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Background  Sex determination relies on a hierarchically structured network of genes, and is one of the most plastic processes in evolution. The evolution of sex-determining genes within a network, by neo- or sub-functionalization, also requires the regulatory landscape to be rewired to accommodate these novel gene functions. We previously showed that in medaka fish, the regulatory landscape of the master male-determining gene  dmrt1bY  underwent a profound rearrangement, concomitantly with acquiring a dominant position within the sex-determining network. This rewiring was brought about by the exaptation of a transposable element (TE) called  Izanagi , which is co-opted to act as a silencer to turn off the  dmrt1bY  gene after it performed its function in sex determination.    Results  We now show that a second TE,  Rex1 , has been incorporated into  Izanagi . The insertion of  Rex1  brought in a preformed regulatory element for the transcription factor Sox5, which here functions in establishing the temporal and cell-type-specific expression pattern of  dmrt1bY . Mutant analysis demonstrates the importance of Sox5 in the gonadal development of medaka, and possibly in mice, in a  dmrt1bY -independent manner. Moreover, Sox5 medaka mutants have complete female-to-male sex reversal.    Conclusions  Our work reveals an unexpected complexity in TE-mediated transcriptional rewiring, with the exaptation of a second TE into a network already rewired by a TE. We also show a dual role for Sox5 during sex determination: first, as an evolutionarily conserved regulator of germ-cell number in medaka, and second, by de novo regulation of  dmrt1  transcriptional activity during primary sex determination due to exaptation of the Rex1 transposable element.    Electronic supplementary material  The online version of this article (10.1186/s12915-018-0485-8) contains supplementary material, which is available to authorized users.

Sox5 is involved in germ-cell regulation and sex determination in medaka following co-option of nested transposable elements