Diss. ETH. No. 14278 EVOLUTIONARY ECOLOGY AND ADAPTIVENESS OF IMMUNE DEFENSES OF THE SOCIAL INSECT BOMBUS TERRESTRIS (L.) (HYMENOPTERA: APIDAE) A dissertation submitted to the SWISS FEDERAL INSTITUTE OF TECHNOLOGY for the degree of Doctor ofNatural Seiences Presented by Yannick Moret Diplöme d'Etudes Approfondies (D.E.A.) ofPopulation Biology, Genetics and Eco-Ethology, University ofTours, France Born February 5, 1973 From Montlucon, France. Accepted on the recommendation of Prof. Dr. P. Schmid-Hempel, examiner Prof. Dr. J. Koella, co-examiner 7 1. RESUME Les parasites et les pathogenes peuvent affecter la survie, la croissance et la reproduction de leurs hötes. Ces effets nefastes ont conduit, parmi les populations d'hötes, a la selection de nombreux mecanismes de resistance, Parmi ceux-ci, le systeme immunitaire des animaux est l'un des plus repandu. Malgre l'importance de la pression de selection exercee par les parasites, les populations d'hötes presentent des niveaux de resistance ou d'immunocompetence tres varies. Pour expliquer cette grande variation, des discussions recentes en ecologie et en evolution ont emis l'hypothese selon laquelle l'immunite serait coüteuse et contraindrait l'expression d'autres composantes de la valeur selective (ou fitness). Par consequent, la selection naturelle favoriserait I'accroissement de l'immunocompetence uniquement lorsque celle-ci serait benefique, Afin d' examiner la veracite de cette hypothese, j' ai etudie, au cours de cette these, les coüts sur la fitness associes ä l'utilisation du systeme immunitaire. Cette etude a ete realisee sur le bourdon Bambus terrestris (L.), un insecte social facile a elever en laboratoire. B. terrestris est connu pour etre la cible de nombreux parasites et doit, par consequent, solieiter tres frequement son systeme immunitaire. L'utilisation du systeme immunitaire requiere des ressources (nutriments et energie) et pourrait imposer un coüt capable d'affecter la fitness de l'höte, Dans cette etude, pour forcer les bourdons leur systeme immunitaire, des ouvrieres ont ete exposees a ä activer des stimulations immunogeniques standards. En fonction de la disponibilite de ressource, il a pu etre dementre qu'une reponse immunitaire impose un coüt substantiel sur la survie des ouvrieres. De plus, lorsque les ouvrieres utilisent leur fonetion immunitaire pendant une periode prolongee du cycle de vie de la colonie, le succes reproducteur de cette derniere est diminue. Des donnees supplementaires montrent que des compromis d'allocation (ou trade-offs) pourraient exister entre les composantes mernes du systeme immunitaire des bourdons. Par consequent, les resultats presentes ici supportent l'hypothese mentionnee plus haut selon laquelle le coüt des defenses immunitaires pourrait contraindre l'evolution de l'immunite. 8 Cependant, cette etude montre aussi que des changements phenotypiques de 1'histoire de vie des colonies de bourdons peuvent resulter de l' activation du systeme immunitaire. Ces modifications de l'histoire de vie aideraient ä reduire l'impact du coüt des defenses immunitaires lorsque celles-ci sont necessaires, Ainsi, la combinaison du coüt de la fonction immunitaire et de la necessite de se defendre contre les parasites pourrait avoir conduit a la selection d'adaptations permettant le maintient d'un niveau dimmunocompetence eleve mais avec un coüt attenue au mieux. 9 2. SUMMARY Parasites and pathogens can negatively affect the survival, growth and reproduction of their hosts. These negative effects lead, in host populations, to selection for various resistance mechanisms. Among these, the immune system of animals is one of the most widespread. Despite the strong selective pressure imposed by parasites, host populations exhibit high natural variation in pathogen resistance or immunocompetence. To explain this variation, recent discussion in evolutionary ecology entertained the hypothesis that immunity might be costly and trade-off against other fitness components. Hence, natural selection would favour enhanced immunocompetence only when it is beneficial. To examine the extent to which this hypothesis could be supported I investigated, in this thesis, the fitness costs associated with the use of the immune system. In this study, the model system used was the bumblebee Bambus terrestris (L.), which can be easily bred in the laboratory. B. terrestris is known to be targeted by many parasites and thus may face frequent challenges to its immune system. Here, to induce bumblebees to use their immune system, workers were exposed to standardised immunogenic challenges. According to levels of environmental stress (resource limitation) a substantial individual cost ofthe immune response was seen to decrease worker's survival. In addition, forcing workers to use their immune system over prolonged periods of time during the colony life cycle resulted in a decrease in a colony's reproductive success. Furthermore, additional data showed that trade-offs between components of the immune system of bumblebees exist. Therefore, the results presented here support the hypothesis above in which the cost of the immune defences may constrain the evolution of immunity. However, also in this study, adaptive phenotypic changes of life history patterns were observed due to the activation of the immune system. These may help to decrease or compensate for the cost of immune defences. This suggests that the cost of immune defences associated with the necessity of defence against parasites may also select for adaptations leading to an affordable, albeit costly immunity.