A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly

Haruhiko Fujiwara and colleagues report the genome sequences of two swallowtail butterfly species, Papilio xuthus and Papilio polytes , and the identification of a chromosomal inversion underlying the mimetic phenotype in P. polytes females. The inversion interacts with dsx to control mimetic coloration patterns in an allele-specific manner. In Batesian mimicry, animals avoid predation by resembling distasteful models. In the swallowtail butterfly Papilio polytes , only mimetic-form females resemble the unpalatable butterfly Pachliopta aristolochiae . A recent report showed that a single gene, doublesex ( dsx ), controls this mimicry 1 ; however, the detailed molecular mechanisms remain unclear. Here we determined two whole-genome sequences of P. polytes and a related species, Papilio xuthus , identifying a single ∼130-kb autosomal inversion, including dsx , between mimetic ( H -type) and non-mimetic ( h -type) chromosomes in P. polytes . This inversion is associated with the mimicry-related locus H , as identified by linkage mapping. Knockdown experiments demonstrated that female-specific dsx isoforms expressed from the inverted H allele ( dsx ( H )) induce mimetic coloration patterns and simultaneously repress non-mimetic patterns. In contrast, dsx ( h ) does not alter mimetic patterns. We propose that dsx ( H ) switches the coloration of predetermined wing patterns and that female-limited polymorphism is tightly maintained by chromosomal inversion.