The mimetic wing pattern of Papilio polytes butterflies is regulated by a doublesex-orchestrated gene network

Abstract

The swallowtail butterfly Papilio polytes is sexually dimorphic and exhibits female-limited Batesian mimicry. This species also has two female forms, a non-mimetic form with male-like wing patterns, and a mimetic form resembling an unpalatable model, Pachliopta aristolochiae. The mimicry locus H constitutes a dimorphic Mendelian ‘supergene’, including a transcription factor gene doublesex (dsx). However, how the mimetic-type dsx (dsx-H) orchestrates the downstream gene network and causes the mimetic traits remains unclear. Here we performed RNA-seq-based gene screening and found that Wnt1 and Wnt6 are up-regulated by dsx-H during the early pupal stage and are involved in the red/white pigmentation and patterning of mimetic female wings. In contrast, a homeobox gene abdominal-A is repressed by dsx-H and involved in the non-mimetic colouration pattern. These findings suggest that dual regulation by dsx-H, induction of mimetic gene networks and repression of non-mimetic gene networks, is essential for the switch from non-mimetic to mimetic pattern in mimetic female wings.