Parallel evolution of Batesian mimicry supergene in two <i>Papilio</i> butterflies, <i>P. polytes</i> and <i>P. memnon</i>.

Abstract

Batesian mimicry protects animals from predators when mimics resemble distasteful models. The female-limited Batesian mimicry in <i>Papilio</i> butterflies is controlled by a supergene locus switching mimetic and nonmimetic forms. In <i>Papilio polytes</i>, recent studies revealed that a highly diversified region (HDR) containing <i>doublesex</i> (<i>dsx</i>-HDR) constitutes the supergene with dimorphic alleles and is likely maintained by a chromosomal inversion. In the closely related <i>Papilio memnon</i>, which exhibits a similar mimicry polymorphism, we performed whole-genome sequence analyses in 11 butterflies, which revealed a nearly identical <i>dsx</i>-HDR containing three genes (<i>dsx</i>, <i>Nach-like</i>, and <i>UXT</i>) with dimorphic sequences strictly associated with the mimetic/nonmimetic phenotypes. In addition, expression of these genes, except that of <i>Nach-like</i> in female hind wings, showed differences correlated with phenotype. The dimorphic <i>dsx</i>-HDR in <i>P. memnon</i> is maintained without a chromosomal inversion, suggesting that a separate mechanism causes and maintains allelic divergence in these genes. More abundant accumulation of transposable elements and repetitive sequences in the <i>dsx</i>-HDR than in other genomic regions may contribute to the suppression of chromosomal recombination. Gene trees for Dsx, Nach-like, and UXT indicated that mimetic alleles evolved independently in the two <i>Papilio</i> species. These results suggest that the genomic region involving the above three genes has repeatedly diverged so that two allelic sequences of this region function as developmental switches for mimicry polymorphism in the two <i>Papilio</i> species. The supergene structures revealed here suggest that independent evolutionary processes with different genetic mechanisms have led to parallel evolution of similar female-limited polymorphisms underlying Batesian mimicry in <i>Papilio</i> butterflies.