Transposable element insertions are associated with Batesian mimicry in the pantropical butterfly Hypolimnas misippus

Abstract

Hypolimnas misippus is a Batesian mimic of the toxic African Queen butterfly (Danaus chrysippus). Female H. misippus butterflies use two major wing patterning loci (M and A) to imitate the four colour morphs of D. chrysippus found in different regions of Africa. In this study, we examine the evolution of the M locus and identify it as an example of adaptive atavism. This phenomenon involves a morphological reversion to an ancestral character that results in an adaptive phenotype. We show that H. misippus has re-evolved a wing pattern present in other Hypolimnas species for Batesian mimicry of a D. chrysippus morph. Using haplotagging, a linked-read sequencing technology, we discover two large transposable element (TE) insertions located at the M locus and establish that these insertions are present in the dominant allele responsible for producing the ancestral and mimetic phenotype. By conducting a comparative analysis involving additional Hypolimnas species, we demonstrate that the dominant allele is derived. This suggests that the TEs disrupt a cis-regulatory element, leading to the reversion to an ancestral phenotype that is then utilized for Batesian mimicry of a distinct model, a different morph of D. chrysippus. Our findings present a compelling instance of convergent evolution and adaptive atavism, in which the same pattern element has independently evolved multiple times in Hypolimnas butterflies, repeatedly playing a role in Batesian mimicry of diverse model species.