcasting synthetic and recorded calls to identify those frog call parameters that affect midge attraction. At our study site in Pacific lowland Costa Rica, we found that overall midge attraction was influenced by both spectral and temporal acoustic parameters. Low dominant frequencies (below 1 kHz) and short pulse durations (between 125 and 500 ms) attracted the highest numbers of midges in tests with synthetic sinusoidal pure tones. These preferences partially explained the relative attractiveness of the advertisement calls of ten local frog species. The advertisement calls of the common and widespread Giant Bullfrog, Leptodactylus savagei (Anura: Leptodactylidae), attracted by far the largest number of midges, suggesting that this frog species might be a key resource for frog‐biting midges in Costa Rica. Although we found that calls of different frog species attracted different midge species/morphospecies in statistically different proportions, acoustic niche differentiation among midge species appeared to be moderate, suggesting either a limited degree of host specialization or the use of additional short‐range, that is, chemical, host recognition cues.     

On the role of host phenotypic plasticity in host shifting by parasites

Ecological speciation appears to contribute to the diversification of insect herbivores and other parasites, which together comprise a major component of Earth's biodiversity. Host shifts are likely an important step in ecological speciation, and understanding how such shifts occur is critical to forming and testing hypotheses explaining parasite diversity. In this article, I argue that phenotypic variation in hosts arising from environmental variation (phenotypic plasticity) can promote shifts in parasites by bridging both spatiotemporal and phenotypic gaps between ancestral and novel hosts. This hypothesis, which I call the ‘plastic‐bridge hypothesis’, is conceptually distinct from those invoking genetic variation in bridging these gaps. I describe the mechanistic basis of plastic bridges, review circumstantial evidence in support of the hypothesis and suggest strategies for testing it. I use herbivorous insects and their host plants as a model, but the proposed ideas apply to any system fitting a broad definition of a host‐parasite relationship. The plastic‐bridge perspective suggests that parasite diversity is not only due to divergent selection provided by hosts, but also to the intraspecific variation that facilitates shifts between them. This view is timely, as biological invasion and range shifts associated with climate change foster novel interactions between parasites and hosts.     

Determining the relative roles of species replacement and species richness differences in generating beta‐diversity patterns

Aim To determine the relative contribution of species replacement and species richness differences to the emergence of beta‐diversity patterns. Innovation A novel method that disentangles all compositional differences (β_cc, overall beta diversity) in its two components, species replacement (β_‐3) and species richness differences (β_rich) is proposed. The performance of the method was studied with ternary plots, which allow visualization of the influence of the relative proportions of shared and unique species of two sites over each metric. The method was also tested in different hypothetical gradients and with real datasets. The novel method was compared with a previous proposal based on the partitioning of overall compositional differences (β_sor) in replacement (β_sim) and nestedness (β_nes). The linear response of β_cc contrasts with the curvilinear response of β_sor to linear gradients of dissimilarity. When two sites did not share any species, β_sim was always 1 and β_‐3 only reached 1 when the number of exclusive species of both sites was equal. β_‐3 remained constant along gradients of richness differences with constant replacement, while β_sim decreased. β_rich had a linear response to a linear gradient of richness differences with constant species replacement, whereas β_nes exhibited a hump‐shaped response. Moreover, β_sim > β_nes when clearly almost all species of one site were lost, whereas β_‐3 < β_rich in the same circumstances. Main conclusions The behaviour of the partition of β_cc into β_‐3 and β_rich is consistent with the variation of replacement and richness differences. The partitioning of β_sor into β_sim and β_nes overestimates the replacement component and underestimates richness differences. The novel methodology allows the discrimination of different causes of beta‐diversity patterns along latitudinal, biogeographic or ecological gradients, by estimating correctly the relative contributions of replacement and richness differences.