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 β-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

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

The wild side: Assessing evolutionary ecology of defence against parasites in nature

Interactions with enemies are an important source of extrinsic mortality in nature. As such, traits that alleviate the detrimental effects of enemies are expected to be under strong selection and to evolve rapidly following shifts in the level of enemy-induced mortality. The evolutionary effects of increasing enemy pressure on defensive traits against those enemies are straight forward and well supported both theoretically and empirically – increased enemy pressure should lead to increased investment in defences and promote the evolution of defences. The consequences of relaxing enemy pressure, on the flip-side, are more complex to predict given that the evolution of defensive traits are now more strongly influenced by their trade-offs with other fitness enhancing traits. In this dissertation I assessed, in nature, the eco-evolutionary implications of enemy release on defence against parasites and on host speciation. Through laboratory and field assays I used a common and deleterious parasite (Gyrodactylus spp.) and its poeciliid host (Poecilia reticulata - guppies) as a model system. First, I assessed whether removal of this parasite in replicate introductions in the wild led to the rapid evolutionary loss of resistance to Gyrodactylus and whether this evolution occurred in parallel between the sexes. After two generations of laboratory rearing to control for plasticity and maternal effects I found that, contrary to theoretical expectations, female guppies that had evolved for four and eight generations released from Gyrodactylus had rapidly and repeatably evolved increased resistance to the parasite. I concluded that this evolution is likely caused by rapid life-history evolution in response to release from predators. In addition, I found non-parallel evolution of the sexes. Male guppies in the ancestral population had higher resistance to Gyrodactylus than females, and parasite release in the introduced populations did not lead to male evolution of resistance, which –in turn - led to the evolutionary reduction of sexual dimorphism. I argue that the non-parallel evolution of resistance is caused by previous selection for high resistance in males that constrains further evolution of the trait. Given that the results indicate that simultaneous relaxation in predation pressure may have accounted for the findings, I then evaluated in a multidimensional selection context (i.e., changes in parasitism, predation, diet and productivity) whether evolution under enemy release, led to the formation of reproductive barriers (ecological speciation) through the evolution of mate choice and signaling traits. Despite theoretical expectations that multidimensional divergent selection would promote ecological speciation and observed rapid evolution of male signaling traits, enemy release in this system does not promote the evolution of assortative mating. I conclude that other aspects of sexual selection – conserved preference for novel males – counteracts the influence of strong multifarious divergent selection.Finally, I tested whether inter-specific social interactions (mixed-species group formation) can provide a degree of enemy release against contagious parasites, a rarely considered but potential advantage of mixed-species group formation. I found that the presence and abundance of Gyrodactylus is lower in poeciliids forming mixed-species groups than those forming single species groups, which is consistent with the hypothesis that mixed-species groups provide a level of protection against contagious parasites. These studies add a new dimension to the growing evidence of contemporary evolution in the wild and point to the need for the re-consideration of simple expectations from host-parasite theory, and more broadly relaxed selection. In particular, the results highlight the need for increased consideration of multiple sources of selection and pleiotropy when studying evolution in natural contexts.Les interactions avec les ennemis sont une source importante de mortalité dans les milieux naturels. Dès lors, on doit s'attendre à ce que les traits réduisant ces effets néfastes soient soumis à une forte sélection et qu'ils évoluent rapidement selon cette mortalité. Les effets dus à l'accroissement de la pression des ennemis sur les traits défensifs sont connus théoriquement et empiriquement – investissement dans les défenses et promotion de l'évolution des défenses. Les conséquences du relâchement de la pression due aux ennemis, en revanche, sont plus complexes à prévoir étant donné que l'évolution des traits défensifs est à présent plus fortement influencée par leurs "trade-offs” avec d'autres traits augmentant la fitness. Dans cette dissertation, j'évalue, en milieu naturel, les implications eco-évolutives du relâchement de la pression de l'ennemi sur la défense contre les parasites et sur la spéciation. Au travers d'expériences (laboratoire et terrain), j'utilise un parasite commun et délétère (Gyrodactylus spp.) et son hôte poecilidé (Poecilia reticulata – guppies) comme système modèle. Tout d'abord, je teste si le retrait du parasite en milieu naturel entraîne une rapide perte évolutive de la résistance à Gyrodactylus, et si cette évolution a lieu en parallèle entre les sexes. J'ai trouvé que, contrairement aux prédictions théoriques, les femelles guppies qui avaient évolué en l'absence de Gyrodactylus montraient un accroissement de la résistance envers le parasite. J'en ai conclu que cela est probablement du à une évolution rapide d'histoire de vie en réponse à la diminution de pression par les prédateurs. De plus, j'ai trouvé une évolution non-parallèle des sexes. Les mâles guppies de la population ancestrale avaient une résistance plus forte au Gyrodactylus que les femelles, et le relâchement de la pression parasitaire n'a pas modifié la résistance des mâles, ce qui a conduit à une réduction évolutive du dimorphisme sexuel. Je soutiens que cette évolution non parallèle est causée par la sélection passée pour une forte résistance chez les mâles qui contraint l'évolution future de ce trait.J'ai testé ensuite, dans un contexte de sélection multidimensionnelle (i.e., changements en termes de parasitisme, prédation, alimentation et productivité), si l'évolution en conditions de relâchement de la pression due à l'ennemi, conduit à la formation de barrières reproductives (spéciation écologique) au travers de l'évolution du choix du partenaire et des traits de signalisation. La sélection divergente multidimensionnelle devrait théoriquement promouvoir la spéciation écologique et l'évolution rapide observée des traits de signalement des mâles. Néanmoins, la diminution de pression due à l'ennemi dans ce système ne promeut pas l'évolution de l'accouplement entre semblables. Je conclus que la préférence conservée pour les nouveaux mâles contrebalance l'influence de la sélection divergente.Enfin, je teste si les interactions sociales inter-spécifiques (formation de groupes mixtes d'espèces) peut fournir un certain degré de relâchement de la pression due aux parasites dangereux, un avantage potentiel mais rarement considéré de la formation des groupes mixtes d'espèces. J'ai trouvé que la présence et l'abondance des Gyrodactylus est plus faible dans les poecilidés formant des groupes mixtes que dans ceux formant des groupes monospécifiques, ce qui est en accord avec l'hypothèse énoncée. Ces études ajoutent une nouvelle dimension aux preuves d'une évolution contemporaine en milieu naturel et établit la nécessité de reconsidérer les prédictions simples de la théorie hôte-parasite, et plus largement de la sélection en contexte de relâchement de contraintes. En particulier, ces résultats mettent en lumière la nécessité de considérer davantage les multiples sources de sélection et la pléiotropie quand on étudie l'évolution en contexte naturel

Do gynogenetic species escape evolving enemies?

Gynogenetic organisms are asexual females of one species that require sperm from males of another species to initiate reproduction (but except in rare instances of ‘paternal leakage’, those sperm do not contribute to the genetic make-up of the gynogens’ offspring). Gynogenetic organisms seem to combine disadvantages of both sexual and asexual reproductive strategies (e.g., mating costs, reduced genetic diversity). We borrowed logic from the Red Queen Hypothesis (RQH) to help explain the persistence of gynogenetic species in nature, which is a paradox. The RQH is the most oft-cited explanation for the maintenance of sex. It states that evolving enemies generate a constantly changing environment, which provides the conditions that make sex advantageous. Under this scenario, asexual organisms cannot evolve fast enough to ‘keep up’ with co-evolving parasites and disease causing organisms, and ultimately show reduced fitness compared to sexual individuals. The RQH tends to view asexuality generally, ignoring important nuance in nature like gynogenetic species in mixed assemblages with closely related sexual species. We outline tests of the argument that sperm dependency prevents asexual gynogens from outcompeting sexuals in mixed species assemblages and that this further allows gynogens to escape evolving enemies

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

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

Dargent_et_al_disassortative

Data based on video and photos of female mate choice trials. See publication for details

Low prevalence of the parasite Ophryocystis elektroscirrha at the range edge of the eastern North American monarch (Danaus plexippus) butterfly population

Every year monarch butterflies (Danaus plexippus Linnaeus, 1758) from the eastern North American population migrate from Mexico to Southern Canada in the spring. This northward migration has been shown to reduce monarch infection with the host-specific parasite Ophryocystis elektroscirrha (OE) (McLaughlin and Myers, 1970); yet, the prevalence of OE at their range limits, and the mechanism(s) responsible, is unknown. We assessed OE infection levels of monarchs at the northern edge of the eastern population distribution around Ottawa, Canada, and found extremely low levels of infection (~1% with upper confidence intervals close to 3%). Low OE infection levels are likely due to low densities of monarchs in this region and/or migratory escape effects, where migrating individuals leave behind areas with high density of conspecifics and high potential for parasite accumulation and transmission. Future work should aim to disentangle the relative contribution of these two mechanisms for governing the decrease in parasitism at the range limits of migratory populations.The accepted manuscript in pdf format is listed with the files at the bottom of this page. The presentation of the authors' names and (or) special characters in the title of the manuscript may differ slightly between what is listed on this page and what is listed in the pdf file of the accepted manuscript; that in the pdf file of the accepted manuscript is what was submitted by the author