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Abstract Color vision is thought to play a key role in the evolution of animal coloration, while achromatic vision is rarely considered as a mechanism for species recognition. Here we test the hypothesis that brightness vision rather than color vision helpsAdelpha fessoniabutterflies identify potential mates while their co-mimetic wing coloration is indiscriminable to avian predators. We examine the trichromatic visual system ofA. fessoniaand characterize its photoreceptors using RNA-seq, eyeshine, epi-microspectrophotometry, and optophysiology. We model the discriminability of its wing color patches in relation to those of its co-mimic,A. basiloides, throughA. fessoniaand avian eyes. Visual modeling suggests that neitherA. fessonianor avian predators can readily distinguish the co-mimics’ coloration using chromatic or achromatic vision under natural conditions. These results suggest that mimetic colors are well-matched to visual systems to maintain mimicry, and that mate avoidance between these two look-alike species relies on other cues. 

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, someHeliconiusbutterflies 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 studiedHeliconius 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 theH. charithoniagenome, we discovered thatUVRh1is present on the W chromosome, making it obligately female-specific. By knocking outUVRh1, we show that UVRh1 protein expression is absent in mutant female eye tissue, as in wild-type male eyes. A PCR survey ofUVRh1sex-linkage across the genus shows that species with female-specific UVRh1 expression lackUVRh1gDNA in males. Thus, acquisition of sex linkage is sufficient to achieve female-specific expression ofUVRh1, though this does not preclude other mechanisms, likecis-regulatory evolution from also contributing. Moreover, both this event, and mutations leading to differential UV opsin sensitivity, occurred early in the history ofHeliconius. 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).