Sexual dimorphism in the compound eye of Heliconius erato: a nymphalid butterfly with at least five spectral classes of photoreceptor

Most butterfly families expand the number of spectrally-distinct photoreceptors in their compound eye by opsin gene duplications together with lateral filter pigments, however most nymphalid genera have limited diversity, with only three or four spectral types of photoreceptor. Here we examine the spatial pattern of opsin expression and photoreceptor spectral sensitivities in Heliconius erato, a nymphalid with duplicate ultraviolet opsin genes, UVRh1 and UVRh2. We find that the H. erato compound eye is sexually dimorphic. Females express the two UV opsin proteins in separate photoreceptors, but males do not express UVRh1. Intracellular recordings confirmed that females have three short wavelength-sensitive photoreceptors (λ_max=356 nm, ∼390 nm and 470 nm), while males have two (λ_max=390 nm and ∼470 nm). We also found two long wavelength-sensitive photoreceptors (green, λ_max ∼555 nm, and red, λ_max ∼600 nm), which express the same LW opsin. The red cell's shifted sensitivity is probably due to perirhabdomal filtering pigments. Sexual dimorphism of the UV-absorbing rhodopsins may reflect the females' need to discriminate conspecifics from co-mimics. Red-green color vision may be used to detect differences in red coloration on Heliconius wings, or for host-plant identification. Among nymphalids so far investigated, only H. erato is known to possess five spectral classes of photoreceptor; sexual dimorphism of the eye via suppression of one class of opsin (here UVRh1 in males) has not—to our knowledge—been reported in any animal.