Phoretic Poecilochirus mites specialize on their burying beetle hosts

Recurring species interactions can cause species to adapt to each other. Specialization will increase the fitness of symbionts in the coevolved association but may reduce the flexibility of symbiont choice as it will often decrease fitness in interactions with other than the main symbiont species. We analyzed the fitness interactions between a complex of two cryptic mite species and their sympatric burying beetle hosts in a European population. Poecilochirus mites (Mesostigmata, Parasitidae) are phoretic on burying beetles and reproduce alongside beetles, while these care for their offspring at vertebrate carcasses. While Poecilochirus carabi is typically found on Nicrophorus vespilloides beetles, P. necrophori is associated with N. vespillo. It has long been known that the mites discriminate between the two beetle species, but the fitness consequences of this choice remained unknown. We experimentally associated both mite species with both beetle species and found that mite fitness suffered when mites reproduced alongside a nonpreferred host. In turn, there is evidence that one of the beetle species is better able to cope with the mite species they are typically associated with. The overall fitness effect of mites on beetles was negative in our laboratory experiments. The Poecilochirus mites studied here are thus specialized competitors or parasites of burying beetles.     

Review. When to leave the brood chamber? Routes of dispersal in mites associated with burying beetles

Most nests of brood-caring insects are colonized by a rich community of mite species. Since these nests are ephemeral and scattered in space, phoresy is the principal mode of dispersal in mites specializing on insect nests. Often the mites will arrive on the nest-founding insect, reproduce in the nest and their offspring will disperse on the insect's offspring. A literature review shows that mites reproducing in the underground brood chambers of burying beetles use alternative routes for dispersal. For example, the phoretic instars of Poecilochirus spp. (Mesostigmata: Parasitidae) disperse early by attaching to the parent beetles. Outside the brood chamber, the mites switch host at carcasses and pheromone-emitting male beetles, where juvenile and mature burying beetles of several species congregate. Because they preferably switch to beetles that are reproductively active and use all species of burying beetles within their ranges, they have a good chance of arriving in a new brood chamber. Other mite associates of burying beetles (Alliphis necrophilus and Uropodina) disperse from the brood chamber on the beetle offspring. We suggest that these mites forgo the possible time gain of dispersing early on the parent beetles because their mode of attachment precludes host switching. Their phoretic instars, once attached, have to stay on their host and so only dispersing on the beetle offspring guarantees that they are present on reproducing burying beetles of the next season. The mites associated with burying beetles providean example of multiple solutions to one life history problem – how to find a new brood chamber for reproduction. Mites that have mobile phoretic instars disperse on the parent beetles and try to arrive in the next brood chamber by host switching. They are independent of the generation cycle of a single host and several generations of mites per host generation are possible. Mites that are constrained by their mode of attachment disperse on the beetle offspring and wait until their host becomes mature and reproduces. By doing this they synchronize their generation time with the generation time of their host species. Exp Appl Acarol 22: 621–631 © 1998 Kluwer Academic Publishers     

Host–parasite interactions and vectors in the barn swallow in relation to climate change

Recent climate change has affected the phenology of numerous species, and such differential changes may affect host–parasite interactions. Using information on vectors (louseflies, mosquitoes, blackflies) and parasites (tropical fowl mite Ornithonyssus bursa, the lousefly Ornithomyia avicularia, a chewing louse Brueelia sp., two species of feather mites Trouessartia crucifera and Trouessartia appendiculata, and two species of blood parasites Leucozytozoon whitworthi and Haemoproteus prognei) of the barn swallow Hirundo rustica collected during 1971–2008, I analyzed temporal changes in emergence and abundance, relationships with climatic conditions, and changes in the fitness impact of parasites on their hosts. Temperature and rainfall during the summer breeding season of the host increased during the study. The intensity of infestation by mites decreased, but increased for the lousefly during 1982–2008. The prevalence of two species of blood parasites increased during 1988–2008. The timing of first mass emergence of mosquitoes and blackflies advanced. These temporal changes in phenology and abundance of parasites and vectors could be linked to changes in temperature, but less so to changes in precipitation. Parasites had fitness consequences for hosts because intensity of the mite and the chewing louse was significantly associated with delayed breeding of the host, while a greater abundance of feather mites was associated with earlier breeding. Reproductive success of the host decreased with increasing abundance of the chewing louse. The temporal decrease in mite abundance was associated with advanced breeding of the host, while the increase in abundance of the lousefly was associated with earlier breeding. Virulence by the tropical fowl mite decreased with increasing temperature, independent of confounding factors. These findings suggest that climate change affects parasite species differently, hence altering the composition of the parasite community, and that climate change causes changes in the virulence of parasites. Because the changing phenology of different species of parasites had both positive and negative effects on their hosts, and because the abundance of some parasites increased, while that of other decreased, there was no consistent temporal change in host fitness during 1971–2008.     

EFFECTS OF A HAEMATOPHAGOUS MITE ON THE BARN SWALLOW (HIRUNDO RUSTICA): A TEST OF THE HAMILTON AND ZUK HYPOTHESIS

I tested three assumptions of the Hamilton and Zuk hypothesis (1982), which suggests that the extravagant male plumage of many bird species allows females to choose mates that are resistant to the parasites exploiting the host population at a given time. By choosing such males as mates, females will rear offspring carrying the genes for resistance. I tested three necessary conditions for the Hamilton and Zuk model: (1) whether parasites affect the fitness of their hosts; (2) whether there is heritable variation in parasite resistance, and (3) whether the expression of the sexual ornament varies with parasite burden. The haematophagous mite Ornithonyssus bursa (Macronyssidae, Gamasida) sucks blood from their Barn Swallow (Hirundo rustica) hosts. Experimental manipulation of mite loads and partial cross-fostering experiments on Barn Swallows, where half of the nestlings in the brood were exchanged with nestlings from another nest, shows that parasite burdens and origin, but not rearing conditions, of Bam Swallow nestlings, affected their adult tarsus length and maximum body weight shortly before fledging. Mite loads of adult Barn Swallows at spring arrival were more similar to mite loads of their own offspring, whether reared in their own or in foster nests inoculated with mites, than to loads of foster offspring. Parent Barn Swallows with long tail ornaments had offspring with smaller mite loads in the partial cross-fostering experiments. The amount of increase in male tail ornaments from one year to another was negatively related to experimentally manipulated mite loads of Barn Swallow nests during the preceding breeding season. In conclusion, the three assumptions of the hypothesis were supported by the experimental tests.     

Of mice and worms: are co-infections with unrelated parasite strains more damaging to definitive hosts?

Intraspecific competition between co-infecting parasites can influence the amount of virulence, or damage, they do to their host. Kin selection theory dictates that infections with related parasite individuals should have lower virulence than infections with unrelated individuals, because they benefit from inclusive fitness and increased host longevity. These predictions have been tested in a variety of microparasite systems, and in larval stage macroparasites within intermediate hosts, but the influence of adult macroparasite relatedness on virulence has not been investigated in definitive hosts. This study used the human parasite Schistosoma mansoni to determine whether definitive hosts infected with related parasites experience lower virulence than hosts infected with unrelated parasites, and to compare the results from intermediate host studies in this system. The presence of unrelated parasites in an infection decreased parasite infectivity, the ability of a parasite to infect a definitive host, and total worm establishment in hosts, impacting the less virulent parasite strain more severely. Unrelated parasite co-infections had similar virulence to the more virulent of the two parasite strains. We combine these findings with complementary studies of the intermediate snail host and describe trade-offs in virulence and selection within the life cycle. Damage to the host by the dominant strain was muted by the presence of a competitor in the intermediate host, but was largely unaffected in the definitive host. Our results in this host–parasite system suggest that unrelated infections may select for higher virulence in definitive hosts while selecting for lower virulence in intermediate hosts.     

Virulence reaction norms across a food gradient

Host-parasite interactions involve competition for nutritional resources between hosts and the parasites growing within them. Consuming part of a host's resources is one cause of a parasite's virulence, i.e. part of the fitness cost imposed on the host by the parasite. The influence of a host's nutritional conditions on the virulence of a parasite was experimentally tested using the mosquito Aedes aegypti and the microsporidian parasite Vavraia culicis. A condition-dependent expression of virulence was found and a positive relation between virulence and transmissibility was established. Spore production was positively influenced by host food availability, indicating that the parasite's within-host growth is limited by host condition. We also investigated how the fitness of each partner varied across the nutritional gradient and demonstrated that the sign of the correlation between host fitness and parasite fitness depended on the amount of nutritional resources available to the host.     

Survival and reproductive rate of mites in relation to resistance of their barn swallow hosts

Parasite resistance may act via a number of different mechanisms that regulate or control the survival and the reproductive rate of parasites. Observations and experiments were used to test for effects of host resistance on parasite survival and rate of reproduction. Natural levels of infestation of barn swallow Hirundo rustica nests by the tropical fowl mite Ornithonyssus bursa were positively related to brood size, inversely related to the length of the outermost tail feathers of male nest owners (a secondary sexual character) and affected by time of reproduction by the host. A mite inoculation experiment, in which 50 adult mites were introduced into nests during the laying period of the host, was used to test for differential survival and reproduction of mites as a function of host resistance. The relationship between survival and reproduction of parasites, male tail length and host resistance was investigated. There was a negative relationship between mite numbers per nest after fledging of nestlings and male tail length. This relationship was mainly caused by a reduction in the number of mites in the first and second nymph stage with increasing tail length of male hosts, implying a reduction in rate of reproduction of mites. The proportion of mites that had recently fed was inversely related to tail length of male hosts. The proportion of nymph stages was positively related to the proportion of mites that had recently had a blood meal. Parasite resistance of barn swallows to the tropical fowl mite thus appeared to act through increased mortality rate of adult and nymph stages of mites, and through reduced reproductive rates of mites on resistant hosts. This is the first study demonstating a direct relationship between fitness components of a parasite and the expression of a secondary sexual character of a host. Received: 11 January 2000 / Accepted: 22 March 2000     

Within-host Competition Does Not Select for Virulence in Malaria Parasites; Studies with Plasmodium yoelii

In endemic areas with high transmission intensities, malaria infections are very often composed of multiple genetically distinct strains of malaria parasites. It has been hypothesised that this leads to intra-host competition, in which parasite strains compete for resources such as space and nutrients. This competition may have repercussions for the host, the parasite, and the vector in terms of disease severity, vector fitness, and parasite transmission potential and fitness. It has also been argued that within-host competition could lead to selection for more virulent parasites. Here we use the rodent malaria parasite Plasmodium yoelii to assess the consequences of mixed strain infections on disease severity and parasite fitness. Three isogenic strains with dramatically different growth rates (and hence virulence) were maintained in mice in single infections or in mixed strain infections with a genetically distinct strain. We compared the virulence (defined as harm to the mammalian host) of mixed strain infections with that of single infections, and assessed whether competition impacted on parasite fitness, assessed by transmission potential. We found that mixed infections were associated with a higher degree of disease severity and a prolonged infection time. In the mixed infections, the strain with the slower growth rate was often responsible for the competitive exclusion of the faster growing strain, presumably through host immune-mediated mechanisms. Importantly, and in contrast to previous work conducted with Plasmodium chabaudi, we found no correlation between parasite virulence and transmission potential to mosquitoes, suggesting that within-host competition would not drive the evolution of parasite virulence in P. yoelii.     

Contrasting diversity dynamics of phoretic mites and beetles associated with vertebrate carrion

Carrion is an ephemeral and nutrient-rich resource that attracts a diverse array of arthropods as it decomposes. Carrion-associated mites often disperse between animal carcasses using phoresy, the transport of one species by another. Yet few studies have contrasted the dynamics of mite assemblages with other insect taxa present at carrion. We examined and compared the changes in abundance, species richness and composition of mite and beetle assemblages sampled at kangaroo carcasses in a grassy eucalypt woodland at four different times over a 6-month period. We found that the majority of mites were phoretic, with the mesostigmatid genera Uroseius (Uropodidae), Macrocheles (Macrochelidae) and Parasitus (Parasitidae) the most abundant taxa (excluding astigmatid mites). Abundance and richness patterns of mites and beetles were very different, with mites reaching peak abundance and richness at weeks 6 and 12, and beetles at weeks 1 and 6. Both mites and beetles showed clear successional patterns via changes in species presence and relative abundance. Our study shows that mesostigmatid mite assemblages have a delay in peak abundance and richness relative to beetle assemblages. This suggests that differences in dispersal and reproductive traits of arthropods may contribute to the contrasting diversity dynamics of carrion arthropod communities, and further highlights the role of carrion as a driver of diversity and heterogeneity in ecosystems.     

Fitness costs of phoretic nematodes in the burying beetle,Nicrophorus vespilloides

Nicrophorusvespilloides is a social beetle that rears its offspring on decomposing carrion. Wild beetles are frequently associated with two types of macrobial symbionts, mites, and nematodes. Although these organisms are believed to be phoretic commensals that harmlessly use beetles as a means of transfer between carcasses, the role of these symbionts on N. vespilloides fitness is poorly understood. Here, we show that nematodes have significant negative effects on beetle fitness across a range of worm densities and also quantify the density‐dependent transmission of worms between mating individuals and from parents to offspring. Using field‐caught beetles, we provide the first report of a new nematode symbiont in N. vespilloides, most closely related to Rhabditoides regina, and show that worm densities are highly variable across individuals isolated from nature but do not differ between males and females. Next, by inoculating mating females with increasing densities of nematodes, we show that worm infections significantly reduce brood size, larval survival, and larval mass, and also eliminate the trade‐off between brood size and larval mass. Finally, we show that nematodes are efficiently transmitted between mating individuals and from mothers to larvae, directly and indirectly via the carcass, and that worms persist through pupation. These results show that the phoretic nematode R. regina can be highly parasitic to burying beetles but can nevertheless persist because of efficient mechanisms of intersexual and intergenerational transmission. Phoretic species are exceptionally common and may cause significant harm to their hosts, even though they rely on these larger species for transmission to new resources. However, this harm may be inevitable and unavoidable if transmission of phoretic symbionts requires nematode proliferation. It will be important to determine the generality of our results for other phoretic associates of animals. It will equally be important to assess the fitness effects of phoretic species under changing resource conditions and in the field where diverse interspecific interactions may exacerbate or reduce the negative effects of phoresy.     

Differential host defense against multiple parasites in ants

Host–parasite interactions are ideal systems for the study of coevolutionary processes. Although infections with multiple parasite species are presumably common in nature, most studies focus on the interactions of a single host and a single parasite. To the best of our knowledge, we present here the first study on the dependency of parasite virulence and host resistance in a multiple parasite system. We evaluated whether the strength of host defense depends on the potential fitness cost of parasites in a system of two Southeast Asian army ant hosts and five parasitic staphylinid beetle species. The potential fitness costs of the parasites were evaluated by their predation behavior on host larvae in isolation experiments. The host defense was assessed by the ants’ aggressiveness towards parasitic beetle species in behavioral studies. We found clear differences among the beetle species in both host–parasite interactions. Particular beetle species attacked and killed the host larvae, while others did not. Importantly, the ants’ aggressiveness was significantly elevated against predatory beetle species, while non-predatory beetle species received almost no aggression. As a consequence of this defensive behavior, less costly parasites are more likely to achieve high levels of integration in the ant society. We conclude that the selection pressure on the host to evolve counter-defenses is higher for costly parasites and, thus, a hierarchical host defense strategy has evolved that depends on the parasites’ impact.     

Parallel effects of a B chromosome and a mite that decrease female fitness in the grasshopper Eyprepocnemis plorans

The effects of a genomic parasite (a B chromosome) and an ectoparasite (a mite) on the fitness of the host (the grasshopper Eyprepocnemis plorans) have been analysed in 60 experimental females. These two parasites differ in their infectious transmission mode. B chromosomes are vertically transmitted from host-parents to offspring, but mites are horizontally transmitted from one grasshopper to another within the same generation. The transmission mode can influence the virulence of these parasites, so that it should be expected that B chromosomes would be less virulent than mites. However, as mite transmission is linked to host mobility, some attenuation is also expected. Four egg pods were analysed from each female, the first two egg pods were laid after a mating and the remaining two were not preceded by a mating. The results show that B chromosomes severely decrease the proportion of eggs containing an embryo (egg fertility), mainly from the second egg pod onwards. Mites also decrease egg fertility but, in addition, they produced a decrease in the rate of embryo production over time (embryo productivity), which might be derived from both the fertility decrease and a slight delay in egg production. The analysis of the relative effect of both parasites suggests that they have a synergistic effect on embryo clutch size and egg fertility. Possible mechanisms for the observed effects are discussed.     

Conflict between parasites with different transmission strategies infecting an amphipod host

Competition between parasites within a host can influence the evolution of parasite virulence and host resistance, but few studies examine the effects of unrelated parasites with conflicting transmission strategies infecting the same host. Vertically transmitted (VT) parasites, transmitted from mother to offspring, are in conflict with virulent, horizontally transmitted (HT) parasites, because healthy hosts are necessary to maximize VT parasite fitness. Resolution of the conflict between these parasites should lead to the evolution of one of two strategies: avoidance, or sabotage of HT parasite virulence by the VT parasite. We investigated two co-infecting parasites in the amphipod host, Gammarus roeseli: VT microsporidia have little effect on host fitness, but acanthocephala modify host behaviour, increasing the probability that the amphipod is predated by the acanthocephalan's definitive host. We found evidence for sabotage: the behavioural manipulation induced by the Acanthocephala Polymorphus minutus was weaker in hosts also infected by the microsporidia Dictyocoela sp. (roeselum) compared to hosts infected by P. minutus alone. Such conflicts may explain a significant portion of the variation generally observed in behavioural measures, and since VT parasites are ubiquitous in invertebrates, often passing undetected, conflict via transmission may be of great importance in the study of host-parasite relationships.     

Adaptive population structure shifts in invasive parasitic mites,Varroa destructor

Comparative studies of genetic diversity and population structure can shed light on the ecological and evolutionary factors governing host–parasite interactions. Even though invasive parasites are considered of major biological importance, little is known about their adaptative potential when infesting the new hosts. Here, the genetic diversification of Varroa destructor, a novel parasite of Apis mellifera originating from Asia, was investigated using population genetics to determine how the genetic structure of the parasite changed in distinct European populations of its new host. To do so, mites infesting two categories of hosts in four European regions were compared: (a) adapted hosts surviving through means of natural selection, thereby expected to impose strong selective pressure on the mites, and (b) treated host populations, surviving mite infestations because acaricides are applied, therefore characterized by a relaxed selection imposed by the host on the mites. Significant genetic divergence was found across regions, partially reflecting the invasion pattern of V. destructor throughout Europe and indicating local adaptation of the mite to the host populations. Additionally, varying degrees of genotypic changes were found between mites from adapted and treated colonies. Altogether, these results indicate that V. destructor managed to overcome the genetic bottlenecks following its introduction in Europe and that host‐mediated selection fostered changes in the genetic structure of this mite at diverse geographic scales. These findings highlight the potential of parasites to adapt to their local host populations and confirm that adaptations developed within coevolutionary dynamics are a major determinant of population genetic changes.     

Behaviours of phoretic mites (Acari) associated with Ips pini and Ips grandicollis (Coleoptera: Curculionidae) during host‐tree colonization

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Selection for plasmid post-segregational killing depends on multiple infection: evidence for the selection of more virulent parasites through parasite-level competition

Is the virulence of parasites an outcome of optimized infection? Virulence has often been considered an inevitable consequence of parasite reproduction when the cost incurred by the parasite in reducing the fitness of its current host is offset by increased infection of new hosts. More recent models have focused on how competition occurring between parasites during co-infection might effect selection of virulence. For example, if co-infection was common, parasites with higher intrinsic growth rates might be selected, even at the expense of being optimally adapted to infect new hosts. If growth rate is positively correlated with virulence, then competition would select increased virulence. We tested these models using a plasmid-encoded virulence determinant. The virulence determinant did not contribute to the plasmid's reproduction within or between hosts. Despite this, virulent plasmids were more successful than avirulent derivatives during selection in an environment allowing within-host competition. To explain these findings we propose and test a model in which virulent parasites are selected by reducing the reproduction of competitors.     

Effect of Population Density and Female Body Size on Number and Size of Offspring in a Species with Size‐Dependent Contests over Resources

When size‐dependent contests over resources influence reproductive success, the trade‐off between number and size of offspring depends on the frequency of contests. Under these circumstances, clutch size should decrease and offspring size should increase as contests become more frequent. We tested these predictions with the burying beetle Nicrophorus pustulatus through manipulation of rearing densities. Burying beetles reproduce on small vertebrate carcasses, a rare but high quality food source for the larvae. Large beetles are more likely to win contests over carcasses and gain exclusive access to a carcass. The winner of a contest kills eggs and larvae already present on a carcass. As a result of the rarity of carcasses, burying beetles are unlikely to breed more than once. As predicted, brood size of N. pustulatus decreased with increasing rearing density. Despite a negative correlation between brood size and larval mass, larval mass did not increase with increasing rearing density. This may be due to the special biology of N. pustulatus which can use snake eggs for reproduction. Potentially larger supply of resources and generally small population densities of N. pustulatus may weaken selection on body size and thus the correlation between brood size and larval mass. As size‐dependent constraints can limit reproductive phenotypes, we examined whether female size influenced reproductive phenotype. Small females produced larger broods with smaller, but more variable, offspring than large females. Mechanical constraints of egg size seem an unlikely explanation for the differences because burying beetles can compensate for small egg size through parental care. Energetic constraints may impact small females because body mass and brood size of small females decreased with increasing density. Yet, at all density levels small females produced larger, not smaller, broods than large females. The larger and more variable broods of small females seem to be in agreement with a bet‐hedging strategy.     

Effects of tapeworm infection on male reproductive success and mating vigor in the red flour beetle,Tribolium castaneum

Parasites may exert negative effects on host survivorship and reproductive success. The effects of parasites on female host fitness have been well documented; however, the effects of parasites on the reproductive success of male hosts and particularly the underlying mechanisms that alter male fitness are not well understood. Previous studies demonstrated that infection by rat tapeworm (Hymenolepis diminuta) reduced the fitness of male red flour beetles (Tribolium castaneum) in an environment of female mate choice and strong male-male competition. The present study determined the role of female mate choice and male insemination capacity on observed fitness reduction of male beetles by the tapeworm parasites. We found that infected males showed reduced mating vigor and consequently inseminated fewer females than did uninfected males. Specifically, tapeworm infection reduced the number of offspring sired by a male by 14-22% even when male-male competition and female mate choice were absent. Further, the insemination capacity of males diminished by 30% because of infection. Female beetles did not discriminate against infected males in precopulatory mate choice experiments. Copulatory courtship, a determinant of postcopulatory female choice, was not significantly different between infected and uninfected males. Hence, we concluded that female beetles did not show either pre- or postcopulatory choice against tapeworm-infected males. Therefore, tapeworm-induced reduction in the reproductive success of male beetles possibly results from altered reproductive biology, such as lower mating vigor and decreased sperm quantity or quality.     

VIRULENCE AND COMPETITIVENESS: TESTING THE RELATIONSHIP DURING INTER‐ AND INTRASPECIFIC MIXED INFECTIONS

Understanding the reasons why different parasites cause different degrees of harm to their hosts is an important objective in evolutionary biology. One group of models predicts that if hosts are infected with more than one strain or species of parasite, then competition between the parasites will select for higher virulence. While this idea makes intuitive sense, empirical data to support it are rare and equivocal. We investigated the relationship between fitness and virulence during both inter‐ and intraspecific competition for a fungal parasite of insects, Metarhizium anisopliae. Contrary to theoretical expectations, competition favored parasite strains with either a lower or a higher virulence depending on the competitor: when in interspecific competition with an entomopathogenic nematode, Steinernema feltiae, less virulent strains of the fungus were more successful, but when competing against conspecific fungi, more virulent strains were better competitors. We suggest that the nature of competition (direct via toxin production when competing against the nematode, indirect via exploitation of the host when competing against conspecific fungal strains) determines the relationship between virulence and competitive ability.     

Interactions among bacterial strains and fluke genotypes shape virulence of co-infection

Most studies of virulence of infection focus on pairwise host–parasite interactions. However, hosts are almost universally co-infected by several parasite strains and/or genotypes of the same or different species. While theory predicts that co-infection favours more virulent parasite genotypes through intensified competition for host resources, knowledge of the effects of genotype by genotype (G × G) interactions between unrelated parasite species on virulence of co-infection is limited. Here, we tested such a relationship by challenging rainbow trout with replicated bacterial strains and fluke genotypes both singly and in all possible pairwise combinations. We found that virulence (host mortality) was higher in co-infections compared with single infections. Importantly, we also found that the overall virulence was dependent on the genetic identity of the co-infecting partners so that the outcome of co-infection could not be predicted from the respective virulence of single infections. Our results imply that G × G interactions among co-infecting parasites may significantly affect host health, add to variance in parasite fitness and thus influence evolutionary dynamics and ecology of disease in unexpected ways.