Compound eyes of the small white butterfly Pieris rapae have three distinct classes of red photoreceptors
The two subspecies of the small white butterfly, the European Pieris rapae rapae and the Asian P. r. crucivora, differ in wing colouration. Under ultraviolet light, the wings of both male and female P. r. rapae appear dark, whereas the wings of male P. r. crucivora are dark and those of females are bright. It has been hypothesized that these sexually dimorphic wing reflections in P. r. crucivora may have induced the evolution of a fluorescing-screening pigment in the violet-opsin-expressing photoreceptors of males, thus facilitating greater wavelength discrimination near 400 nm. Comparing the compound eyes of the two subspecies using genetic, microscopical, spectrographic, and histological methods revealed no differences that would meaningfully affect photoreceptor sensitivity, suggesting that the fluorescing-screening pigment did not evolve in response to sexually dimorphic wing reflections. Our investigation further revealed that (i) the peri-rhabdomal reddish-screening pigments differ among the three ommatidial types; (ii) each of the ommatidial types exhibits a unique class of red photoreceptor with a distinct spectral peak; and (iii) the blue, green, and red photoreceptors of P. rapae exhibit a polarization sensitivity > 2, with red photoreceptors allowing for a two-channel opponency form of polarization sensitivity.
KeywordsSpectral sensitivity Polarization sensitivity Fluorescence Pigments Phylogeny
We thank Atsuko Matsushita for assistance and instruction with microscopy and histology, and the UBC Bioimaging Facility for assistance with electron microscopy. We also thank Doekele G. Stavenga and two anonymous reviewers who provided most helpful and constructive comments and advice on earlier drafts of this paper.
Compliance with ethical standards
Conflict of interest
The NSERC-Industrial Research Chair to GG was supported by Scotts Canada Ltd. as the industrial partner.
This study was supported by an Alexander Graham Bell Canadian Graduate Scholarship to AB, by the KAKENHI of the Japan Society for the Promotion of Science (JSPS; #26251036, 18H05273 to KA; #2604764 to PP), and by an NSERC-Industrial Research Chair to GG.
- Arikawa K, Mizuno S, Scholten DGW, Kinoshita M, Seki T, Kitamoto J, Stavenga DG (1999a) An ultraviolet absorbing pigment causes a narrow-band violet receptor and a single-peaked green receptor in the eye of the butterfly Papilio. Vis Res 39:1–8. https://doi.org/10.1016/S0042-6989(98)00070-4 CrossRefPubMedGoogle Scholar
- Ogawa Y, Kinoshita M, Stavenga DG, Arikawa K (2013) Sex-specific retinal pigmentation results in sexually dimorphic long-wavelength-sensitive photoreceptors in the eastern pale clouded yellow butterfly, Colias erate. J Exp Biol 216:1916–1923. https://doi.org/10.1242/jeb.083485 CrossRefPubMedGoogle Scholar
- Salcedo E, Zheng L, Phistry M, Bagg EE, Britt SG (2003) Molecular basis for ultraviolet vision in invertebrates. J Neurosci 23:10873–10878. https://doi.org/10.1523/JNEUROSCI.23-34-10873.2003 CrossRefPubMedPubMedCentralGoogle Scholar
- Snyder AW (1979) Physics of vision in compound eyes. In: Autrum HJ (ed) Handbook of sensory physiology, vol VII/6a. Springer, Berlin, pp 225–313Google Scholar
- Stavenga DG (2006) Invertebrate photoreceptor optics. In: Nilsson D-E, Warrant EJ (eds) Invertebrate vision. Cambridge University Press, Cambridge, pp 1–42Google Scholar
- Webb SE, Shelton AM (1988) Laboratory rearing of the imported Cabbageworm. In: New Yorks food and life sciences bulletin. New York State Agricultural Experiment Station, GenevaGoogle Scholar