Transposons drove the evolution of a male sex-determining gene from a female gene with deep introgression across cichlids.

Abstract

Sex-determination mechanisms and their master regulators are diverse among vertebrates. Components of downstream regulatory pathways can sometimes be co-opted as new upstream triggers. Here, we report a notable finding of cross-pathway recruitment: A gene from the female differentiation cascade was repurposed as a male master sex-determining (MSD) gene. We identify <i>figlaY</i>, a Y-linked truncated duplicate of the female-associated <i>figla</i>, as the MSD gene in Mozambique tilapia. <i>figlaY</i> originated through duplication and translocation in an ancestral cichlid lineage and subsequently introgressed into multiple lineages. Transposable elements facilitated <i>figlaY</i>'s emergence by mediating duplication, truncation, and regulatory rewiring. Functionally, FIGLAY suppresses the <i>zp2</i> promoter activated by the FIGLA/E12 heterodimer, acting as a dominant-negative regulator that inhibits ovarian differentiation and promotes testis development. This discovery reveals an unprecedented evolutionary route from female to male sex determination, i.e., a "genetic defection" from an initially female pathway. This previously unknown mechanism expands the vertebrate sex-determination toolkit.