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PubMed2003

Nestling discrimination without recognition: a possible defence mechanism for hosts towards cuckoo parasitism?

One of the great evolutionary puzzles is why hosts of parasitic birds discriminate finely against alien eggs, but almost never discriminate against parasitic chicks. A theoretical model has shown that an adaptive host response to alien eggs can be based on learning. However, learned nestling discrimination is too costly to be favoured by selection in hosts of evicting parasites, such as the European cuckoo (Cuculus canorus). Indeed, parasitic chick rejection has never been reported for any European cuckoo host species. As learned nestling discrimination is maladaptive, one can expect that a viable alternative for hosts would be to use discrimination mechanisms not involving learning and/or recognition. We suggest that hosts may starve and desert cuckoo chicks that require higher amounts of food than an average host brood at fledging (i.e. feeding rates to a parasite are outside the normal range of host behaviour in unparasitized nests). Our observations of the reed warbler (Acrocephalus scirpaceus) at parasitized nests indicate that such behaviour could possibly work in this host species.

Animals↗
PubMed2004

Parasite-mediated reduction in fecundity of mountain hares.

Mountain hare populations in Scotland exhibit regular 10 year fluctuations in abundance. Simple models of host-parasite population dynamics suggest that parasite-mediated reductions in host fecundity can cause a transition from stable to cyclic host population dynamics. We tested the hypothesis that parasites reduce hare fecundity by experimentally reducing parasite burdens and recording female survival, body condition and fecundity. We captured 41 adult female hares in October 2002; 22 were treated with Ivermectin to remove parasites and 19 were left untreated as controls. The treated and untreated hares were culled in May 2003 together with a second control group of nine unhandled hares. Treatment with Ivermectin significantly reduced the abundance of Trichostrongylus retortaeformis and increased-the fecundity of the hares, but had no measurable effect on body condition or over-winter survival. These results are consistent with the hypothesis that parasites may be a contributory cause of cycles in populations of mountain hares.

Animals↗
PubMed2006

Ranging patterns and parasitism in primates.

Competing hypotheses exist concerning the influence of ranging patterns on parasitism. More intensive use of a home range could result in greater exposure to infectious agents that accumulate in the soil. Alternatively, when more intensive ranging is associated with territorial defence, this could decrease home range overlap and produce lower levels of parasitism. We tested these hypotheses using phylogenetic comparative methods and parasite richness data for 119 primate species. Helminth richness increased with the defensibility index, a quantitative measure of home range use that correlates with the degree of territoriality in primates. This association was independent of other host traits that influence parasite richness in primates. Results involving non-vector transmitted helminths produced the most significant results, suggesting that the relationship between territorial behaviour and parasitism is driven by accumulation of parasites in defended home ranges. In addition, costs associated with greater ranging could increase susceptibility to infectious agents.

Animals↗
PubMed1995

Dynamic interactions in malaria: host heterogeneity meets parasite polymorphism.

The spectrum of disease severity in Plasmodium falciparum malaria can be attributed to heterogeneity in parasite virulence or to heterogeneity in host factors. However, the two are not necessarily separate explanations for the same phenomena: they may actually complement each other. The conjoint effects of host and parasite heterogeneity can serve to explain certain intriguing epidemiological observations, such as, why there is a reduction in incidence of severe malaria in certain host genotypes without a concomitant reduction in mild disease. By assuming that severe disease is caused by a rare independently transmitted parasite strain, and that the probability of disease is nonlinearly related to the number of effective infections by a certain strain, the disproportionate reduction in the rate of the rarer disease within resistant host genotypes may be explained. Conversely, heterogeneity in host resistance may, under certain circumstances, facilitate the maintenance of diversity in parasite virulence. In this paper we discuss the coevolutionary consequences of heterogeneity in host resistance and diversity in parasite virulence by using a simple mathematical model that attempts to integrate the population genetics of the system with its ecological dynamics. This allows a unified perspective on malaria transmission that synthesises current evidence regarding the effects of host and parasite heterogeneities on malarial disease.

Animals↗
PubMed2000

Parasite-associated growth enhancement in a fish-cestode system.

Parasites impose an energetic cost upon their hosts, yet, paradoxically instances have been reported in which infection is associated with enhanced, rather than diminished, host growth rates. Field studies of these parasite effects are problematic, since the pre-infection condition of the hosts is generally unknown. Here, we describe a laboratory experiment in which the growth rate and body condition of 76 laboratory-reared three-spined stickleback fishes were examined before, during and after each fish was fed the infective stage of the parasitic cestode Schistocephalus solidus. Twenty-one of these fishes went on to become infected by the cestode. Fishes were individually housed and provided with an abundant food supply to eliminate the potentially masking effects of variable competitive ability. Infection occurred independently of fish gender, size, body condition or pre-exposure growth rate. After exposure to the cestode, infected fishes grew faster (excluding parasite weight) and maintained a similar or better body condition compared with uninfected fishes, despite developing enlarged spleens. The accelerated growth could not be explained by reduced gonadal development. This result, one of few demonstrations of parasite-associated growth enhancement in fishes, is discussed with respect to other such parasite systems.

Animals↗
PubMed2002

The role of parasites in the dynamics of a reindeer population.

Even though theoretical models show that parasites may regulate host population densities, few empirical studies have given support to this hypothesis. We present experimental and observational evidence for a host-parasite interaction where the parasite has sufficient impact on host population dynamics for regulation to occur. During a six year study of the Svalbard reindeer and its parasitic gastrointestinal nematode Ostertagia gruehneri we found that anthelminthic treatment in April-May increased the probability of a reindeer having a calf in the next year, compared with untreated controls. However, treatment did not influence the over-winter survival of the reindeer. The annual variation in the degree to which parasites depressed fecundity was positively related to the abundance of O. gruehneri infection the previous October, which in turn was related to host density two years earlier. In addition to the treatment effect, there was a strong negative effect of winter precipitation on the probability of female reindeer having a calf. A simple matrix model was parameterized using estimates from our experimental and observational data. This model shows that the parasite-mediated effect on fecundity was sufficient to regulate reindeer densities around observed host densities.

Animal Diseases↗
PubMed2006

Antagonistic coevolution with parasites increases the cost of host deleterious mutations.

The fitness consequences of deleterious mutations are sometimes greater when individuals are parasitized, hence parasites may result in the more rapid purging of deleterious mutations from host populations. The significance of host deleterious mutations when hosts and parasites antagonistically coevolve (reciprocal evolution of host resistance and parasite infectivity) has not previously been experimentally investigated. We addressed this by coevolving the bacterium Pseudomonas fluorescens and a parasitic bacteriophage in laboratory microcosms, using bacteria with high and low mutation loads. Directional coevolution between bacterial resistance and phage infectivity occurred in all populations. Bacterial population fitness, as measured by competition experiments with ancestral genotypes in the absence of phage, declined with time spent coevolving. However, this decline was significantly more rapid in bacteria with high mutation loads, suggesting the cost of bacterial resistance to phage was greater in the presence of deleterious mutations (synergistic epistasis). As such, resistance to phage was more costly to evolve in the presence of a high mutation load. Consistent with these data, bacteria with high mutation loads underwent less rapid directional coevolution with their phage populations, and showed lower levels of resistance to their coevolving phage populations. These data suggest that coevolution with parasites increases the rate at which deleterious mutations are purged from host populations.

Directed Molecular Evolution↗
PubMed2002

Obligate brood parasites as selective agents for evolution of egg appearance in passerine birds.

Many passerine host species have counteracted the parasite egg mimicry in their coevolutionary arms race with the common cuckoo (Cuculus canorus) by evolving increased interclutch and reduced intraclutch variation in egg appearance. Such variations make it easier for hosts to recognize a foreign egg, reduce the possibility of making recognition errors, and reduce the ability of the cuckoo to mimic the eggs of a particular host. Here, we investigate if such clutch characteristics have evolved among North American passerines. We predict that due to the absence of brood parasites with egg mimicry on this continent, these passerines should (1) not show any relationship between rejection rates and intra- or interclutch variation, and (2) intraclutch variation should be lower and interclutch variation higher in European hosts exposed to cuckoo parasitism as compared to North American hosts parasitized by cowbirds. Here we present data that show support for most of these and other predictions, as well as when controlling statistically for effects of common descent. However, the effect of continent on intraclutch variation was less than predicted and we discuss a possible reason for this. All things considered, the results demonstrate that parasitism by a specialist brood parasite with egg mimicry is a powerful selective force regarding the evolution of egg characteristics in passerine birds.

Animals↗
PubMed2003

A consideration of patterns of virulence arising from host-parasite coevolution.

In this article we explore how host survival and fecundity are affected by host-parasite coevolution. We examine a situation in which hosts upon being infected can mount a defensive response to clear the infection, but in which there is a fecundity cost to such immunological up-regulation. We also suppose that the parasite exploits the host and thereby causes an elevated host mortality rate. We determine the coevolutionary stable strategies of the parasite's level of exploitation and the host's level of up-regulation, and illustrate the patterns of reduced host fitness (i.e., virulence) that these produce. We find that counterintuitive patterns of virulence are often expected to arise as a result of the interaction between coevolved host and parasite strategies. In particular, despite the fact that the parasite imposes only a mortality cost on the host, coevolution by the host results in a pattern whereby infected hosts always have the same probability of death from infection, but they vary in the extent to which their fecundity is reduced. This contrasts with previous results and arises from our inclusion of two important factors absent from previous theory: costs of immunological up-regulation and a more suitable measure of parasite-induced mortality.

Animals↗
PubMed2004

Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites.

Intestinal worm infections characteristically induce T-helper 2 cell (Th2) cytokine production. We reviewed studies performed with mice infected with either of two intestinal nematode parasites, Nippostrongylus brasiliensis or Trichinella spiralis, that evaluate the importance of the Th2 cytokine interleukin-4 (IL-4) and IL-13 in protection against these parasites. These studies demonstrate that while IL-4/IL-13 protect against both parasites by activating signal transducer and activator of transcription 6 (Stat6) through IL-4 receptor alpha (IL-4Ralpha) ligation, Stat6 activation protects against these parasites through different mechanisms. Stat6-dependent gene transcription promotes expulsion of N. brasiliensis solely through effects on non-bone marrow-derived cells that may include enhancement of intestinal smooth muscle contractility, changes in intestinal epithelial cell function, and increased intestinal mucus secretion. In contrast, Stat6 signaling promotes immunity to T. spiralis both through effects on bone marrow-derived cells that can be reproduced by treating mice with IL-4 or IL-13 and through effects on non-bone marrow-derived cells. The former effects appear to include T-cell-dependent induction of intestinal mastocytosis, while the latter sensitize non-bone marrow-derived cells to mast cell-produced mediators. We argue that a limited ability of the host immune system to distinguish among different nematode parasites has led to the evolution of a stereotyped Th2 response that activates a set of effector mechanisms that protects against most intestinal nematode parasites.

Animals↗
PubMed2004

Toward an understanding of the interaction between filarial parasites and host antigen-presenting cells.

Lymphatic filarial infection, from an immunologic point of view, is one of the most complex parasite infections. Not only are there different clinical manifestations that reflect differing immune responses, but the parasite's multiple stages, each with distinct anatomic tropism, add a compartmental layer of complexity to an already complicated process. Moreover, these parasites have finely tuned immune evasion strategies that enable escape from the innate immune system. As different stages of the parasite interact with different types of antigen-presenting cells that, in turn, may play a significant role in shaping the subsequent adaptive immune response, the focus of this review is to provide insight into the interaction between filarial parasites and antigen-presenting cells with an eye toward understanding how they influence parasite antigen-driven T-cell responses.

Animals↗
PubMedDate not supplied

Hormonal and immunological mechanisms mediating sex differences in parasite infection.

The prevalence and intensity of infections caused by protozoa, nematodes, trematodes, cestodes, and arthropods is higher in males than females. The primary thesis of this review is that immunological differences exist between the sexes that may underlie increased parasitism in males compared to females. Several field and laboratory studies link sex differences in immune function with circulating steroid hormones; thus, the roles of sex steroids, including testosterone, oestradiol, and progesterone, as well as glucocorticoids will be discussed. Not only can host hormones affect responses to infection, but parasites can both produce and alter hormone concentrations in their hosts. The extent to which changes in endocrine-immune interactions following infection are mediated by the host or the parasite will be considered. Although males are more susceptible than females to many parasites, there are parasites for which males are more resistant than females and endocrine-immune interactions may underlie this sex reversal. Finally, although immunological differences exist between the sexes, genetic and behavioural differences may explain some variability in response to infection and will be explored as alternative hypotheses for how differences between the sexes contribute to dimorphic responses to parasites.

Behavior↗
PubMed2006

Microsatellite analysis reveals strong but differential impact of a social parasite on its two host species.

The speed and the dynamics of the co-evolutionary process strongly depend on the relative strengths of reciprocal selection pressures exerted by the interacting species. Here, we investigate the influence of an obligate social parasite, the slave-making ant Harpagoxenus sublaevis, on populations of the two main host species Leptothorax acervorum and Leptothorax muscorum from a German ant community. A combination of genetic and demographic data allowed us to analyse the consequences of raiding pressure on the hosts' life history and possible host preferences of the parasite. We can demonstrate that slave raids during which the social parasite pillages brood from neighbouring host colonies are both frequent and extremely destructive for both host species. Microsatellite analysis showed that, on average, a single slave-maker colony conducts more than three raids per year and that host colonies mostly perish in the aftermath of these parasite attacks. Only in few cases, surviving nests of previously raided host colonies were found in the surroundings of slave-maker colonies. As a consequence of the high prevalence of parasites and their recurrent and devastating slave raids on host colonies, the life expectancy of host colonies was severely reduced. Combining our results on host-specific parasitic colony founding and raiding frequencies with the post-raid survival rate, we can demonstrate an overall higher mortality rate for the smaller host species L. muscorum. This might be caused by a preference of H. sublaevis for this secondary host species as demographic data on host species usage indicate.

Animals↗
PubMed2007

Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles.

We quantified the clonal diversity of the New Zealand marine trematode Maritrema novaezealandensis (n = 1250) within Zeacumantus subcarinatus snail (n = 25) and Macrophthalmus hirtipes crab (n = 25) intermediate hosts using four to six microsatellite loci, and investigated the potential biological and physical factors responsible for the observed genetic patterns. Individual snails harboured one to five trematode genotypes and 48% of snails were infected by multiple parasite genotypes. Overall, the number of parasite genotypes did not increase with snail size, but was highest in intermediate-sized snails. Significantly larger numbers of parasite genotypes were detected in crabs (relative to snails; P < 0.001), with 16-25 genotypes recovered from individual crabs. Although crabs are typically infected by small numbers of cercariae sourced from many snails, they are occasionally infected by large numbers of cercariae sourced from single snails. The latter cases explain the significant genetic differentiation of trematode populations detected among their crab hosts (F(ST) = 0.009, P < 0.001). Our results suggest that the timing of infection and/or intraspecific competition among parasite clones within snails determine(s) the diversity of parasite clones that snails harbour. The presence of a large number of infected snails and tidal mixing of cercariae prior to infection results in crabs potentially harbouring hundreds of parasite genotypes despite the crabs' territorial behaviour.

Animals↗
PubMed2006

The effect of altitude on parasite density case definitions for malaria in northeastern Tanzania.

OBJECTIVES: Malaria clinical trials need precise endpoints to measure efficacy. In endemic areas where asymptomatic parasitaemia is common, 'fever plus parasitaemia' may not differentiate between malaria cases and non-cases. Case definitions based on parasite cut-off densities may be more appropriate but may vary with age and transmission intensity. This study examines appropriate case definitions from parasitological surveys conducted over a broad range of transmission intensities, using altitude as a proxy for transmission intensity. METHODS: Cross-sectional data collected from 24 villages at different altitudes in an endemic area of northeastern Tanzania were used to calculate malaria-attributable fractions using a modified Poisson regression method. We modelled fever as a function of parasite density and determined the optimum cut-off densities of parasites to cause fever using sensitivity and specificity analyses. RESULTS: The optimum cut-off density varied by altitude in children aged under 5 years: a case definition of 4,000 parasites per mul at altitudes <600 m (high transmission intensity) was most appropriate, compared with 1,000 parasites per mul at altitudes >600 m (low transmission intensity). In children aged over 5 years and adults, there was little variation by altitude and a case definition of any parasites plus fever was the most appropriate. CONCLUSIONS: Locally appropriate case definitions of malaria should be used for research purposes. In our setting, these varied independently with age and transmission intensity.

Adolescent↗
PubMed2004

Parasites make male pipefish careless.

Parasite-mediated sexual selection is expected to favour the avoidance of matings with infected individuals. However, the extent to which the costs and benefits of discriminating against parasitized mates trade off may depend upon numerous factors. I investigated the effects of sex and infection status on choosiness in sex-role reversed deep-snouted pipefish (Syngnathus typhle L.) that were either artificially infected with the trematode parasite Cryptocotyle sp. or sham-infected. Sham-infected males were significantly more likely to associate with a sham-infected female rather than with a Cryptocotyle-infected female. Infected males failed to discriminate against infected potential partners. Males were choosier the larger they were relative to the females available for choice. Females were not discriminatory, regardless of their infection status. Given an inverse relation between female fecundity and parasite load, choosy unparasitized males may gain enhanced reproductive success from their choice decisions. In contrast, more heavily infected wild-caught males gave birth to slightly fewer, but not smaller offspring than did uninfected or lightly infected males, suggesting only a low direct premium on choosy females. The detrimental effects of parasitism on male choosiness, and the lack of female discrimination against infected males likely have profound repercussions on the strength of sexual selection acting on the two sexes and on the dynamics of host-parasite interactions in this system.

Analysis of Variance↗
PubMed2005

The social parasite wasp Polistes atrimandibularis does not form host races.

Parasites that exploit the parental behaviour of several host species may be selected to form distinct host-specific genetic lineages. This process is well documented in bird brood parasites, but not in insect social parasites. Polistes atrimandibularis is the only paper-wasp social parasite known to exploit four host species. It does not form genetically distinct host races according to analyses based on microsatellite loci. Also, there were no size-matching between parasites and host species. Instead, P. atrimandibularis queens seemed to be successful as parasites in this population only when they originated from nests of P. dominulus, the largest species. The other host species are a sink for P. atrimandibularis since adult females emerging from those nests appear too small to usurp colonies themselves. Traits that may help P. atrimandibularis infiltrate multiple species may include its nonaggressive usurpation tactics and its ability to acquire host cuticular hydrocarbon recognition labels.

Analysis of Variance↗
PubMed2006

Host ploidy, parasitism and immune defence in a coevolutionary snail-trematode system.

We studied the role of host ploidy and parasite exposure on immune defence allocation in a snail-trematode system (Potamopyrgus antipodarum-Microphallus sp.). In the field, haemocyte (the defence cell) concentration was lowest in deep-water habitats where infection is relatively low and highest in shallow-water habitats where infection is common. Because the frequency of asexual triploid snails is positively correlated with depth, we also experimentally studied the role of ploidy by exposing both diploid sexual and triploid asexual snails to Microphallus eggs. We found that triploid snails had lower haemocyte concentrations than did diploids in both parasite-addition and parasite-free treatments. We also found that both triploids and diploids increased their numbers of large granular haemocytes at similar rates after parasite exposure. Because triploid P. antipodarum have been shown to be more resistant to allopatric parasites than diploids, the current results suggest that the increased resistance of triploids is because of intrinsic genetic properties rather than to greater allocation to defence cells. This finding is consistent with recent theory on the advantages of increased ploidy for hosts combating coevolving parasites.

Animals↗