Data from: Sex-linked gene traffic underlies the acquisition of sexually dimorphic UV color vision in Heliconius butterflies

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 Heliconius 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 Heliconius
charithonia, 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
H. charithonia genome, we discovered that UVRh1 is present on the W
chromosome, making it obligately female-specific. By knocking out UVRh1,
we show that UVRh1 protein expression is absent in mutant female eye
tissue, as in wild-type male eyes. A PCR survey of UVRh1 sex-linkage
across the genus shows that species with female-specific UVRh1 expression
lack UVRh1 gDNA in males. Thus, acquisition of sex linkage is sufficient
to achieve female-specific expression of UVRh1, though this does not
preclude other mechanisms, like cis-regulatory evolution from also
contributing. Moreover, both this event, and mutations leading to
differential UV opsin sensitivity, occurred early in the history of
Heliconius. 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).