Ancient balancing selection at tan underlies female colour dimorphism in Drosophila erecta.

Amir Yassin,Henry Chung,Michel Veuille,John E. Pool,Jean R. David,Héloïse Bastide

doi:10.1038/ncomms10400

Abstract

Dimorphic traits are ubiquitous in nature, but the evolutionary factors leading to dimorphism are largely unclear. We investigate a potential case of sexual mimicry in Drosophila erecta, in which females show contrasting resemblance to males. We map the genetic basis of this sex-limited colour dimorphism to a region containing the gene tan. We find a striking signal of ancient balancing selection at the ‘male-specific enhancer' of tan, with exceptionally high sequence divergence between light and dark alleles, suggesting that this dimorphism has been adaptively maintained for millions of years. Using transgenic reporter assays, we confirm that these enhancer alleles encode expression differences that are predicted to generate this pigmentation dimorphism. These results are compatible with the theoretical prediction that divergent phenotypes maintained by selection can evolve simple genetic architectures.

Highlights

Dimorphic traits are ubiquitous in nature, but the evolutionary factors leading to dimorphism are largely unclear
The femalelimited colour dimorphism (FLCD) found in D. erecta and other Drosophila species is reminiscent of a classic system of sexual mimicry described in some damselfly species, in which male-mimicking females are believed to benefit from avoiding harassment by males when population densities are high[14,15]
It seems plausible that the cost of mating for females may be higher in D. erecta than in its non-FLCD relatives, in light of the species’ larger and serrated male phallus and the corresponding protective plates found in females[17]

Summary

Introduction

Dimorphic traits are ubiquitous in nature, but the evolutionary factors leading to dimorphism are largely unclear. We confirm that these enhancer alleles encode expression differences that are predicted to generate this pigmentation dimorphism These results are compatible with the theoretical prediction that divergent phenotypes maintained by selection can evolve simple genetic architectures. A surprising number of traits in natural populations shows variation that is dichotomous, rather than continuous (for example, sexes, social castes, colour morphs, left–right asymmetry), and these dimorphisms can have either a complex or simple genetic architecture[2,3,4]. Our results support a hypothesis in which long-term balancing selection on female colour morphs yielded a simple genetic architecture involving the modification of a sexually dimorphic enhancer

Methods

Results

Conclusion