Conversion of somatic sex identity in the testis induces female-specific cellular behaviors in the soma and early oocyte specification in the germline

Abstract

Establishment and maintenance of cellular sex identity is essential for reproduction. Critically, the sex identity of somatic and germline cells must correspond for sperm or oocytes to be produced, with mismatched identity causing infertility in all organisms from flies to humans. In the Drosophila testis, Chronologically inappropriate morphogenesis (Chinmo) is required for maintenance of adult male somatic identity. Loss of chinmo leads to progressive feminization of the male soma, including adoption of female-specific cell morphologies, tissue organization and gene expression. However, the degree to which this feminized soma in the male engages female-specific cellular behaviors or influences the associated XY germline is unknown. Using extended live imaging, we have visualized the process of male-to-female somatic sex conversion upon chinmo loss of function. We find that feminized soma in the testis engage cell behaviors characteristic of ovarian follicle cells (FCs), including female-specific incomplete cytokinesis, as early as one day of chinmo inhibition. In the ovary, FCs collectively migrate around the underlying germ cells to establish the elongated shape of the oocyte. Surprisingly, we find that FC-like soma in chinmo-depleted testes also engage this female-specific collective cell migration. Critically, migration of FC-like cells in the testis has the same molecular requirements as FC migration in the ovary. Depletion of the basement membrane protein Perlecan or adhesion protein Ecadherin significantly disrupts rotational migration in both the ovary and chinmo-depleted testes. Finally, we find that feminized soma non-autonomously alters sex identity of the associated XY germ cells, inducing expression of a protein required for early oocyte specification. Taken together, our work reveals a dramatic transformation of somatic cell behavior during the process of sex conversion and provides a powerful model to study soma-derived induction of oocyte identity.