Abstract
Tumors form as a result of abnormal and uncontrolled proliferation of cells within a multicellular organism, which can lead to cancer. Although this phenomenon exists in all metazoans, most research has focused on malignancies in humans and domestic animals. Thus, the evolutionary ecology of host-tumor interactions and their consequences for ecosystem functioning is a virtually untouched area of research.To address these scientific questions, the biological model used in this thesis is a freshwater cnidarian, the brown hydra Hydra oligactis, some of whose laboratory lines harbor tumors with notable specificities. In addition to the fact that the benign/malignant status of these tumors is not clear, they are capable of vertical transmission, during asexual reproduction of their host by budding. Furthermore, tumorous hydras have an increased number of tentacles compared to healthy hydras.This thesis is organized in 5 sections, an introduction with two synthesis articles, three chapters presenting the research done and a general discussion. The first synthesis deals with the comparison between benign and malignant tumors, the second one deals with the costs of anticancer defenses in host organisms.Our research on H. oligactis first described spontaneous tumors within several wild-type lineages (Chapter 1). This work shows that brown hydra tumors always appear to be of germline origin. Moreover, we show that the presence of a bacterial species of the order Chlamydiales, could play a role in the initiation and/or maintenance of these tumor processes.We then studied (chapter 2) the impact of the tumor-bacterial transmissible complex (i.e. tumor cells and bacteria) on the life history traits of the hydra host. This work shows that polyps derived from tumorous parents, prior to becoming tumoral themselves, intensify their sexual and asexual reproductive efforts. Moreover, these tumorous polyps subsequently have a reduced survival compared to healthy ones. The adaptive nature of these life history trait changes, for the host and/or for the transmissible tumor cells, is discussed. This chapter also focuses on the origin of the increased number of tentacles in tumor polyps. By transplanting different tumors into hydras of varying genetic background, we showed that polyps developing supernumerary tentacles after transplantation were always those that had received tumor tissue from hydras lines harboring transmissible tumors, and already associated with the appearance of supernumerary tentacles in their original host. Rather than a compensatory response initiated by the host, the growth of supernumerary tentacles in some tumor-bearing hydras would therefore be induced by transmissible tumor cells.Finally, in order to improve our understanding of the ecological consequences of host-tumor interactions on ecosystem functioning, we experimentally explored (Chapter 3) the relationships that tumor-bearing hydras have with other animal species living in aquatic environments. We demonstrated that, compared to healthy hydras, tumorous ones had an increased risk of predation by fish, a higher rate of colonization by commensal ciliates, and their ability to capture prey was superior due to their increased number of tentacles.Taken together, this work argues for a better consideration of tumor processes in evolutionary ecology, both in terms of the ecological and evolutionary trajectory of host species and the consequences of these interactions on ecosystem functioning.