Male manipulation impinges on social-dependent tumor suppression in Drosophila melanogaster females

Author:

Akiki Perla,Delamotte Pierre,Poidevin Mickael,van Dijk Erwin L.,Petit Apolline J. R.,Le Rouzic Arnaud,Mery Frederic,Marion-Poll Frederic,Montagne Jacques

Abstract

AbstractPhysiological status can influence social behavior, which in turn can affect physiology and health. Previously, we reported that tumor growth in Drosophila virgin females depends on the social context, but did not investigate the underlying physiological mechanisms. Here, we sought to characterize the signal perceived between tumorous flies, ultimately discovering that the tumor suppressive effect varies depending on reproductive status. Firstly, we show that the tumor suppressive effect is neither dependent on remnant pheromone-like products nor on the microbiota. Transcriptome analysis of the heads of these tumorous flies reveals social-dependent gene-expression changes related to nervous-system activity, suggesting that a cognitive-like relay might mediate the tumor suppressive effect. The transcriptome also reveals changes in the expression of genes related to mating behavior. Surprisingly, we observed that this social-dependent tumor-suppressive effect is lost in fertilized females. After mating, Drosophila females change their behavior—favoring offspring survival—in response to peptides transferred via the male ejaculate, a phenomenon called “male manipulation”. Remarkably, the social-dependent tumor suppressive effect is restored in females mated by sex-peptide deficient males. Since male manipulation has likely been selected to favor male gene transmission, our findings indicate that this evolutionary trait impedes social-dependent tumor growth slowdown.

Funder

French Government

France Génomique French National Program "Investissement d’Avenir"

CNRS, MITI-80prime interdisciplinary programs to FM, FMP and JM

Fondation ARC contre le Cancer

French league against Cancer

Publisher

Springer Science and Business Media LLC

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