Persistence of host and parasite populations subject to experimental size-selective removal

Predators have the potential to limit the spread of pathogens not only by selecting infected prey but also by shaping prey demographics. We tested this idea with an epidemiological experiment in which we simulated variable levels of size-selective predation on zooplankton hosts and monitored the persistence of host and parasite populations. In the absence of simulated predation, the virulent protozoan Caullerya mesnili frequently drove its host Daphnia galeata to extinction. Uninfected control populations showed lower extinction rates and higher average densities than infected populations in the absence of simulated predation (all of the latter went extinct or remained infected). With a weak removal rate of the largest hosts, the proportion of populations in which the parasite drove the host to extinction decreased, while the number of populations in which the host persisted and the parasite went extinct increased. Host-parasite coexistence was also observed in some cases. With intermediate levels of removal, most of the parasite populations went extinct, while the host populations persisted. With an even higher removal rate, Daphnia were driven to extinction as well. Thus, variation in one factor, size-selective mortality, resulted in four different patterns of population dynamics. Our results highlight the potential role of predation in shaping the epidemiology and community structure of host-parasite systems.     

Effects of antagonistic coevolution on parasite‐mediated host coexistence

Parasites can promote diversity by mediating coexistence between a poorer and superior competitor, if the superior competitor is more susceptible to parasitism. However, hosts and parasites frequently undergo antagonistic coevolution. This process may result in the accumulation of pleiotropic fitness costs associated with host resistance, and could breakdown coexistence. We experimentally investigated parasite‐mediated coexistence of two genotypes of the bacterium Pseudomonas fluorescens, where one genotype underwent coevolution with a parasite (a virulent bacteriophage), whereas the other genotype was resistant to the evolving phages at all time points, but a poorer competitor. In the absence of phages, the resistant genotype was rapidly driven extinct in all populations. In the presence of the phages, the resistant genotype persisted in four of six populations and eventually reached higher frequencies than the sensitive genotype. The coevolving genotype showed a reduction in the growth rate, consistent with a cost of resistance, which may be responsible for a decline in its relative fitness. These results demonstrate that the stability of parasite‐mediated coexistence of resistant and susceptible species or genotypes is likely to be affected if parasites and susceptible hosts coevolve.     

The changing ecology of primate parasites: Insights from wild‐captive comparisons

Host movements, including migrations or range expansions, are known to influence parasite communities. Transitions to captivity—a rarely studied yet widespread human‐driven host movement—can also change parasite communities, in some cases leading to pathogen spillover among wildlife species, or between wildlife and human hosts. We compared parasite species richness between wild and captive populations of 22 primate species, including macro‐ (helminths and arthropods) and micro‐parasites (viruses, protozoa, bacteria, and fungi). We predicted that captive primates would have only a subset of their native parasite community, and would possess fewer parasites with complex life cycles requiring intermediate hosts or vectors. We further predicted that captive primates would have parasites transmitted by close contact and environmentally—including those shared with humans and other animals, such as commensals and pests. We found that the composition of primate parasite communities shifted in captive populations, especially because of turnover (parasites detected in captivity but not reported in the wild), but with some evidence of nestedness (holdovers from the wild). Because of the high degree of turnover, we found no significant difference in overall parasite richness between captive and wild primates. Vector‐borne parasites were less likely to be found in captivity, whereas parasites transmitted through either close or non‐close contact, including through fecal‐oral transmission, were more likely to be newly detected in captivity. These findings identify parasites that require monitoring in captivity and raise concerns about the introduction of novel parasites to potentially susceptible wildlife populations during reintroduction programs.     

Refugia and connectivity sustain amphibian metapopulations afflicted by disease

Metapopulation persistence in fragmented landscapes depends on habitat patches that can support resilient local populations and sufficient connectivity between patches. Yet epidemiological theory for metapopulations has largely overlooked the capacity of particular patches to act as refuges from disease, and has suggested that connectivity can undermine persistence. Here, we show that relatively warm and saline wetlands are environmental refuges from chytridiomycosis for an endangered Australian frog, and act jointly with connectivity to sustain frog metapopulations. We coupled models of microclimate and infection probability to map chytrid prevalence, and demonstrate a strong negative relationship between chytrid prevalence and the persistence of frog populations. Simulations confirm that frog metapopulations are likely to go extinct when they lack environmental refuges from disease and lose connectivity between patches. This study demonstrates that environmental heterogeneity can mediate host–pathogen interactions in fragmented landscapes, and provides evidence that connectivity principally supports host metapopulations afflicted by facultative pathogens.     

Intermediate fragmentation per se provides stable predator-prey metapopulation dynamics

The extent to which a landscape is fragmented affects persistence of predator-prey dynamics. Increasing fragmentation concomitantly imposes conditions that stabilise and destabilise metapopulations. For the first time, we explicitly assessed the hypothesis that intermediate levels provide optimal conditions for stability. We examine four structural changes arising from increased fragmentation: increased fragment number; decreased fragment size; increased connectedness (corridors scaled to fragment); increased fragment heterogeneity (based on connectedness). Using the model predator-prey system (Didinium-Paramecium) we support our hypothesis, by examining replicated metapopulations dynamics at five fragmentation levels. Although both species became extinct without fragmentation, prey survived at low and high levels, and both survived at intermediate levels. By examining time to extinction, maximum abundances, and population asynchrony we conclude that fragmentation produces structural heterogeneity (independent of environmental heterogeneity), which influences stability. Our analysis suggests why some theoretical, field and microcosm studies present conflicting views of fragmentation effects on population persistence.     

The dynamics of preferential host switching: Host phylogeny as a key predictor of parasite distribution*

Parasites often jump to and become established in a new host species. There is much evidence that the probability of such host shifts decreases with increasing phylogenetic distance between donor and recipient hosts, but the consequences of such preferential host switching remain little explored. We develop a computational model to investigate the dynamics of parasite host shifts in the presence of this phylogenetic distance effect. In this model, a clade of parasites evolves on an evolving clade of host species where parasites can cospeciate with their hosts, switch to new hosts, speciate within hosts or become extinct. Our model predicts that host phylogenies are major determinants of parasite distributions across trees. In particular, we predict that trees consisting of few large clades of host species and those with fast species turnover should harbor more parasites than trees with many small clades and those that diversify more slowly. Within trees, large clades are predicted to exhibit a higher fraction of infected species than small clades. We discuss our results in the light of recent cophylogenetic studies in a wide range of host–parasite systems.     

Collective defence portfolios of ant hosts shift with social parasite pressure

Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host''s nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.     

Stochastic environmental fluctuations drive epidemiology in experimental host–parasite metapopulations

Environmental fluctuations are important for parasite spread and persistence. However, the effects of the spatial and temporal structure of environmental fluctuations on host–parasite dynamics are not well understood. Temporal fluctuations can be random but positively autocorrelated, such that the environment is similar to the recent past (red noise), or random and uncorrelated with the past (white noise). We imposed red or white temporal temperature fluctuations on experimental metapopulations of Paramecium caudatum, experiencing an epidemic of the bacterial parasite Holospora undulata. Metapopulations (two subpopulations linked by migration) experienced fluctuations between stressful (5°C) and permissive (23°C) conditions following red or white temporal sequences. Spatial variation in temperature fluctuations was implemented by exposing subpopulations to the same (synchronous temperatures) or different (asynchronous temperatures) temporal sequences. Red noise, compared with white noise, enhanced parasite persistence. Despite this, red noise coupled with asynchronous temperatures allowed infected host populations to maintain sizes equivalent to uninfected populations. It is likely that this occurs because subpopulations in permissive conditions rescue declining subpopulations in stressful conditions. We show how patterns of temporal and spatial environmental fluctuations can impact parasite spread and host population abundance. We conclude that accurate prediction of parasite epidemics may require realistic models of environmental noise.     

Host sympatry and body size influence parasite straggling rate in a highly connected multihost,multiparasite system

Parasite lineages commonly diverge when host lineages diverge. However, when large clades of hosts and parasites are analyzed, some cases suggest host switching as another major diversification mechanism. The first step in host switching is the appearance of a parasite on an atypical host, or “straggling.” We analyze the conditions associated with straggling events. We use five species of colonially nesting seabirds from the Galapagos Archipelago and two genera of highly specific ectoparasitic lice to examine host switching. We use both genetic and morphological identification of lice, together with measurements of spatial distribution of hosts in mixed breeding colonies, to test: (1) effects of local host community composition on straggling parasite identity; (2) effects of relative host density within a mixed colony on straggling frequency and parasite species identity; and (3) how straggling rates are influenced by the specifics of louse attachment. Finally, we determine whether there is evidence of breeding in cases where straggling adult lice were found, which may indicate a shift from straggling to the initial stages of host switching. We analyzed more than 5,000 parasite individuals and found that only ~1% of lice could be considered stragglers, with ~5% of 436 host individuals having straggling parasites. We found that the presence of the typical host and recipient host in the same locality influenced straggling. Additionally, parasites most likely to be found on alternate hosts are those that are smaller than the typical parasite of that host, implying that the ability of lice to attach to the host might limit host switching. Given that lice generally follow Harrison's rule, with larger parasites on larger hosts, parasites infecting the larger host species are less likely to successfully colonize smaller host species. Moreover, our study supports the general perception that successful colonization of a novel host is extremely rare, as we found only one nymph of a straggling species, which may indicate successful reproduction.     

Infectious disease in animal metapopulations: the importance of environmental transmission

Motivated by an array of infectious diseases that threaten wildlife populations, a simple metapopulation model (subpopulations connected by animal movement) is developed, which allows for both movement-based and environmental transmission. The model demonstrates that for a range of plausible parameterizations of environmental transmission, increased movement rate of animals between discrete habitats can lead to a decrease in the overall proportion of sites that are occupied. This can limit the ability of the rescue effect to ensure locally extinct populations become recolonized and can drive metapopulations down in size so that extinction by mechanisms other than disease may become more likely. It further highlights that, in the context of environmental transmission, the environmental persistence time of pathogens and the probability of acquiring infection by environmental transmission can affect host metapopulations both qualitatively and quantitatively. Additional spillover sources of infection from alternate reservoir hosts are also included in the model and a synthesis of all three types of transmission, acting alone or in combination, is performed revealing that movement-based transmission is the only necessary condition for a decline in the proportion of occupied sites with increasing movement rate, but that the presence of other types of transmission can reverse this qualitative result. By including the previously neglected role of environmental transmission, this work contributes to the general discussion of when dispersal by wild animals is beneficial or detrimental to populations experiencing infectious disease.     

Do threatened hosts have fewer parasites? A comparative study in primates

1. Parasites and infectious diseases have become a major concern in conservation biology, in part because they can trigger or accelerate species or population declines. Focusing on primates as a well-studied host clade, we tested whether the species richness and prevalence of parasites differed between threatened and non-threatened host species. 2. We collated data on 386 species of parasites (including viruses, bacteria, protozoa, helminths and arthropods) reported to infect wild populations of 36 threatened and 81 non-threatened primate species. Analyses controlled for uneven sampling effort and host phylogeny. 3. Results showed that total parasite species richness was lower among threatened primates, supporting the prediction that small, isolated host populations harbour fewer parasite species. This trend was consistent across three major parasite groups found in primates (helminths, protozoa and viruses). Counter to our predictions, patterns of parasite species richness were independent of parasite transmission mode and the degree of host specificity. 4. We also examined the prevalence of selected parasite genera among primate sister-taxa that differed in their ranked threat categories, but found no significant differences in prevalence between threatened and non-threatened hosts. 5. This study is the first to demonstrate differences in parasite richness relative to host threat status. Results indicate that human activities and host characteristics that increase the extinction risk of wild animal species may lead simultaneously to the loss of parasites. Lower average parasite richness in threatened host taxa also points to the need for a better understanding of the cascading effects of host biodiversity loss for affiliated parasite species.     

VARIATION BETWEEN POPULATIONS AND LOCAL ADAPTATION IN ACANTHOCEPHALAN‐INDUCED PARASITE MANIPULATION

Many trophically transmitted parasites manipulate their intermediate host phenotype, resulting in higher transmission to the final host. However, it is not known if manipulation is a fixed adaptation of the parasite or a dynamic process upon which selection still acts. In particular, local adaptation has never been tested in manipulating parasites. In this study, using experimental infections between six populations of the acanthocephalan parasite Pomphorhynchus laevis and its amphipod host Gammarus pulex, we investigated whether a manipulative parasite may be locally adapted to its host. We compared adaptation patterns for infectivity and manipulative ability. We first found a negative effect of all parasite infections on host survival. Both parasite and host origins influenced infection success. We found a tendency for higher infectivity in sympatric versus allopatric combinations, but detailed analyses revealed significant differences for two populations only. Conversely, no pattern of local adaptation was found for behavioral manipulation, but manipulation ability varied among parasite origins. This suggests that parasites may adapt their investment in behavioral manipulation according to some of their host's characteristics. In addition, all naturally infected host populations were less sensitive to parasite manipulation compared to a naive host population, suggesting that hosts may evolve a general resistance to manipulation.     

Parasite diversity drives rapid host dynamics and evolution of resistance in a bacteria‐phage system

Host–parasite evolutionary interactions are typically considered in a pairwise species framework. However, natural infections frequently involve multiple parasites. Altering parasite diversity alters ecological and evolutionary dynamics as parasites compete and hosts resist multiple infection. We investigated the effects of parasite diversity on host–parasite population dynamics and evolution using the pathogen Pseudomonas aeruginosa and five lytic bacteriophage parasites. To manipulate parasite diversity, bacterial populations were exposed for 24 hours to either phage monocultures or diverse communities containing up to five phages. Phage communities suppressed host populations more rapidly but also showed reduced phage density, likely due to interphage competition. The evolution of resistance allowed rapid bacterial recovery that was greater in magnitude with increases in phage diversity. We observed no difference in the extent of resistance with increased parasite diversity, but there was a profound impact on the specificity of resistance; specialized resistance evolved to monocultures through mutations in a diverse set of genes. In summary, we demonstrate that parasite diversity has rapid effects on host–parasite population dynamics and evolution by selecting for different resistance mutations and affecting the magnitude of bacterial suppression and recovery. Finally, we discuss the implications of phage diversity for their use as biological control agents.     

Local transmission processes and disease-driven host extinctions

Classic infectious disease theory assumes that transmission depends on either the global density of the parasite (for directly transmitted diseases) or its global frequency (for sexually transmitted diseases). One important implication of this dichotomy is that parasite-driven host extinction is only predicted under frequency-dependent transmission. However, transmission is fundamentally a local process between individuals that is determined by their and/or their vector’s behaviour. We examine the implications of local transmission processes to the likelihood of disease-driven host extinction. Local density-dependent transmission can lead to parasite-driven extinction, but extinction is more likely under local frequency-dependent transmission and much more likely when there is active local searching behaviour. Density-dependent directly transmitted diseases spread locally can therefore lead to deterministic host extinction, but locally frequency-dependent passive vector-borne diseases are more likely to cause extinctions. However, it is active searching behaviour either by a vector or between sexual partners that is most likely to cause the host to go extinct. Our work emphasises that local processes are essential in determining parasite-driven extinctions, and the role of parasites in the extinction of rare species may have been underplayed due to the classic assumption of global density-dependent transmission.     

Genetic diversity, parasite prevalence and immunity in wild bumblebees

Inbreeding and a consequent loss of genetic diversity threaten small, isolated populations. One mechanism by which genetically impoverished populations may become extinct is through decreased immunocompetence and higher susceptibility to parasites. Here, we investigate the relationship between immunity and inbreeding in bumblebees, using Hebridean island populations of Bombus muscorum. We sampled nine populations and recorded parasite prevalence and measured two aspects of immunity: the encapsulation response and levels of phenoloxidase (PO). We found that prevalence of the gut parasite Crithidia bombi was higher in populations with lower genetic diversity. Neither measure of immune activity was correlated with genetic diversity. However, levels of PO declined with age and were also negatively correlated with parasite abundance. Our results suggest that as insect populations lose heterozygosity, the impact of parasitism will increase, pushing threatened populations closer to extinction.     

The impact of host genetic diversity on virus evolution and emergence

Accumulating evidence indicates that biodiversity has an important impact on parasite evolution and emergence. The vast majority of studies in this area have only considered the diversity of species within an environment as an overall measure of biodiversity, overlooking the role of genetic diversity within a particular host species. Although theoretical models propose that host genetic diversity in part shapes that of the infecting parasite population, and hence modulates the risk of parasite emergence, this effect has seldom been tested empirically. Using Rabies virus (RABV) as a model parasite, we provide evidence that greater host genetic diversity increases both parasite genetic diversity and the likelihood of a host being a donor in RABV cross‐species transmission events. We conclude that host genetic diversity may be an important determinant of parasite evolution and emergence.     

Parasite spread in experimental metapopulations: resistance,tolerance and host competence

Host competence, defined as the likelihood that a host will transmit infection, may be affected by an individual's resistance to infection and its ability to withstand damage caused by infection (tolerance). Host competence may therefore be one of the most important factors to impact host–parasite dynamics, yet the relationships among resistance, tolerance and competence are poorly understood. The objective of the present study was to determine whether individual host resistance (ability to resist or minimize infection) and/or tolerance (ability to withstand or minimize reduction in fitness due to infection) contributed to the competence (ability to spread infection) of hosts using guppies infected with the ectoparasite, Gyrodactylus turnbulli. This individual-fish level analysis used data collected from a previous metapopulation experiment that had tracked host–parasite dynamics at the metapopulation scale using individually marked guppies that were moved among experimental tanks within replicate metapopulations. Fish tolerance was measured as the residual from a fish's expected survival post-infection for a given parasite burden. Fish resistance was measured as the peak parasite load (– log-transformed). Host competence was measured as the incidence (number of new infections over two days after the arrival of a fish to a tank) weighted by the density of available uninfected fish in the tank. In contrast to the assumption of a trade-off between resistance and tolerance, individual fish tolerance and resistance were both negatively associated with competence. Connectivity (the number of fish with which an individual came into contact) was not associated with competence. Our results indicate that resistance and tolerance are both important to disease spread. These findings highlight the importance of understanding how individual defence against parasites may contribute to its competence as a host, and therefore impact metapopulation-level dynamics.     

Detecting local adaptation in a natural plant-pathogen metapopulation: a laboratory vs. field transplant approach

Antagonistic coevolution between hosts and parasites in spatially structured populations can result in local adaptation of parasites. Traditionally parasite local adaptation has been investigated in field transplant experiments or in the laboratory under a constant environment. Despite the conceptual importance of local adaptation in studies of (co)evolution, to date no study has provided a comparative analysis of these two methods. Here, using information on pathogen population dynamics, I tested local adaptation of the specialist phytopathogen, Podosphaera plantaginis, to its host, Plantago lanceolata at three different spatial scales: sympatric host population, sympatric host metapopulation and allopatric host metapopulations. The experiment was carried out as a field transplant experiment with greenhouse-reared host plants from these three different origins introduced into four pathogen populations. In contrast to results of an earlier study performed with these same host and parasite populations under laboratory conditions, I did not find any evidence for parasite local adaptation. For interactions governed by strain-specific resistance, field studies may not be sensitive enough to detect mean parasite population virulence. Given that parasite transmission potential may be mediated by the abiotic environment and genotype-by-environment interactions, I suggest that relevant environmental variation should be incorporated into laboratory studies of parasite local adaptation.     

Population dynamics under parasitic sex ratio distortion.

We analyse the population dynamic effects of sex ratio distortion by vertically transmitted, feminizing parasites. We show that, for diploid hosts, sex ratio distortion may lead to extinction as males become too rare to maintain the host population through reproduction. Feminizers can magnify Allee effects, broadening the range of conditions leading to extinction of small populations. Depending on male mating constraints and strength of density dependence, feminizers may either increase or decrease the equilibrium host density. Under conditions leading to deterministic host extinction, stochastic elimination of the parasite may allow the host population to recover. Hence, infection by parasitic sex ratio distorters may be transient in finite populations. We consider the implications of this process for parasite prevalence, host population regulation, and sex ratio evolution.     

Synergistic effects of an extreme weather event and habitat fragmentation on a specialised insect herbivore

Habitat fragmentation is considered to be one of the main causes of population decline and species extinction worldwide. Furthermore, habitat fragmentation can decrease the ability of populations to resist and to recover from environmental disturbances such as extreme weather events, which are expected to occur at an increasing rate as a result of climate change. In this study, we investigated how calcareous grassland fragmentation affected the impact of the climatically extreme summer of 2003 on egg deposition rates, population size variation and survival of the blue butterfly Cupido minimus, a specialist herbivore of Anthyllis vulneraria. Immediately after the 2003 summer heat wave, populations of the host plant declined in size; this was paralleled with decreases in population size of the herbivore and altered egg deposition rates. In 2006 at the end of the monitoring period, however, most A. vulneraria populations had recovered and only one population went extinct. In contrast, several butterfly populations had gone extinct between 2003 and 2006. Extinction probability was significantly related to initial population size, with small populations having a higher risk of extinction than large populations. These results support the prediction that species of higher trophic levels are more susceptible to extinction due to habitat fragmentation and severe disturbances.