Random parasite encounters coupled with condition-linked immunity of hosts generate parasite aggregation

Parasite aggregation is viewed as a natural law in parasite-host ecology but is a paradox insofar as parasites should follow the Poisson distribution if hosts are encountered randomly. Much research has focused on whether parasite aggregation in or on hosts is explained by aggregation of infective parasite stages in the environment, or by heterogeneity within host samples in terms of host responses to infection (e.g., through representation of different age classes of hosts). In this paper, we argue that the typically aggregated distributions of parasites may be explained simply. We propose that aggregated distributions can be derived from parasites encountering hosts randomly, but subsequently by parasites being 'lost' from hosts based on condition-linked escape or immunity of hosts. Host condition should be a normally distributed trait even among otherwise homogeneous sets of hosts. Our model shows that mean host condition and variation in host condition have different effects on the different metrics of parasite aggregation. Our model further predicts that as host condition increases, parasites become more aggregated but numbers of attending parasites are reduced overall and this is important for parasite population dynamics. The effects of deviation from random encounter are discussed with respect to the relationship between host condition and final parasite numbers.     

Bottom–up regulation of parasite population densities in freshwater ecosystems

Theory predicts the bottom–up coupling of resource and consumer densities, and epidemiological models make the same prediction for host–parasite interactions. Empirical evidence that spatial variation in local host density drives parasite population density remains scarce, however. We test the coupling of consumer (parasite) and resource (host) populations using data from 310 populations of metazoan parasites infecting invertebrates and fish in New Zealand lakes, spanning a range of transmission modes. Both parasite density (no. parasites per m²) and intensity of infection (no. parasites per infected hosts) were quantified for each parasite population, and related to host density, spatial variability in host density and transmission mode (egg ingestion, contact transmission or trophic transmission). The results show that dense and temporally stable host populations are exploited by denser and more stable parasite populations. For parasites with multi‐host cycles, density of the ‘source’ host did not matter: only density of the current host affected parasite density at a given life stage. For contact‐transmitted parasites, intensity of infection decreased with increasing host density. Our results support the strong bottom–up coupling of consumer and resource densities, but also suggest that intraspecific competition among parasites may be weaker when hosts are abundant: high host density promotes greater parasite population density, but also reduces the number of conspecific parasites per individual host.     

Within-host population dynamics and the evolution of microparasites in a heterogeneous host population

Abstract Why do parasites harm their hosts? The general understanding is that if the transmission rate and virulence of a parasite are linked, then the parasite must harm its host to maximize its transmission. The exact nature of such trade‐offs remains largely unclear, but for vertebrate hosts it probably involves interactions between a microparasite and the host immune system. Previous results have suggested that in a homogeneous host population in the absence of super‐ or coinfection, within‐host dynamics lead to selection of the parasite with an intermediate growth rate that is just being controlled by the immune system before it kills the host (Antia et al. 1994). In this paper, we examine how this result changes when heterogeneity is introduced to the host population. We incorporate the simplest form of heterogeneity–random heterogeneity in the parameters describing the size of the initial parasite inoculum, the immune response of the host, and the lethal density at which the parasite kills the host. We find that the general conclusion of the previous model holds: parasites evolve some intermediate growth rate. However, in contrast with the generally accepted view, we find that virulence (measured by the case mortality or the rate of parasite‐induced host mortality) increases with heterogeneity. Finally, we link the within‐host and between‐host dynamics of parasites. We show how the parameters for epidemiological spread of the disease can be estimated from the within‐host dynamics, and in doing so examine the way in which trade‐offs between these epidemiological parameters arise as a consequence of the interaction of the parasite and the immune response of the host.     

Role of parasite transmission in promoting inbreeding: I. Infection intensities drive individual parasite selfing rates

Among parasitic organisms, inbreeding has been implicated as a potential driver of host–parasite co‐evolution, drug‐resistance evolution and parasite diversification. Yet, fundamental topics about how parasite life histories impact inbreeding remain to be addressed. In particular, there are no direct selfing‐rate estimates for hermaphroditic parasites in nature. Our objectives were to elucidate the mating system of a parasitic flatworm in nature and to understand how aspects of parasite transmission could influence the selfing rates of individual parasites. If there is random mating within hosts, the selfing rates of individual parasites would be an inverse power function of their infection intensities. We tested whether selfing rates deviated from within‐host random mating expectations with the tapeworm Oochoristica javaensis. In doing so, we generated, for the first time in nature, individual selfing‐rate estimates of a hermaphroditic flatworm parasite. There was a mixed‐mating system where tapeworms self‐mated more than expected with random mating. Nevertheless, individual selfing rates still had a significant inverse power relationship to infection intensities. The significance of this finding is that the distribution of parasite infection intensities among hosts, an emergent property of the transmission process, can be a key driver in shaping the primary mating system, and hence the level of inbreeding in the parasite population. Moreover, we demonstrated how potential population selfing rates can be estimated using the predicted relationship of individual selfing rates to intensities and showed how the distribution of parasites among hosts can indirectly influence the primary mating system when there is density‐dependent fecundity.     

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta‐analysis, focusing on a model taxon: acanthocephalan parasites. Acanthocephala is a phylum of helminth parasites that use vertebrates as final hosts and invertebrates as intermediate hosts, and is one of the few parasite groups for which manipulation is predicted to be ancestral. We compiled 279 estimates of parasite‐induced alterations in phenotypic trait value, from 81 studies and 13 acanthocephalan species, allocating a sign to effect size estimates according to the direction of alteration favouring parasite transmission, and grouped traits by category. Phylogenetic inertia accounted for a low proportion of variation in effect sizes. The overall average alteration of trait value was moderate and positive when considering the expected effect of alterations on trophic transmission success (signed effect sizes, after the onset of parasite infectivity to the final host). Variation in the alteration of trait value was affected by the category of phenotypic trait, with the largest alterations being reversed taxis/phobia and responses to stimuli, and increased vulnerability to predation, changes to reproductive traits (behavioural or physiological castration) and immunosuppression. Parasite transmission would thereby be facilitated mainly by changing mainly the choice of micro‐habitat and the anti‐predation behaviour of infected hosts, and by promoting energy‐saving strategies in the host. In addition, infection with larval stages not yet infective to definitive hosts (acanthella) tends to induce opposite effects of comparable magnitude to infection with the infective stage (cystacanth), although this result should be considered with caution due to the low number of estimates with acanthella. This analysis raises important issues that should be considered in future studies investigating the adaptive significance of host manipulation, not only in acanthocephalans but also in other taxa. Specifically, the contribution of phenotypic traits to parasite transmission and the range of taxonomic diversity covered deserve thorough attention. In addition, the relationship between behaviour and immunity across parasite developmental stages and host–parasite systems (the neuropsychoimmune hypothesis of host manipulation), still awaits experimental evidence. Most of these issues apply more broadly to reported cases of host manipulation by other groups of parasites.     

Priority effects within coinfected hosts can drive unexpected population‐scale patterns of parasite prevalence

Organisms are frequently coinfected by multiple parasite strains and species, and interactions between parasites within hosts are known to influence parasite prevalence and diversity, as well as epidemic timing. Importantly, interactions between coinfecting parasites can be affected by the order in which they infect hosts (i.e. within‐host priority effects). In this study, we use a single‐host, two‐pathogen, SI model with environmental transmission to explore how within‐host priority effects scale up to alter host population‐scale infection patterns. Specifically, we ask how parasite prevalence changes in the presence of different types of priority effects. We consider two scenarios without priority effects and four scenarios with priority effects where there is either an advantage or a disadvantage to being the first to infect in a coinfected host. Models without priority effects always predict negative relationships between the prevalences of both parasites. In contrast, models with priority effects can yield unimodal prevalence relationships where the prevalence of a focal parasite is minimized or maximized at intermediate prevalences of a coinfecting parasite. The mechanism behind this pattern is that as the prevalence of the coinfecting parasite increases, most infections of the focal parasite change from occurring as solo infections, to first arrival coinfections, to second arrival coinfections. The corresponding changes in parasite fitness as the focal parasite moves from one infection class to another then map to changes in focal parasite prevalence. Further, we found that even when parasites interact negatively within a host, they still can have positive prevalence relationships at the population scale. These results suggest that within‐host priority effects can change host population‐scale infection patterns in systematic (and initially counterintuitive) ways, and that taking them into account may improve disease forecasting in coinfected populations.     

On the capacity of macroparasites to control insect populations

A graphical model of the population dynamics of macroparasites and their hosts is developed. Three principal means by which the parasites can be regulated are considered: reduction in host density as a result of parasite-induced host mortality, reduction in host density as a result of parasite-induced host sterility, and competition among parasites within multiply-infected hosts. The means by which parasites are regulated has a major effect on the degree to which they can depress host population densities. In particular, a parasite that sterilizes its host is expected to reduce host density more than one that causes an equivalent decline in host fitness through increased mortality. A special case of the model is developed for herbivorous insects that, in the absence of parasites, are limited by larval food resources. Parasites that are regulated via parasite-induced host sterility will control the insect populations below the level set by larval resources if the threshold host density for the parasites (N(T)) is less than the ratio of carrying capacity to net reproductive rate of the insects (K/R). Data are presented showing that all three means of parasite regulation, but especially parasite-induced host sterility, can operate in Howardula aoronymphium, a nematode parasite of mycophagous Drosophila flies. Data from a field cage experiment show that, if these nematodes are regulated primarily via reductions in host density due to this sterility, the parameters N(T), K, and R are such that Howardula is likely to play an important role in controlling Drosophila populations. However, this conclusion must be tempered by the fact that these nematodes also cause increased host mortality and experience within-host competition, making the conditions for parasite control of the flies more stringent.     

The population biology of parasite-induced changes in host behavior

The ability of parasites to change the behavior of infected hosts has been documented and reviewed by a number of different authors (Holmes and Bethel, 1972; Moore, 1984a). This review attempts to quantify the population dynamic consequences of this behavior by developing simple mathematical models for the most frequently recorded of such parasite life cycles. Although changes in the behavior of infected hosts do occur for pathogens with direct life cycles, they are most commonly recorded in the intermediate hosts of parasites with complex life cycles. All the changes in host behavior serve to increase rates of transmission of the parasites between hosts. In the simplest case the changes in behavior increase rates of contact between infected and susceptible conspecific hosts, whereas in the more complex cases fairly sophisticated manipulations of the host's behavioral repertory are achieved. Three topics are dealt with in some detail: (1) the behavior of the insect vectors of such diseases as malaria and trypanosomiasis; (2) the intermediate hosts of helminths whose behavior is affected in such a way as to make them more susceptible to predation by the definitive host in the life cycle; and (3) the behavior and fecundity of molluscs infected with asexually reproducing parasitic flatworms. In each case an expression is derived for R0, the basic reproductive rate of the parasite when first introduced into the population. This is used to determine the threshold numbers of definitive and intermediate hosts needed to maintain a population of the pathogen. In all cases, parasite-induced changes in host behavior tend to increase R0 and reduce the threshold number of hosts required to sustain the infection. The population dynamics of the interaction between parasites and their hosts are then explored using phase plane analyses. This suggests that both the parasite and intermediate host populations may show oscillatory patterns of abundance. When the density of the latter is low, parasite-induced changes in host behavior increase this tendency to oscillate. When intermediate host population densities are high, parasite population density is determined principally by interactions between the parasites and their definitive hosts, and changes in the behavior of intermediate hosts are less important in determining parasite density. Analysis of these models also suggests that both asexual reproduction of the parasite within a host and parasite-induced reduction in host fecundity may be stabilizing mechanisms when they occur in the intermediate hosts of parasite species with indirect life cycles.(ABSTRACT TRUNCATED AT 400 WORDS)     

Interactions between frequency-dependent and vertical transmission in host-parasite systems.

We investigate host-pathogen dynamics and conditions for coexistence in two models incorporating frequency-dependent horizontal transmission in conjunction with vertical transmission. The first model combines frequency-dependent and uniparental vertical transmission, while the second addresses parasites transmitted vertically via both parents. For the first model, we ask how the addition of vertical transmission changes the coexistence criteria for parasites transmitted by a frequency-dependent horizontal route, and show that vertical transmission significantly broadens the conditions for parasite invasion. Host-parasite coexistence is further affected by the form of density-dependent host regulation. Numerical analyses demonstrate that within a host population, a parasite strain with horizontal frequency-dependent transmission can be driven to extinction by a parasite strain that is additionally transmitted vertically for a wide range of parameters. Although models of asexual host populations predict that vertical transmission alone cannot maintain a parasite over time, analysis of our second model shows that vertical transmission via both male and female parents can maintain a parasite at a stable equilibrium. These results correspond with the frequent co-occurrence of vertical with sexual transmission in nature and suggest that these transmission modes can lead to host-pathogen coexistence for a wide range of systems involving hosts with high reproductive rates.     

Ecological conditions that favor the evolution of intermediate-virulence in an environmentally transmitted parasite

In this paper we develop and analyze several populaion-dynamic models of an environmentally transmitted symbiotic parasite infecting an isolated population of susceptible hosts. In our most basic model infection acts only to decrease the average lifetime of the infected host, parasites are only transmitted to uninfected hosts, there is no recovery from infection, and the rate of parasite transmission is an increasing function of the level of parasite virulence. It is shown that invasion of the parasite-free equilibrium cannot occur for virulence levels that are either too high or too low. We then incorporate a number of modifications to the model, among them the possibility that host fertility is reduced by infection, and that transmission rate depends additionally on susceptible host density. It is shown that the essential nature of the conditions for invasion are preserved. Thus, natural selection for intermediate virulence is a generic property of a broad class of population models.     

From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions

In most host-parasite systems, variation in parasite burden among hosts drives transmission dynamics. Heavily infected individuals introduce disproportionate numbers of infective stages into host populations or surrounding environments, causing sharp increases in frequency of infection. Parasite aggregation within host populations may result from variation among hosts in exposure to infective propagules and probability of subsequent establishment of parasites in the host. This is because individual host heterogeneities contribute to a pattern of parasite overdispersion that emerges at the population level. We quantified relative roles of host exposure and parasite establishment in producing variation in parasite burdens, to predict which hosts are more likely to bear heavy burdens, using big brown bats (Eptesicus fuscus) and their helminths as a model system. We captured bats from seven colonies in Michigan and Indiana, USA, assessed their helminth burdens, and collected data on intrinsic and extrinsic variables related to exposure, establishment, or both. Digenetic trematodes had the highest prevalence and mean abundance while cestodes and nematodes had much lower prevalence and mean abundance. Structural equation modeling revealed that best-fitting models to explain variations in parasite burden included genetic heterozygosity and immunocompetence as well as distance to the nearest water source and the year of host capture. Thus, both differential host exposure and differential parasite establishment significantly influence heterogeneous helminth burdens, thus driving population-level patterns of parasite aggregation.     

An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence

Epidemiological models predict a positive relationship between host population density and abundance of macroparasites. Here I lest these by a comparative study. I used data on communities of four groups of parasites inhabiting the gastrointestinal tract of mammals, nematodes of the orders Oxyurida. Ascarida. Enoplida and Spirurida. respectively. The data came from 44 mammalian species and represent examination of 16886 individual hosts. I studied average prevalence of all nematodes within an order in a host species, a measure of community level abundance, and considered the potential confounding effects of host body weight, fecundity, age at maturity and diet. Host population density was positively correlated with parasite prevalence within the order Oxyurida, where all species have direct life cycles. Considering the effects of other variables did not change this. This supports the assumption that parasite transmission rate generally is a positive function of host population density_: It also strengthens the hypothesis that host densities generally act as important determinants of species richness among directly transmitted parasites and suggests that negative influence of such parasites on host population growth rate increase with increasing host population density among host species. Within the other three nematode orders, where a substantial number of the species have indirect life cycles, no relationships between prevalence and host population density were seen, Again. considering the effects of other variables did not affect this conclusion. This suggests that host population density is a poor predictor of species richness of indirectly transmitted parasites and that effects of such parasites on host population dynamics do not scale with host densities among species of hosts.     

Can parasites synchronise the population fluctuations of sympatric tetraonids? –examining some minimum conditions

Sympatric populations of tetraonid birds tend to fluctuate in synchrony, at least on local scales. If shared parasites among sympatric populations of different tetraonid species are to operate as a local, synchronizing factor for population fluctuations at least two conditions should be met: i) the host species should share the same (or similar) parasite species, and ii) geographical location should contribute significantly more to the variation in the parasite species composition and abundance than differences among host species. We examined these conditions among subpopulations of sympatric willow ptarmigan and rock ptarmigan and found that host species shared a common pool of parasite species, and geographic location was more important than host species in determining parasite abundance across locations. There was no time lag between density oscillations in the two hosts, suggesting a symmetrical pattern of transmission and maintenance of parasites within habitats governed by the density of hosts and the environment. These findings are consistent with the idea that parasites may play a role in generating synchronous density fluctuations, but large scale experiments are needed to verify this hypothesis.     

Effectively vertical transmission of a Drosophila‐parasitic nematode: mechanism and consequences

1. Long‐term control of insects by parasites is possible only if the parasite populations persist. Because parasite transmission rate depends on host density, parasite populations may go extinct during periods of low host density. Vertical transmission of parasites, however, is independent of host density and may therefore provide a demographic bridge through times when their insect hosts are rare. 2. The nematode Howardula aoronymphium, which parasitises mycophagous species of Drosophila, can experience both horizontal and effectively vertical transmission, relative rates of which depend, in theory at least, on the density of hosts at breeding sites. 3. A nine‐generation experiment was carried out in which nematodes were transmitted either exclusively vertically or primarily horizontally. This experiment revealed that these parasites can persist and exhibit positive population growth even when there is only vertical transmission. 4. Assays at the end of the experiment revealed that the vertically transmitted nematodes had suffered no inbreeding depression and that they were similar to the horizontally transmitted nematodes in terms of virulence, infectivity, within‐host growth rate, and fecundity. Thus, vertical transmission of H. aoronymphium did not appear to compromise the ability of these parasites to control Drosophila populations.     

Come with me if you want to live: sympatric parasites follow different transmission routes through aquatic host communities

Community composition, including the relative density of each host species, plays a vital role in the transmission of parasites or disease in freshwater ecosystems. Whereas some host species can effectively transmit parasites, others can act as dead ends (non-viable transmission routes), accumulating large numbers of parasites throughout their life, thus becoming important sinks for parasite populations. Although population sinks have been identified in certain host-parasite systems, robust field estimates of the proportions of parasites that are lost to these hosts are lacking. Here, we quantified the distribution of encysted larval hairworms (phylum Nematomorpha), common parasites in lotic ecosystems, in two subalpine stream communities of New Zealand. With parasite and host population densities calculated per m², we identified which host species most likely contributed to the transmission of three sympatric hairworm morphotypes identified in both streams, and which species acted as population sinks. We also tested for seasonal patterns and peaks in the abundance of each morphotype in the two communities over the sampling season. Finally, we tested whether hosts emerging from the streams had comparable abundances of hairworm morphotypes throughout the sampling period. For each morphotype, different key sets of host species harboured more hairworms on average (abundance) than others, depending on the stream. For one morphotype in particular, two species of hosts were found to be important population sinks that inhibited over a third of these parasites from completing their life cycle. We also observed a clear peak in abundance for another hairworm morphotype during summer. Our data suggest that hosts emerging from the streams matched their aquatic counterparts with respect to hairworm abundance, indicating no infection-dependent reduction in emergence success. Our findings suggest that, depending on relative community composition, sympatric parasites follow different host transmission pathways, some of which lead to dead ends that potentially impact overall infection dynamics. In turn, this information can help us understand the spread or emergence of disease in both freshwater and terrestrial environments, since hairworms infect terrestrial arthropods to complete their life cycle.     

Condition-dependent expression of virulence in a trypanosome infecting bumblebees

Parasite virulence affects both the temporal dynamics of host-parasite relationships and the degree to which parasites regulate host populations. If hosts can compensate for parasitism, then parasites may exhibit condition-dependent virulence, with high virulence being seen only when the host is under conditions of stress. Despite their usually low level of virulence, theory suggests that such parasites may still affect host population dynamics. We tested whether a trypanosome intestinal parasite of bumblebees, Crithidia bombi , expresses condition-dependent virulence. Hosts were infected with the parasite and then kept under either favourable or starvation (stressed) conditions. Under favourable conditions the infection caused no mortality, while when hosts were starved the infection increased the host mortality rate by 50%. In addition, we found a parasite-related change in host resource allocation patterns. Infected bees invested relatively more resources into their fat body and less into their reproductive system than did non-infected bees. Whether this reallocation is parasite-driven, to enhance transmission, or a host-response to parasitism, remains unknown.     

Temporal patterns of genetic variation for resistance and infectivity in a Daphnia-microparasite system

Theoretical studies have indicated that the population genetics of host-parasite interactions may be highly dynamic. with parasites perpetually adapting to common host genotypes and hosts evolving resistance to common parasite genotypes. The present study examined temporal variation in resistance of hosts and infectivity of parasites within three populations of Daphnia magna infected with the sterilizing bacterium Pasteuria ramosa. Parasite isolates and host clones were collected in each of two years (1997, 1998) from one population; in two other populations, hosts were collected from both years, but parasites from only the first year. We then performed infection experiments (separately for each population) that exposed hosts to parasites from the same year or made combinations involving hosts and parasites from different years. In two populations, patterns were consistent with the evolution of host resistance: either infectivity or the speed with which parasites sterilized hosts declined from 1997 to 1998. In another population, infectivity, virulence, and parasite spore production did not vary among host-year or parasite-year. For this population, we also detected strong within-population genetic variation for resistance. Thus, in this case, genetic variability for fitness-related traits apparently did not translate into evolutionary change. We discuss a number of reasons why genetic change may not occur as expected in parasite-host systems, including negative correlations between resistance and other traits, gene flow, or that the dynamic process itself may obscure the detection of gene frequency changes.     

Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals

Epidemiological theory predicts positive correlations between host population density or body mass and species richness among parasite communities. Here I test these predictions by a comparative study of communities of directly transmitted mammalian parasites, gastrointestinal strongylid nematodes. I use data from 45 species of mammals, representing examination of 17 200 individual hosts. The variable studied was the average number of gastrointestinal strongylid nematode species per host population, and three different methods were used to obtain estimates of parasite species richness that are unbiased by number of host individuals examined. Analyses were done using the phylogenetically independent contrast method. Host population density and parasite species richness were strongly positively correlated when the effects of host body weight had been controlled for. Controlling for other variables did not change this, and the relationship was found regardless of method used to correct for uneven sampling effort among host species. A positive relationship between parasite species richness and host body weight was also found, but the effect of host densities had to be controlled for to see this. These relationships between host traits and species richness of directly transmitted parasites are stronger than patterns found using data on indirectly transmitted mammalian parasites, and suggests that links between host traits and parasite species richness are stronger than previously suggested. The results are consistent with parasite species richness being positively linked to pathogen transmission rates and reductions in transmission rates possibly increasing extinction probabilities in parasite populations. The results also suggest that parasites may exert a cost of increases in rate of population energy usage, and thus show that pathogens may be important in generating independence between body mass and rate of population energy usage among host species.     

Parasite diversity declines with host evolutionary distinctiveness: A global analysis of carnivores

Evolutionarily distinctive host lineages might harbor fewer parasite species because they have fewer opportunities for parasite sharing than hosts having extant close relatives, or because diverse parasite assemblages promote host diversification. We evaluate these hypotheses using data from 930 species of parasites reported to infect free‐living carnivores. We applied nonparametric richness estimators to estimate parasite diversity among well‐sampled carnivore species and assessed how well host evolutionary distinctiveness, relative to other biological and environmental factors, explained variation in estimated parasite diversity. Species richness estimates indicate that the current published literature captures less than 50% of the true parasite diversity for most carnivores. Parasite species richness declined with evolutionary distinctiveness of carnivore hosts (i.e., length of terminal ranches of the phylogeny) and increased with host species body mass and geographic range area. We found no support for the hypothesis that hosts from more diverse lineages support a higher number of generalist parasites, but we did find evidence that parasite assemblages might have driven host lineage diversification through mechanisms linked to sexual selection. Collectively, this work provides strong support for host evolutionary history being an essential predictor of parasite diversity, and offers a simple model for predicting parasite diversity in understudied carnivore species.     

Effects of resource availability and social aggregation on the species richness of raccoon endoparasite infracommunities

Within populations the contact rate of hosts and infectious parasites is mediated by the interactions of resource availability, host density, and host behavior. Fluctuations in host density can result in the loss or extinction of a parasite population as contact rates between parasites and susceptible individuals drop below thresholds of parasite population persistence. Less understood is how changes in resources and the behavioral ecology of host populations affect parasites. We used food provisioning to experimentally assess the effects of resource availability and of inducing host aggregation on the endoparasite community of free‐ranging raccoons. Twelve independent raccoon populations were subjected to differential resource provisioning for two years: a clumped food distribution to aggregate hosts (n = 5 populations), a dispersed food distribution to add food without aggregating hosts (n = 3), and a no food treatment (n = 4). Remote cameras indicated that aggregation sizes were three to four times greater in aggregated versus non‐aggregated populations. We considered endoparasites with direct and indirect life cycles separately and determined the best‐fit models of parasite species richness in relation to host aggregation, food supplements, and host age and sex. Social aggregation had a negligible impact on the species richness of directly or indirectly transmitted parasites. However, food additions decreased the number of indirectly transmitted parasite species by 35% in the oldest age classes. These results suggest that while resource availability can influence the transmission of indirectly transmitted parasites, an examination of additional factors will be necessary to understand the role of host contact and factors that shape the community structure of endoparasites in natural environments.