Dynamics of a feline retrovirus (FeLV) in host populations with variable spatial structure.

The predictions of epidemic models are remarkably affected by the underlying assumptions concerning host population dynamics and the relation between host density and disease transmission. Furthermore, hypotheses underlying distinct models are rarely tested. Domestic cats (Felis catus) can be used to compare models and test their predictions, because cat populations show variable spatial structure that probably results in variability in the relation between density and disease transmission. Cat populations also exhibit various dynamics. We compare four epidemiological models of Feline Leukaemia Virus (FeLV). We use two different incidence terms, i.e. proportionate mixing and pseudo-mass action. Population dynamics are modelled as logistic or exponential growth. Compared with proportionate mixing, mass action incidence with logistic growth results in a threshold population size under which the virus cannot persist in the population. Exponential growth of host populations results in systems where FeLV persistence at a steady prevalence and depression of host population growth are biologically unlikely to occur. Predictions of our models account for presently available data on FeLV dynamics in various populations of cats. Thus, host population dynamics and spatial structure can be determinant parameters in parasite transmission, host population depression, and disease control.     

Ecology and dynamics of the blood parasite, Hepatozoon tuatarae (Apicomplexa), in tuatara (Sphenodon punctatus) on Stephens Island, New Zealand

We explored infection patterns and temporal dynamics of the protozoan blood parasite Hepatozoon tuatarae (Apicomplexa) infecting the tuatara (Sphenodon punctatus), a protected reptile living on Stephens Island, New Zealand. In March 2006, we surveyed tuatara in five study sites to examine spatial variation in infection prevalence, and four times, from May 2005 to November 2006, we recaptured marked individuals within three study sites to examine the temporal dynamics of infection. We also examined how blood-parasite infection patterns were influenced by host sex, body size, and host infestation with ticks (Amblyomma sphenodonti) and mites (Neotrombicula spp.), which are potential vectors of the blood parasite. Infection prevalence (16.9-24% infected) and intensity (<0.01-0.1% blood cells infected) were low in all samples. Infection intensity varied among the five sampled sites in March 2006, but prevalence did not. Neither infection prevalence nor intensity varied with time, and infections were detected in consecutive samples from recaptured individuals for up to 18 mo. Neither survey showed an influence of host sex on infection, but both surveys showed infection intensity declined with increasing host body size, as did infection prevalence in the spatial survey. In the temporal survey, we found a positive relationship between the tick numbers on hosts and blood-parasite infection intensity, which were stronger in two of the sampling periods and among larger hosts. These data suggest that exposure and susceptibility to infection decreases with host size and that ticks, but not mites, are probably the vectors in this ancient host-parasite association of a long-lived (>50 yr) host.     

Host species,and not environment,predicts variation in blood parasite prevalence,distribution, and diversity along a humidity gradient in northern South America

Environmental factors strongly influence the ecology and evolution of vector‐borne infectious diseases. However, our understanding of the influence of climatic variation on host–parasite interactions in tropical systems is rudimentary. We studied five species of birds and their haemosporidian parasites (Plasmodium and Haemoproteus) at 16 sampling sites to understand how environmental heterogeneity influences patterns of parasite prevalence, distribution, and diversity across a marked gradient in water availability in northern South America. We used molecular methods to screen for parasite infections and to identify parasite lineages. To characterize spatial heterogeneity in water availability, we used weather‐station and remotely sensed climate data. We estimated parasite prevalence while accounting for spatial autocorrelation, and used a model selection approach to determine the effect of variables related to water availability and host species on prevalence. The prevalence, distribution, and lineage diversity of haemosporidian parasites varied among localities and host species, but we found no support for the hypothesis that the prevalence and diversity of parasites increase with increasing water availability. Host species and host × climate interactions had stronger effects on infection prevalence, and parasite lineages were strongly associated with particular host species. Because climatic variables had little effect on the overall prevalence and lineage diversity of haemosporidian parasites across study sites, our results suggest that independent host–parasite dynamics may influence patterns in parasitism in environmentally heterogeneous landscapes.     

Spatial but not temporal co-divergence of a virus and its mammalian host

Co-divergence between host and parasites suggests that evolutionary processes act across similar spatial and temporal scales. Although there has been considerable work on the extent and correlates of co-divergence of RNA viruses and their mammalian hosts, relatively little is known about the extent to which virus evolution is determined by the phylogeographic history of host species. To test hypotheses related to co-divergence across a variety of spatial and temporal scales, we explored phylogenetic signatures in Andes virus (ANDV) sampled from Chile and its host rodent, Oligoryzomys longicaudatus. ANDV showed strong spatial subdivision, a phylogeographic pattern also recovered in the host using both spatial and genealogical approaches, and despite incomplete lineage sorting. Lineage structure in the virus seemed to be a response to current population dynamics in the host at the spatial scale of ecoregions. However, finer scale analyses revealed contrasting patterns of genetic structure across a latitudinal gradient. As predicted by their higher substitution rates, ANDV showed greater genealogical resolution than the rodent, with topological congruence influenced by the degree of lineage sorting within the host. However, despite these major differences in evolutionary dynamics, the geographic structure of host and virus converged across large spatial scales.     

Parasite survey of a Daphnia hybrid complex: host-specificity and environment determine infection

1. Hybridization between species is a common phenomenon in plants and animals. If parasite prevalence differs for hybrids and parental species (i.e. taxa) there may be considerable consequences for relative hybrid fitness. Some studies have investigated hybrid complexes for infection, and complex-specific differences in parasite prevalence have been detected. 2. Based on the results of a field study on a hybridizing Daphnia population from a single lake, it has been hypothesized that permanently over- or under-infected hybrids do not exist. The observed field-patterns can only be temporal because taxa, in addition to single genotypes, might be the subject of parasite driven host frequency-dependent selection. Thus, parasites will track any common taxon within a hybrid complex. 3. In the present study, hybridizing Daphnia populations from 43 lakes were screened for parasite infections to obtain indirect evidence for coevolutionary cycles. It was hypothesized that, due to time lags between the evolution of resistance in host populations and the evolution of the parasite towards tracking of a common host taxon, the same Daphnia taxon will be over-infected in some lakes, while being under-infected in others. 4. Two of the four parasite species were specialists: their prevalence differed among coexisting Daphnia taxa. The varying infection patterns detected across spatially segregated hybridizing Daphnia populations are consistent with theoretical predictions for coevolutionary cycles. Thus the infection patterns, as observed under natural conditions, are temporal and unstable. 5. Additionally, the spatial distribution of the four parasite species was analysed with respect to habitat differences. The results show that the presence of a particular parasite on a host taxon was determined not only by the host-specificity of the parasite, but also by host-habitat relations.     

Effect of sexual segregation on host-parasite interaction: Model simulation for abomasal parasite dynamics in alpine ibex (Capraibex)

We investigated whether sexual segregation might affect parasite transmission and host dynamics, hypothesising that if males are the more heavily infected sex and more responsible for the transmission of parasite infections, female avoidance of males and the space they occupy could reduce infection rates. A mathematical model, simulating the interaction between abomasal parasites and a hypothetical alpine ibex (Capraibex) host population composed of its two sexes, was developed to predict the effect of different degrees of sexual segregation on parasite intensity and on host abundance. The results showed that when females tended to be segregated from males, and males were distributed randomly across space, the impact of parasites was the lowest, resulting in the highest host abundance, with each sex having the lowest parasite intensity. The predicted condition that minimises the impact of parasites in our model was the one closest to that observed in nature where females actively seek out the more segregated sites while males are less selective in their ranging behaviour. The overlapping of field observation with the predicted optimal strategy lends support to our idea that there might be a connection between parasite transmission and sexual segregation. Our simulations provide the biological boundaries of host-parasite interaction needed to determine a parasite-mediated effect on sexual segregation and a formalised null hypothesis against which to test future field experiments.     

DYNAMIC TRANSMISSION,HOST QUALITY,AND POPULATION STRUCTURE IN A MULTIHOST PARASITE OF BUMBLEBEES

The evolutionary ecology of multihost parasites is predicted to depend upon patterns of host quality and the dynamics of transmission networks. Depending upon the differences in host quality and transmission asymmetries, as well as the balance between intra‐ and interspecific transmission, the evolution of specialist or generalist strategies is predicted. Using a trypanosome parasite of bumblebees, we ask how host quality and transmission networks relate to parasite population structure across host species, and thus the potential for the evolution of specialist strains adapted to different host species. Host species differed in quality, with parasite growth varying across host species. Highly asymmetric transmission networks, together with differences in host quality, likely explain local population structure of the parasite across host species. However, parasite population structure across years was highly dynamic, with parasite populations varying significantly from one year to the next within individual species at a given site. This suggests that, while host quality and transmission may provide the opportunity for short‐term host specialization by the parasite, repeated bottlenecking of the parasite, in combination with its own reproductive biology, overrides these smaller scale effects, resulting in the evolution of a generalist parasite.     

Host patch traits have scale-dependent effects on diversity in a stickleback parasite metacommunity

Many metacommunities are distributed across habitat patches that are themselves aggregated into groups. Perhaps the clearest example of this nested metacommunity structure comes from multi-species parasite assemblages, which occupy individual hosts that are aggregated into host populations. At both spatial scales, we expect parasite community diversity in a given patch (either individual host or population) to depend on patch characteristics that affect colonization rates and species sorting. But, are these patch effects consistent across spatial scales? Or, do different processes govern the distribution of parasite community diversity among individual hosts, versus among host patches? To answer these questions, we document the distribution of parasite richness among host individuals and among populations in a metapopulation of threespine stickleback Gasterosteus aculeatus. We find some host traits (host size, gape width) are associated with increased parasite richness at both spatial scales. Other patch characteristics affect parasite richness only among individuals (sex), or among populations (lake size, lake area, elevation and population mean heterozygosity). These results demonstrate that some rules governing parasite richness in this metacommunity are shared across scales, while others are scale-specific.     

Genetic structure of Schstosoma mansoni in western Kenya: The effects of geography and host sharing

We examined the spatial structure of Schistosoma mansoni, a parasite of humans, from natural infections at two levels: across the Lake Victoria basin of Kenya and among snail hosts. Using 20 microsatellite markers we examined geographic patterns of relatedness and population structure of cercariae and found weak, but significant structure detected by some, but not all analyses. We hypothesise structure created by aggregations of clonal individuals or adherence of hosts to local transmission sites is eroded by high amounts of gene flow in the region. This finding also supports previous hypotheses concerning the evolution of drug resistance in the region. Intrasnail dynamics were investigated in the context of aggregation and kin selection theory to determine how relatedness and also sex influence host sharing and host exploitation. Cercarial production did not differ significantly between snails with one or two genotypes suggesting that mixed infections resulted in decreased individual fitness and provides a framework for reproductive competition. Coinfection patterns in snails were independent of parasite relatedness indicating that schistosomes were not aggregated according to their relatedness and that kin selection was not influencing host sharing. Additionally, host exploitation in coinfections (measured by cercarial production) was not negatively correlated with relatedness, as predicted by classical models due to increased competition and thus exploitation when parasites are unrelated. Because of the low levels of relatedness within the population, schistosomes may rarely encounter close relatives and kin selection mechanisms that influence the distribution of individuals within snails or the virulence mode of the parasites may simply have not evolved.     

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.     

Host–parasite determinants of parasite population structure: lessons from bats and mites on the importance of time

By definition, parasitic organisms are strongly dependant on their hosts, and for a great majority, this dependence includes host-to-host transmission. Constraints imposed by the host's spatial distribution and demography, in combination with those of the parasite, can lead to a metapopulation structure, where parasite populations are highly stochastic (i.e. prone to frequent extinctions and re-colonizations) and where drift becomes a major force shaping standing genetic variation. This, in turn, will directly affect the observed population structure, along with the ability of the parasite to adapt (or co-adapt) to its host. However, only a specific consideration of temporal dynamics can reveal the extent to which drift shapes parasite population structure; this is rarely taken into account in population genetic studies of parasitic organisms. The study by Bruyndonckx et al. in this issue of Molecular Ecology does just this and, in doing so, illustrates how a comparison of host–parasite co-structures in light of temporal dynamics can be particularly informative for understanding the ecological and evolutionary constraints imposed by the host. More specifically, the authors examine spatial and temporal population genetic data of a parasitic mite Spinturnix bechsteini that exclusively exploits the Bechstein's bat Myotis bechsteinii and consider these data in relation to host–parasite life histories and the population structure of the host.     

Assessment of Anopheles salivary antigens as individual exposure biomarkers to species-specific malaria vector bites

The development of parasitological immunity against malaria affects the ability to detect infection, the efficiency of the local human parasite reservoir at infecting mosquitoes, and the response to reintroduction of parasites to previously cleared areas. Observations of similar age-trends in detected prevalence and mean parasitaemia across more than an order-of-magnitude of variation in baseline transmission complicate simple exposure-driven explanations. Mathematical models often employ age-dependent immune factors to match the observed trends, while the present model uses a new detailed mechanistic model of parasite transmission dynamics to explain age-trends through the mechanism of parasite diversity. Illustrative simulations are performed for multiple field sites in Tanzania and Nigeria, and observed age-trends and seasonality in parasite prevalence are recreated in silico, proffering possible mechanistic explanations of the observational data. Observed temporal dynamics in measured parasitaemia are recreated for each location and age-prevalence outputs are studied. Increasing population-level diversity in malaria surface antigens delays development of broad parasitological immunity. A local parasite population with high diversity can recreate the observed trends in age-prevalence across more than an order of magnitude of variation in transmission intensities. Mechanistic models of human immunity and parasite antigen diversity can recreate the observed temporal patterns for the development of parasitological immunity across a wide range of transmission intensities. This has implications for the distribution of disease burden across the population, the human transmission reservoir, design of elimination campaigns, and development and roll-out of potential vaccines.     

Host and parasite recruitment correlated at a regional scale

Drivers of large-scale variability in parasite prevalence are not well understood. For logistical reasons, explorations of spatial patterns in parasites are often performed as observational studies. However, to understand the mechanisms that underlie these spatial patterns, standardized and controlled comparisons are needed. Here, we examined spatial variability in infection of an important fishery species and ecosystem engineer, the oyster (Crassostrea virginica) by its pea crab parasite (Zaops ostreus) across 700 km of the southeastern USA coastline. To minimize the influence of host genetics on infection patterns, we obtained juvenile oysters from a homogeneous source stock and raised them in situ for 3 months at multiple sites with similar environmental characteristics. We found that prevalence of pea crab infection varied between 24 and 73 % across sites, but not systematically across latitude. Of all measured environmental variables, oyster recruitment correlated most strongly (and positively) with pea crab infection, explaining 92 % of the variability in infection across sites. Our data ostensibly suggest that regional processes driving variation in oyster recruitment similarly affect the recruitment of one of its common parasites.     

Effect of Ascaridia compar infection on rock partridge population dynamics: empirical and theoretical investigations

Helminth parasites have the potential to significantly affect the dynamics of their hosts. As a consequence, they can dramatically threaten the persistence of endangered species, such as rock partridge Alectoris graeca saxatilis, found in the Province of Trento (northern Italy). The aim of this work was to understand the effect of helminth parasites on rock partridge fitness, and the subsequent potential effects on host population dynamics. In particular, we investigated the hypothesis that infections from Ascaridia compar induce rock partridge population cycles observed in Trentino. In order to support this hypothesis, we compared the predictions obtained from a host–parasite interaction model including variable parasite aggregation with multi‐annual empirical data of A. compar infection in natural host populations. We estimated host demographic parameters using rock partridge census data from Trentino, and the parasitological parameters from a series of experimental infections in a captive rock partridge population. The host–parasite model predicted higher A. compar abundance in rock partridge populations exhibiting cyclic dynamics compared to non‐cyclic ones. In addition, for cyclic host populations, the model predicted an increase in mean parasite burden with the length of cycle period. Model predictions were well‐supported by field data: significant differences in parasite infection between cyclic and non‐cyclic populations and among cyclic populations with different oscillation periods were observed. On the basis of these results, we conclude that helminth parasites can not be ruled out as drivers of rock partridge population dynamics in Trentino and must be considered when planning conservation strategies of this threatened species.     

Patterns of parasite abundance and distribution in island populations of Galápagos endemic birds

Parasite life-history characteristics, the environment, and host defenses determine variation in parasite population parameters across space and time. Parasite abundance and distribution have received little attention despite their pervasive effects on host populations and community dynamics. We used analyses of variance to estimate the variability of intensity, prevalence, and abundance of 4 species of lice (Insecta: Phthiraptera) infecting Galápagos doves and Galápagos hawks and 1 haemosporidian parasite (Haemosporida: Haemoproteidae) infecting the doves across island populations throughout their entire geographic ranges. Population parameters of parasites with direct life cycles varied less within than among parasite species, and intensity and abundance did not differ significantly across islands. Prevalence explained a proportion of the variance (34%), similar to infection intensity (33%) and parasite abundance (37%). We detected a strong parasite species-by-island interaction, suggesting that parasite population dynamics is independent among islands. Prevalence (up to 100%) and infection intensity (parasitemias up to 12.7%) of Haemoproteus sp. parasites varied little across island populations.     

Parasitic castration: host species preferences,size-selectivity and spatial heterogeneity

Summary This study investigates host-parasite population dynamics in a marine intertidal community of three barnacle host species (Balanus glandula, Chthamalus fissus andC. dalli). Our paper addresses the following questions: (1) Does prevalence (percentage parasitism) differ among the three host species? (2) What are the spatial and temporal population dynamics within the community? and (3) Does the parasite exhibit size-selective behaviour in any of the three host species? Significant differences in prevalence were found among the three host species; the parasitic castrator (Hemioniscus balani) most heavily infected the least abundant host. Parasitism occurred throughout the year and also showed significant spatial variation.H. balani showed size-selective parasitism inC. fissus, but not inC. dalli. Consequently, the population effects of parasitic castration inC. fissus depend both upon the host population size structure and the intensity of the parasite's size-selectivity.     

Schistocephalus solidus parasite prevalence and biomass intensity in threespine stickleback vary by habitat and diet in boreal lakes

Trophically-transmitted parasites can affect intermediate host behaviors, resulting in spatial differences in parasite prevalence and distribution that shape the dynamics of hosts and their ecosystems. This variability may arise through differences in physical habitats or biological interactions between parasites and their hosts, and may occur on very fine spatial scales. Using a pseudophyllidean cestode (Schistocephalus solidus) and the threespine stickleback (Gasterosteus aculeatus) as a model parasite–host complex, we investigated the association of infection with host diet composition and stomach fullness in different habitats of two large lakes in southwest Alaska. To become infected, the fish must consume pelagic copepods infected with the parasite’s procercoid stage, so we predicted higher infection rates of fish in offshore habitats (where zooplankton are the primary prey) compared to fish from the littoral zone. Sticklebacks collected from the littoral and limnetic zones were assayed for parasites and their stomach contents were classified, counted, and weighed. Contrary to our prediction, permutational multivariate analysis of variance and principal components analysis revealed that threespine sticklebacks in the littoral zone, which consumed a generalist diet (pelagic zooplankton and benthic invertebrates), had higher parasite prevalence and biomass intensity than conspecifics in the limnetic zone, which consumed zooplankton. These results, consistent in two different lakes, suggest that differences in parasite prevalence between habitats may have been determined by a shift in host habitat due to infection, differential host mortality across habitats, differential procercoid prevalence in copepods across habitats, or a combination of the three factors. This paradoxical result highlights the potential for fine spatial variability in parasite abundance in natural systems.     

Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction

The potential for local adaptation between pathogens and their hosts has generated strong theoretical and empirical interest with evidence both for and against local adaptation reported for a range of systems. We use the Linum marginale-Melampsora lini plant-pathogen system and a hierarchical spatial structure to investigate patterns of local adaptation within a metapopulation characterised by epidemic dynamics and frequent extinction of pathogen populations. Based on large sample sizes and comprehensive cross-inoculation trials, our analyses demonstrate strong local adaptation by Melampsora to its host populations, with this effect being greatest at regional scales, as predicted from the broader spatial scales at which M. lini disperses relative to L. marginale. However, there was no consistent trend for more distant pathogen populations to perform more poorly. Our results further show how the coevolutionary interaction between hosts and pathogens can be influenced by local structure such that resistant hosts select for generally virulent pathogens, while susceptible hosts select for more avirulent pathogens. Empirically, local adaptation has generally been tested in two contrasting ways: (1) pathogen performance on sympatric versus allopatric hosts; and (2) sympatric versus allopatric pathogens on a given host population. In situations where no host population is more resistant or susceptible than others when averaged across pathogen populations (and likewise, no pathogen population is more virulent or avirulent than others), results from these tests should generally be congruent. We argue that this is unlikely to be the case in the metapopulation situations that predominate in natural host-pathogen interactions, thus requiring tests that control simultaneously for variation in plant and pathogen populations.     

Landscape heterogeneity shapes host‐parasite interactions and results in apparent plant–virus codivergence

Knowledge on how landscape heterogeneity shapes host–parasite interactions is central to understand the emergence, dynamics and evolution of infectious diseases. However, this is an underexplored subject, particularly for plant–virus systems. Here, we analyse how landscape heterogeneity influences the prevalence, spatial genetic structure, and temporal dynamics of Pepper golden mosaic and Pepper huasteco yellow vein begomoviruses infecting populations of the wild pepper Capsicum annuum glabriusculum (chiltepin) in Mexico. Environmental heterogeneity occurred at different nested spatial scales (host populations within biogeographical provinces), with levels of human management varying among host population within a province. Results indicate that landscape heterogeneity affects the epidemiology and genetic structure of chiltepin‐infecting begomoviruses in a scale‐specific manner, probably related to conditions favouring the viruses' whitefly vector and its dispersion. Increased levels of human management of the host populations were associated with higher virus prevalence and erased the spatial genetic structure of the virus populations. Also, environmental heterogeneity similarly shaped the spatial genetic structures of host and viruses. This resulted in the congruence between host and virus phylogenies, which does not seem to be due to host‐virus co‐evolution. Thus, results provide evidence of the key role of landscape heterogeneity in determining plant–virus interactions.     

The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis

We investigated the role of host sex in parasite transmission and questioned: ‘Is host sex important in influencing the dynamics of infection in free living animal populations?’ We experimentally reduced the helminth community of either males or females in a yellow‐necked mice (Apodemus flavicollis) population using an anthelmintic, in replicated trapping areas, and subsequently monitored the prevalence and intensity of macroparasites in the untreated sex. We focussed on the dominant parasite Heligmosomoides polygyrus and found that reducing parasites in males caused a consistent reduction of parasitic intensity in females, estimated through faecal egg counts, but the removal of parasites in females had no significant influence on the parasites in males. This finding suggests that males are responsible for driving the parasite infection in the host population and females may play a relatively trivial role. The possible mechanisms promoting such patterns are discussed.