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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 120; no. 33; p. e2301411120
• Main Authors: Chakraborty, Mahul, Lara, Angelica Guadalupe, Dang, Andrew, McCulloch, Kyle J, Rainbow, Dylan, Carter, David, Ngo, Luna Thanh, Solares, Edwin, Said, Iskander, Corbett-Detig, Russell B, Gilbert, Lawrence E, Emerson, J J, Briscoe, Adriana D
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 15.08.2023
• Subjects: Animals; Biological Sciences; Butterflies & moths; Butterflies - genetics; Butterflies - metabolism; Color vision; Color Vision - genetics; Eye - metabolism; Female; Females; Gene sequencing; Genomes; Heliconius; Males; Opsins - genetics; Opsins - metabolism; Phenotypes; Rhodopsin - metabolism; Sensitivity; Sex linkage; Sexual dimorphism; Traffic models; W chromosomes; Wavelengths; sex chromosome; butterfly; color vision; genome assembly; opsin
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2301411120

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