Parasite infection leads to widespread glucocorticoid hormone increases in vertebrate hosts: A meta-analysis.

Parasites and pathogens (hereafter parasites) commonly challenge organisms, but the extent to which their infections are physiologically stressful to hosts remains unclear. Importantly, vertebrate hormones, glucocorticoids (GCs), have been reported to increase, decrease or show no alterations stemming from infections, challenging the generality of parasite-associated GC responses and motivating a search for important moderator variables. We undertook the first meta-analysis of changes in vertebrate GCs following experimental infection with parasites, extracting 146 effect sizes from 42 studies involving 32 host and 32 parasite species to test for general patterns of GC following infection, as well as the influence of moderators. Overall, infection increased GCs relative to preliminary or control levels when the single largest effect sizes from repeated measures studies were examined, suggesting that parasites of vertebrate hosts can be thought of generally as physiological stressors by elevating GCs. When all effect sizes were included along with the moderator of sampling time post-infection (tPI), parasite infection still had a positive effect on host GCs. However, the strength of that effect did not relate consistently to tPI, illustrating temporal differences in GC changes during the course of infection among parasite taxa (e.g. arthropod vs. bacterial infections). Other moderator variables examined did not influence GC responses. Studies broadening the range of host and parasite taxa, and sampling during critical time windows, would aid in our understanding of variation in the host stress response and its consequences for fitness of both vertebrate hosts and their parasites.

Demasculinization of male guppies increases resistance to a common and harmful ectoparasite.

Parasites are detrimental to host fitness and therefore should strongly select for host defence mechanisms. Yet, hosts vary considerably in their observed parasite loads. One notable source of inter-individual variation in parasitism is host sex. Such variation could be caused by the immunomodulatory effects of gonadal steroids. Here we assess the influence of gonadal steroids on the ability of guppies (Poecilia reticulata) to defend themselves against a common and deleterious parasite (Gyrodactylus turnbulli). Adult male guppies underwent 31 days of artificial demasculinization with the androgen receptor-antagonist flutamide, or feminization with a combination of flutamide and the synthetic oestrogen 17 ß-estradiol, and their parasite loads were compared over time to untreated males and females. Both demasculinized and feminized male guppies had lower G. turnbulli loads than the untreated males and females, but this effect appeared to be mainly the result of demasculinization, with feminization having no additional measurable effect. Furthermore, demasculinized males, feminized males and untreated females all suffered lower Gyrodactylus-induced mortality than untreated males. Together, these results suggest that androgens reduce the ability of guppies to control parasite loads, and modulate resistance to and survival from infection. We discuss the relevance of these findings for understanding constraints on the evolution of resistance in guppies and other vertebrates.

Experimental elimination of parasites in nature leads to the evolution of increased resistance in hosts.

A reduction in the strength of selection is expected to cause the evolution of reduced trait expression. Elimination of a parasite should thus cause the evolution of reduced resistance to that parasite. To test this prediction in nature, we studied the fourth- and eighth-generation descendants of guppies (Poecilia reticulata) introduced into four natural streams following experimental elimination of a common and deleterious parasite (Gyrodactylus spp.). After two generations of laboratory rearing to control for plasticity and maternal effects, we infected individual fish to assess their resistance to the parasite. Contrary to theoretical expectations, the introduced guppy populations had rapidly and repeatably evolved increased resistance to the now-absent parasite. This evolution was not owing to a resistance-tolerance trade-off, nor to differences in productivity among the sites. Instead, a leading candidate hypothesis is that the rapid life-history evolution typical in such introductions pleiotropically increases parasite resistance. Our study adds a new dimension to the growing evidence for contemporary evolution in the wild, and also points to the need for a re-consideration of simple expectations from host-parasite theory. In particular, our results highlight the need for increased consideration of multiple sources of selection and pleiotropy when studying evolution in natural contexts.

Adding parasites to the guppy-predation story: insights from field surveys.

Studies of phenotypic variation in nature often consider only a single potential selective agent. In such cases, it remains an open question as to whether variation attributed to that single measured agent might be influenced by some other unmeasured agent. Previous research has shown that phenotypic variation in the Trinidadian guppy (Poecilia reticulata) is strongly influenced by predation regime, and we here ask whether parasitism might represent an additional important selective agent shaping this variation. We performed a field survey of 26 natural guppy populations of known predation regime in northern Trinidad. We quantified levels of parasitism of guppies by the monogenean ecotoparasite, Gyrodactylus, and examined whether this parasite was associated with guppy body size or male colour. Spatial variation in Gyrodactylus parasitism was consistent between years, and parasite prevalence was generally, but not always, higher at high-predation sites than at low-predation sites. Consistent with previous work, predation regime was related to guppy size and some aspects of male colour, whereas parasitism showed few and only minor associations with the same traits. Moreover, a consideration of parasitism did not alter any interpretations regarding associations between guppy traits and predation regimes. These results suggest that parasitism, at least as quantified in the present study, does not play a major role in shaping variation in guppy body size or colour. Nevertheless, considerable variation in these traits, even within a predation regime, suggests the likely importance of other selective agents beyond just predation regime.

Relative host body condition and food availability influence epidemic dynamics: a Poecilia reticulata-Gyrodactylus turnbulli host-parasite model.

Understanding disease transmission is important to species management and human health. Host body condition, nutrition and disease susceptibility interact in a complex manner, and while the individual effects of these variables are well known, our understanding of how they interact and translate to population dynamics is limited. Our objective was to determine whether host relative body condition influences epidemic dynamics, and how this relationship is affected by food availability. Poecilia reticulata (guppies) of roughly similar size were selected and assembled randomly into populations of 10 guppies assigned to 3 different food availability treatments, and the relative condition index (Kn) of each fish was calculated. We infected 1 individual per group ('source' fish) with Gyrodactyus turnbulli and counted parasites on each fish every other day for 10 days. Epidemic parameters for each population were analysed using generalized linear models. High host Kn-particularly that of the 'source' fish-exerted a positive effect on incidence, peak parasite burden, and the degree of parasite aggregation. Low food availability increased the strength of the associations with peak burden and aggregation. Our findings suggest that host Kn and food availability interact to influence epidemic dynamics, and that the condition of the individual that brings the parasite into the host population has a profound impact on the spread of infection.

Explaining parasite aggregation: more than one parasite species at a time.

Studies generally have neglected parasite-centric views in explorations of whether the oft-seen patterns of parasite aggregation are adaptive. Using simulation models, we explored the effects of aggregation on coinfection with hetero- or conspecific parasite species characterised by different mean abundances. Increasing aggregation increased the probability of conspecific co-occurrence for parasites with low mean abundances, and increased median numbers of conspecifics for all species. In comparison, increasing aggregation generally decreased the probability, intensity and diversity of heterospecific co-occurrence, irrespective of mean abundance. Researchers should weigh the respective costs and benefits of increasing co-occurrence with conspecifics and decreasing coinfection with heterospecifics in explaining aggregation.

Lesser snow goose helminths show recurring and positive parasite infection-diversity relations.

The patterns and mechanisms by which biological diversity is associated with parasite infection risk are important to study because of their potential implications for wildlife population's conservation and management. Almost all research in this area has focused on host species diversity and has neglected parasite diversity, despite evidence that parasites are important drivers of community structure and ecosystem processes. Here, we assessed whether presence or abundance of each of nine helminth species parasitizing lesser snow geese (Chen caerulescens) was associated with indices of parasite diversity (i.e. species richness and Shannon's Diversity Index). We found repeated instances of focal parasite presence and abundance having significant positive co-variation with diversity measures of other parasites. These results occurred both within individual samples and for combinations of all samples. Whereas host condition and parasite facilitation could be drivers of the patterns we observed, other host- or parasite-level effects, such as age or sex class of host or taxon of parasite, were discounted as explanatory variables. Our findings of recurring and positive associations between focal parasite abundance and diversity underscore the importance of moving beyond pairwise species interactions and contexts, and of including the oft-neglected parasite species diversity in infection-diversity studies.

Can mixed-species groups reduce individual parasite load? A field test with two closely related poeciliid fishes (Poecilia reticulata and Poecilia picta).

Predation and parasitism are two of the most important sources of mortality in nature. By forming groups, individuals can gain protection against predators but may increase their risk of being infected with contagious parasites. Animals might resolve this conflict by forming mixed-species groups thereby reducing the costs associated with parasites through a relative decrease in available hosts. We tested this hypothesis in a system with two closely related poeciliid fishes (Poecilia reticulata and Poecilia picta) and their host-specific monogenean ectoparasites (Gyrodactylus spp.) in Trinidad. Fish from three different rivers were sampled from single and mixed-species groups, measured and scanned for Gyrodactylus. The presence and abundance of Gyrodactylus were lower when fish of both species were part of mixed-species groups relative to single-species groups. This is consistent with the hypothesis that mixed-species groups provide a level of protection against contagious parasites. We discuss the importance of potentially confounding factors such as salinity and individual fish size.