Two proposed models will be used to help answer a long observed question in the dynamics of \textit{Manduca sexta} and its related parasitoid wasps-Why is there a large difference in diversity in hyperparasitoid species between tobacco and other related plants such as tomato? Two stage structured differential equation models are presented. The first is a single patch model to study the changes in dynamics that occur between hosts, parasitoids, and hyperparasitoids as the amount of nicotine in the plant increases. The second is a two patch model that allows hyperparasitoids to choose between patches that are nicotine negative (i.e. tomato plants) and nicotine positive (i.e. tobacco plants). Both models will be used to investigate how host nicotine sequestration may impact hyperparasitoid diversity.

Cotesia congregata est une guêpe parasitoïde qui se développe à l’intérieur de la larve du Lépidoptère, Manduca sexta. Ce parasitoïde a développé une stratégie de virulence qui utilise un symbionte viral de la famille des Polydnavirus nommé Cotesia congregata bracovirus. Mon travail de thèse a permis de caractériser le dialogue moléculaire au cours de l’interaction par des approches de transcriptomique à haut débit et de physiologie. Ces travaux ont permis d’établir la première carte fonctionnelle du génome viral et de visualiser l’ensemble des gènes de M. sexta régulés au cours du parasitisme. La régulation des gènes de l’immunité a révélé que le parasitisme n’empêche pas l’induction de peptides antimicrobiens, mais entraine la sous-expression de gènes impliqués dans la réponse cellulaire. De plus j’ai pu mettre en évidence une réduction du nombre de cellules adhérentes au cours de l’interaction et décrire l’induction d’un phénotype de type apoptose d’une catégorie de cellules immunitaires. Ces résultats permettent d’identifier des gènes acteurs de l’interaction et apportent de nouvelles connaissances relatives aux interactions hôtes-parasitoïdes. / Cotesia congregata is a parasitoid wasp that develops inside the lepidopteran larvae, Manduca sexta. This parasitoid wasp has evolved virulence strategies using an obligate viral symbiont from the Polydnavirus family named Cotesia congregata bracovirus. My thesis work has allowed us to characterize the molecular dialogue during the interaction by physiological and high-throughput transcriptomic approaches. This work allowed to obtain the first functional map of the viral genome and to identify all M. sexta genes regulated during parasitism. Regulation of immune genes revealed that parasitism does not prevent induction of antimicrobial peptides, but leads to the down-regulation of genes involved in the cellular response. Moreover, I was able to demonstrate a reduction in the number of adherent cells during the interaction and to describe this induction as an apoptosis-like phenotype targeting a specific population of immune cells. These findings open the way to the identification of candidate genes involved in this particular interaction and provide new insights into host-parasitoid interactions in general.

Prior exposure to plants cues can enhance assortative mating in insects. We hypothesized that, as previously reported for females, males of Cotesia congregata would display inherent responses to plant cues that could be modified by postemergence experience and further, that males originating from two different host-plant complexes (HPCs) would display different behavioral responses to these HPCs. In no-choice contact assays with a non-host plant, searching responses of males and females increased sharply at Day 2 and remained stable through Day 4. In no-choice assays with potential host plants, males searched longer on catalpa than tobacco; responses were not modified by postemergence experience. In choice assays with both HPCs, naïve males did not display orientation preferences; however, males experienced with their natal plant preferred their natal HPC. Results indicate that postemergence experience on the natal host plant induces an orientation preference for the natal HPC and thus, can facilitate assortative mating.

The catalpa sphinx, Ceratomia catalpae, is a specialist on Catalpa trees, which produce iridoid glycosides (IGs). Whereas some trees are defoliated every year, others escape herbivory. Caterpillar populations are either heavily parasitized by the braconid wasp, Cotesia congregata, or remain unparasitized. We hypothesized that these patterns could be explained by variable IG concentrations among trees and insect responses to these chemicals. IG concentrations varied among trees. Percent defoliation was positively related to IG concentration. In comparisons of insect responses to relatively high or low IG concentrations, moths preferred to oviposit on trees with high IG concentrations. Caterpillars did not display a feeding preference nor did wasps differ in searching responses to leaf discs with high or low IG concentrations. Results indicate that observed patterns of herbivory can be explained by moth oviposition preferences for trees with high IG concentrations.

Among the predicted impacts associated with global climate change, warming is of special interest because the rates of physiological processes are temperature-dependent. Insects and other ectotherms are likely to be affected due to their limited ability to control body temperature. In this study, I measured the tolerance to extreme high temperatures, i.e., critical thermal maximum (CTmax), of component species in a tri-trophic system, including an herbivore (Manduca sexta), a primary larval parasitoid (Cotesia congregata) and a hyperparasitoid (genus Silochalcis). For wild insects, the parasitoid had the lowest CTmax, the hyperparasitoid had the highest, and the herbivore was intermediate. For laboratory insects, the parasitoid had a lower CTmax than the herbivore. Results suggest that laboratory colonies can be used to predict relative thermal performance of interacting species in the field. Variations in tolerance to high temperature among component species could disrupt the outcome of interactions in multi-trophic systems.

The ecology and evolution of a species is often considered only within the context of pairwise interactions even though a species' distribution and abundance may be determined by interactions with many species within and between trophic levels. Multiple herbivores often share the same host and may interact indirectly by altering the relationships between herbivores, their host plants and their parasitoids. However, the relationships between parasitoids and herbivore hosts have typically been studied in isolation of other herbivore species. I examined how the outcomes of species interactions change when multiple relationships are considered. Chapter 1 examined the potentially conflicting selection pressures Manduca sexta exerts on Nicotiana tabacum (tobacco), since M. sexta has pollinating adults but herbivorous larvae. I demonstrated that high nectar amino acids do not affect floral visitation, but increased oviposition of herbivores on leaves. Thus, the relative costs and benefits of nectar rewards may depend on the community of pollinators and their life histories. In the remaining chapters I examined how feeding on tobacco by the aphid Myzus persicae altered the interactions between a parasitoid (Cotesia congregata) and its hornworm host (M. sexta). Chapter 2 demonstrated that aphids reduced hornworm abundance and parasitism. Changes in hornworm abundance were not due to density-dependent changes in moth oviposition, but the proportion of caterpillars attacked by parasitoids was inversely density dependent with hornworm density. Chapter 3 examined whether changes in hornworm abundance and parasitism reflected aphid-induced changes in host plant quality or volatile emissions. Aphids increased hornworm mortality, did not affect parasitoid performance, and increased parasitoid search time. In combination with Chapter 2, results suggest that aphids can mediate parasitoid-caterpillar interactions through changes in host plants that reduce hornworm survival and alter parasitoid behavior. Chapter 4 addressed how the outcome of interactions that are altered by aphids changed with spatial scale, and found no effect spatial scale on hornworm abundance and parasitism. In this system, aphids alter parasitoid-caterpillar interactions through changes in plant quality that reduce hornworm performance and abundance, and in turn, influence parasitoid attack. This work demonstrates that the outcome of multispecies interactions may not be predictable from pairwise interactions. / Ph. D.

Endoparasitoids of herbivorous lepidopterans have intimate relationships with their host species as well as the plant on which their host develops. Characteristics of both hosts and plants can affect parasitoid success in tri-trophic systems and thus, drive diversification. Genetic differentiation was estimated for Cotesia congregata (Say) collected from two distinct host-plant complexes, Manduca sexta L. on tobacco (Nicotiana tabacum L.) and Ceratomia catalpae, (Haworth) on catalpa (Catalpa bignonioides Walker), in the mid-Atlantic region of North America using seven microsatellite loci and the mitochondrial COI locus. Microsatellite allele frequencies were differentiated based on host-plant complex, and COI haplotypes from individuals on the same host-plant were identical despite geographic distances between catalpa sites of up to 830 km and distances between tobacco sites of up to 294 km. Results indicate genetic differentiation of subpopulations of C. congregata based on host-plant complex and not geographic distance, and were designated as host races. Cotesia congregata is a gregarious parasitoid, meaning that many individuals develop in a single host larva. Superparasitism, or repeated egg-laying events in the same host larva, is likely to occur in gregarious species. Brood size was not a good predictor of superparasitism in C. congregata, but within-brood male allele diversity indicates either superparasitism or multiple mating by female wasps.

L'hyménoptère Cotesia congregata (Microgastrinae ; Braconidae) pond ses oeufs à l'intérieur de son hôte, la chenille du lépidoptère Manduca sexta (Noctuidae ; Sphingidae) et introduit des particules virales de bracovirus contenant 30 cercles d'ADN double brin. Les gènes viraux portés par ces cercles codent pour une série de protéines qui sont produites dans les tissus de la chenille parasitée. Ces protéines virales jouent un rôle indispensable à la réussite parasitaire. En effet, l'expression des gènes viraux entraîne de nombreuses altérations de la physiologie de l'hôte, notamment un contournement de l'immunité de la chenille qui permet le développement des larves du parasite. D'autre part, le développement de l'hôte est bloqué à un stade pré-pupal. Les travaux portant sur la caractérisation des génomes de bracovirus ont beaucoup progressé et plusieurs familles de gènes ont été découvertes. Une synthèse des connaissances actuelles sur l'immunité des insectes et les gènes de bracovirus potentiellement impliqués dans le contrôle de l'immunité et du développement des lépidoptères est présentée en introduction.<br />Au cours de ma thèse, le séquençage et l'analyse du génome du bracovirus de Cotesia congregata ont été réalisés (Espagne et al 2004). L'existence de plusieurs familles multigéniques a été mise en évidence, notamment la famille des protéines tyrosines phosphatases (PTP) composée de 27 gènes (Provost et al 2004), la famille des cystatines composée de 3 gènes (Espagne et al soumis) et enfin celle des protéines à motif ankyrine composée de 6 gènes (Pennacchio et al en préparation). La caractérisation détaillée de la famille des PTP a été effectuée. La technique d'électrophorèse en champs inversés (FIGE) a permis la localisation physique de ces gènes sur l'ensemble du génome viral, et leur expression a été analysée dans une série de tissus de l'hôte parasité grâce à une méthode de PCR multiplex. Enfin, des tests d'activité biochimique de PTP de bracovirus produites in vitro grâce à un système d'expression en baculovirus.<br />Les gènes des familles décrites sont exprimés dans l'hôte parasité et les protéines possèdent, en général, la fonction biochimique prédite grâce aux domaines conservés qu'elles contiennent. Ceci suggère que ces protéines virales jouent un rôle actif dans les modifications de la physiologie de l'hôte induite par le parasitisme. La caractérisation des gènes viraux exprimés dans l'hôte est une étape indispensable vers l'identification du rôle individuel de chaque protéine dans le contrôle de la physiologie des chenilles parasitées.