Mimetic butterfly wings through mimetic butterfly eyes: Evidence that brightness vision helpsAdelpha fessoniaidentify potential mates

Abstract

Müllerian mimicry arises when conspicuous unprofitable species share a color pattern, gaining protection because predators learn and avoid the warning colors of a bad meal. Coloration also has other functions. For example, how does one butterfly recognize another of the same species to mate? Color vision is thought to play a key role in driving the evolution of animal color patterns via natural or sexual selection, while achromatic (brightness) vision is often ignored as a possible mechanism for species recognition. Here we find evidence that brightness vision rather than color vision helps some mimeticAdelphabutterflies identify potential mates while their co-mimetic wing coloration is indiscriminable to avian predators. To do so, we examined the visual system of the butterflyAdelpha fessonia,a member of a diverse genus of butterflies comprising over 200 taxa with multiple mimicry complexes. We characterized the photoreceptors ofA. fessoniausing RNA-seq, eyeshine, epi-microspectrophotometry, optophysiology and comparative sequence analysis. We used these data to model the discriminability of wing color patches ofA. fessoniain relation to those of its sympatric co-mimic,A. basiloides, throughA. fessoniaand avian visual systems. AdultA. fessoniaeyes express three visual opsin mRNAs encoding long wavelength-, blue-, and ultraviolet-sensitive rhodopsins with peak sensitivities (λmaxvalues) at 530 nm, ∼431 nm and 355 nm, respectively. Red-reflecting ommatidia, found in other nymphalid butterflies such as monarchs andHeliconiusbutterflies, are absent from the eyeshine ofA. fessonia, indicatingA. fessoniaeyes lack heterogeneously expressed red filtering pigments and red-sensitive photoreceptors. Visual models ofAdelphawing coloration suggests thatA. fessoniacan distinguish conspecifics from co-mimics using achromatic vision. Avian predators, on the other hand, cannot distinguish between co-mimic wing color using either chromatic or achromatic cues. Taken together, these results suggest that mimetic wing color patterns and visual systems have evolved in tandem to maintain mimicry while avoiding mating between look-alike species.