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Organisms face a constant risk of attack from parasites. While classic immunology has revealed numerous physiological and molecular mechanisms that underpin host immunity, the recently developed field of ecological immunology has attempted to understand the ecological and evolutionary causes that explain the diversity of such immune mechanisms. However, progress in the field has been hampered by the complex relationship between immunity and fitness as well as the methodological limitations of our experiments. There is an urgent need for eco-immunological studies that combine life history theory with experimentally tractable but ecologically realistic host and pathogen models. In this thesis, I tackle three novel aspects of host defence against parasites in an established model for insect immunity, the fruit fly Drosophila melanogaster, with the entomopathogenic fungus Metarhizium robertsii, one of the most successful natural insect pathogens. In particular, I show in Chapter 2 that an immune and stress response gene, Turandot M, provides specific immunity against sexually transmitted fungal infections; but, this protective effect comes at a cost to life history in the absence of infection. In Chapter 3, I show that when exposed to the fungal pathogen, the fruit fly alters its temperature preference by seeking out cooler temperatures, which results in a dramatic shift in its life history strategy while simultaneously enhancing antifungal resistance, though not tolerance. Finally, I demonstrate in Chapter 4 that exposure to fungal parasites induces fitness-associated maternal effects on offspring meiotic recombination and life history, both of which have the potential to accelerate adaptive evolution. Taken together, these results demonstrate the benefits of integrating life history theory in eco-immunological research. They show that life history responses are an integral component of host defence against parasites, and that Drosophila-Metarhizium is a promising model system for ecological immunology.

Ecological immunology is the study of the ecological and evolutionary factors that explain variation in the function of, and investment in, the immune system. Within this field, reproduction-based trade-offs are an important focus, where studies often address the immunological costs associated with the expression of secondary sexual traits used in mate choice. Specifically, the Immunocompetence Handicap Hypothesis (ICHH) links the expression of secondary sexual traits to immune function, stating that testosterone promotes the expression of these traits while suppressing the immune system. In doing so, testosterone may maintain the honest expression of such traits, but also ultimately cause sex differences in immunity because males tend to have high levels of testosterone. I explore aspects of these topics using two model systems: the Psittaciformes (Parrots: Chapter 2) and the Charadriiformes (shorebirds), in particular the sex-role reversed Red phalarope (Phalaropus fulicarius). In Chapter 2, I employed a phylogenetically informed approach to investigate the relationships among immune investment, plumage colouration and longevity in parrots. I found that immune investment was greater in more colourful species, as well as in those with a slower pace-of-life (i.e., longer incubation periods), but not specifically in those with longer lifespans. In Chapter 3, I investigated the role that reproductive behaviours play in determining sex differences in corticosterone levels. One explanation for sex differences in the stress response is that selection favours a reduced response in incubating birds to reduce nest abandonment. I generally found little support for sex differences in corticosterone being driven by behaviours related to incubation. Moreover, in phalaropes, sex differences in corticosterone were already present prior to incubation. In Chapter 4, I found that males have higher levels of testosterone than females, but that females were immunosuppressed compared to males. However, I found evidence that testosterone may regulate immune function in females, but not males. The observation of female-biased immunosuppression is consistent with Bateman’s Principle, and although there was some evidence of a testosterone-mediated handicap acting through immune function, these results attest to a fundamental lability in the relationship between testosterone and immunity. In Chapter 5, I demonstrated that plumage colouration in phalaropes is condition-dependent and so potentially conveys useful information to conspecifics. Yet, the relationship was negative in both sexes such that more colourful individuals had poorer immunocompetence, which was contrary to predictions. In Chapter 6, I demonstrated that phalaropes pair assortatively (positively) based on plumage colouration, but negatively based on aspects of size. I discuss the results of this dissertation in the light of life history theory, as well as in the context of mechanisms maintaining signal honesty.

La division du travail est une caractéristique clé chez les insectes sociaux et contribue à leur succès écologique. En ce qui concerne les tâches sanitaires, la division du travail au sein d’une colonie peut permettre de réduire la transmission des maladies, de libérer certaines ouvrières pour d’autres tâches, permettant de diminuer les couts associés à l’exécution des tâches sanitaires (sur le plan comportementale et physiologique). Les facteurs externes et internes aux individus déterminant leur participation aux tâches sanitaires ne sont pas bien connus. La plupart des études portent sur l’importance des différences génétiques entre ouvrières. Dans les deux premières études, j’ai examiné le rôle de l’expérience des individus (par exposition répétée à des déchets sanitaires ou à l’exécution d’une tâche) sur la mise en place de différences interindividuelles dans l’exécution d’une tâche sanitaire comportementale. L’exposition à un parasite est une menace fréquente au sein de colonies d’insectes sociaux. En utilisant la fourmi clonale Platythyrea punctata, j’ai voulu savoir si une exposition répétée des individus à des larves portant une faible quantité de conidiospores du champignon Metarhizium robertsii affectait la performance des soins sanitaires portés au couvain. J’ai trouvé que la durée de nettoyage des larves était plus élevée chez des fourmis entrainées, aux larves exposées ou non exposées au champignon, que chez des fourmis inexpérimentées. Un temps de nettoyage plus élevé améliorait l’élimination des conidiospores. Ainsi les fourmis entrainées pourraient être plus efficaces pour éliminer les conidiospores lors d’une attaque parasitaire de la colonie. La décomposition des cadavres représente un risque sanitaire dans les colonies d’insectes sociaux, nécessitant une gestion de cadavres. Dans la deuxième étude, j’ai étudié la possibilité d’une division du travail dans la gestion des cadavres (c'est-à-dire le nettoyage et le transport) chez les ouvrières de la fourmi polygyne et polymorphe Cataglyphis velox. J’ai plus spécifiquement testé si la propensité d’accomplir ces tâches était en rapport avec une récente expérience individuelle ou avec la taille des ouvrières. Nos observations ont montré que la majorité des individus de la colonie n’effectuait que rarement des tâches de gestion de cadavres même si quelques individus pouvaient être impliqués plus fréquemment, au moins sur un laps de temps cours, dans l’exécution de ces tâches. Les résultats suggèrent une faible division du travail dans le nettoyage et le transport des cadavres et une faible modulation de ces tâches par l’exposition répétée des ouvrières à des cadavres. / Division of labor is a key characteristic of social insects and contributes to their ecological success. Especially in disease defense, the intra-colony partitioning of sanitary work can reduce disease transmission, keep nestmates available for other tasks and reduce costs associated with sanitary task performance (i.e. at the behavioral and physiological level). Factors internal and external to the individual affecting sanitary task allocation are not well known and most studies investigated genetic differences between workers performing behavioral sanitary work. In the first two studies I addressed whether individual experience (through repeated exposure to a sanitary hazard or performance of the task) can generate interindividual differences in the performance of behavioral sanitary tasks. Repeated parasite exposure is a common threat in colonies of social insects, posing selection pressures on colony members to respond with improved disease-defense performance. In the clonal ant Platythyrea punctata, I tested whether experience gained by repeated tending of low-level fungus-exposed (Metarhizium robertsii) larvae alters the performance of sanitary brood care. I found that ants trained both with sham- and fungus-treated larvae groomed the brood longer than naive ants. Increased grooming of fungus-treated larvae resulted in more effective fungal removal, thus making trained ants better caretakers under parasite attack of the colony. Decomposing cadavers pose a sanitary risk to social insect colonies, necessitating cadaver management. In the second study I investigated whether cadaver management (i.e. cadaver grooming and transports) is divided among workers and task allocation affected by recent individual experience or worker size in the polymorphic and polygynous ant Cataglyphis velox. Many individuals performed cadaver management infrequently and few individuals dominated task performance. Our results suggested low division of labor for cadaver grooming and transport and a reduced modulation of these behaviors by recurrent exposure to nestmate cadavers.

Parasitic infections are ubiquitous in nature, and host-parasite dynamics can have powerful effects on wildlife populations. Many species have evolved behavioral responses to infection that can help mitigate damage from parasites. Anorexia is a common response to infection observed throughout the animal kingdom. Reducing nutrient intake can help shift host resources from digestion to immunity, as well as limit resources available to parasites. Reduced feeding can weaken the host, but in some host-parasite interactions, this cost is less than that of maintaining an infection. Here, I describe an experiment aimed to explore the effects of the parasitic nematode Aplectana hamatospicula on the Cuban treefrog (Osteopilus septentrionalis) across life stages. Tadpoles were exposed to A. hamatospicula larvae or a sham exposure and growth and behavior were quantified. After metamorphosis, the jumping performance of these frogs was assessed. I revealed that A. hamatospicula could infect and complete its lifecycle in tadpoles. This infection was unique in that it persisted through metamorphosis with the worm continuing to reproduce in the intestinal tract of the terrestrial frogs. These infections reduced the relative mass gain of tadpoles. However, post-metamorphic frogs were able to compensate for this lower growth when provided an ad libitum diet, and infection did not directly or indirectly impact jumping performance, perhaps because of this compensation. Tadpoles that prevented or cleared the infection had a higher rate of anorexia, suggesting that anorexia might be a successful disease-mitigation response to A. hamatospicula.