First evidence for the evolution of host manipulation by tumors during the long-term vertical transmission of tumor cells in .
Justine Boutry, Océane Rieu, Lena Guimard, Jordan Meliani, Aurora M Nedelcu, Sophie Tissot, Nikita Stepanskyy, Beata Ujvari, Rodrigo Hamede, Antoine M Dujon, Jácint Tökölyi, Fréderic Thomas
Author Information
Justine Boutry: CREEC/CANECEV (CREES), MIVEGEC, Unité Mixte de Recherches, IRD 224-CNRS 5290 Université de Montpellier, Montpellier, France. ORCID
Océane Rieu: CREEC/CANECEV (CREES), MIVEGEC, Unité Mixte de Recherches, IRD 224-CNRS 5290 Université de Montpellier, Montpellier, France. ORCID
Lena Guimard: CREEC/CANECEV (CREES), MIVEGEC, Unité Mixte de Recherches, IRD 224-CNRS 5290 Université de Montpellier, Montpellier, France.
Jordan Meliani: CREEC/CANECEV (CREES), MIVEGEC, Unité Mixte de Recherches, IRD 224-CNRS 5290 Université de Montpellier, Montpellier, France.
Aurora M Nedelcu: Department of Biology, University of New Brunswick, Fredericton, Canada. ORCID
Sophie Tissot: CREEC/CANECEV (CREES), MIVEGEC, Unité Mixte de Recherches, IRD 224-CNRS 5290 Université de Montpellier, Montpellier, France.
Nikita Stepanskyy: CREEC/CANECEV (CREES), MIVEGEC, Unité Mixte de Recherches, IRD 224-CNRS 5290 Université de Montpellier, Montpellier, France.
Beata Ujvari: CREEC/CANECEV (CREES), MIVEGEC, Unité Mixte de Recherches, IRD 224-CNRS 5290 Université de Montpellier, Montpellier, France. ORCID
Rodrigo Hamede: School of Biological Sciences, University of Tasmania, Hobart, Australia.
Antoine M Dujon: CREEC/CANECEV (CREES), MIVEGEC, Unité Mixte de Recherches, IRD 224-CNRS 5290 Université de Montpellier, Montpellier, France. ORCID
Jácint Tökölyi: MTA-DE "Momentum" Ecology, Evolution and Developmental Biology Research Group, Department of Evolutionary Zoology, University of Debrecen, Debrecen, Hungary. ORCID
Fréderic Thomas: CREEC/CANECEV (CREES), MIVEGEC, Unité Mixte de Recherches, IRD 224-CNRS 5290 Université de Montpellier, Montpellier, France. ORCID
While host phenotypic manipulation by parasites is a widespread phenomenon, whether tumors, which can be likened to parasite entities, can also manipulate their hosts is not known. Theory predicts that this should nevertheless be the case, especially when tumors (neoplasms) are transmissible. We explored this hypothesis in a cnidarian model system, in which spontaneous tumors can occur in the lab, and lineages in which such neoplastic cells are vertically transmitted (through host budding) have been maintained for over 15 years. Remarkably, the hydras with long-term transmissible tumors show an unexpected increase in the number of their tentacles, allowing for the possibility that these neoplastic cells can manipulate the host. By experimentally transplanting healthy as well as neoplastic tissues derived from both recent and long-term transmissible tumors, we found that only the long-term transmissible tumors were able to trigger the growth of additional tentacles. Also, supernumerary tentacles, by permitting higher foraging efficiency for the host, were associated with an increased budding rate, thereby favoring the vertical transmission of tumors. To our knowledge, this is the first evidence that, like true parasites, transmissible tumors can evolve strategies to manipulate the phenotype of their host.
