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 examined the spatial pattern of opsin expression and photoreceptor spectral sensitivities in Heliconius erato, a nymphalid with duplicate ultraviolet opsin genes, UVRh1 and UVRh2. We found 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 (λmax=356, ∼390 and 470 nm), while males have two (λmax=390 and ∼470 nm). We also found two long wavelength-sensitive photoreceptors (green, λmax∼555 nm, and red, λmax∼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.
The authors declare no competing or financial interests.
K.J.M., D.O. and A.D.B. conceived of the study and set up the recording equipment. K.J.M. and A.D.B. made new reagents. K.J.M. performed antibody staining, imaging, cell counts, intracellular recordings, and analysis. A.D.B. and D.O. assisted with spectral sensitivity analysis. K.J.M. and A.D.B. wrote the manuscript and D.O. provided input.
This work was funded by a National Science Foundation (NSF) Graduate Research Fellowship to K.J.M. and National Science Foundation IOS-1257627 to A.D.B. This work was made possible, in part, through access to the confocal facility of the optical biology shared resource of the Cancer Center support grant (CA-62203) at the University of California, Irvine.
Supplementary information available online at http://jeb.biologists.org/lookup/doi/10.1242/jeb.136523.supplemental
- Received December 16, 2015.
- Accepted May 23, 2016.
- © 2016. Published by The Company of Biologists Ltd