Sex-linked gene traffic underlies the acquisition of sexually dimorphic UV color vision in <i>Heliconius</i> butterflies

Abstract

The acquisition of novel sexually dimorphic traits poses an evolutionary puzzle: How do new traits arise and become sex-limited? Recently acquired color vision, sexually dimorphic in animals like primates and butterflies, presents a compelling model for understanding how traits become sex-biased. For example, some <i>Heliconius</i> butterflies uniquely possess UV (ultraviolet) color vision, which correlates with the expression of two differentially tuned UV-sensitive rhodopsins, UVRh1 and UVRh2. To discover how such traits become sexually dimorphic, we studied <i>Heliconius charithonia</i>, which exhibits female-specific UVRh1 expression. We demonstrate that females, but not males, discriminate different UV wavelengths. Through whole-genome shotgun sequencing and assembly of the <i>H. charithonia</i> genome, we discovered that <i>UVRh1</i> is present on the W chromosome, making it obligately female-specific. By knocking out <i>UVRh1</i>, we show that UVRh1 protein expression is absent in mutant female eye tissue, as in wild-type male eyes. A PCR survey of <i>UVRh1</i> sex-linkage across the genus shows that species with female-specific UVRh1 expression lack <i>UVRh1</i> gDNA in males. Thus, acquisition of sex linkage is sufficient to achieve female-specific expression of <i>UVRh1</i>, though this does not preclude other mechanisms, like <i>cis</i>-regulatory evolution from also contributing. Moreover, both this event, and mutations leading to differential UV opsin sensitivity, occurred early in the history of <i>Heliconius</i>. These results suggest a path for acquiring sexual dimorphism distinct from existing mechanistic models. We propose a model where gene traffic to heterosomes (the W or the Y) genetically partitions a trait by sex before a phenotype shifts (spectral tuning of UV sensitivity).