Simple and complex, sexually dimorphic retinal mosaic of fritillary butterflies

Abstract

Butterflies have variable sets of spectral photoreceptors that underlie colour vision. The photoreceptor organization may be optimized for the detection of body coloration. Fritillaries (Argynnini) are nymphalid butterflies exhibiting varying degrees of sexual dimorphism in wing coloration. In two sister species, the females have orange (Argynnis paphia) and dark wings (Argynnis sagana), respectively, while the males of both species have orange wings with large patches of pheromone-producing androconia. In spite of the differences in female coloration, the eyes of both species exhibit an identical sexual dimorphism. The female eyeshine is uniform yellow, while the males have a complex retinal mosaic with yellow and red-reflecting ommatidia. We found the basic set of ultraviolet-, blue- and green-peaking photoreceptors in both sexes. Males additionally have three more photoreceptor classes, peaking in green, yellow and red, respectively. The latter is the basal R9, indirectly measured through hyperpolarizations in the green-peaking R1-2. In many nymphalid tribes, including the closely related Heliconiini, the retinal mosaic is complex in both sexes. We hypothesize that the simple mosaic of female Argynnini is a secondary reduction, possibly driven by the use of olfaction for intraspecific recognition, whereas vision remains the primary sense for the task in the males. This article is part of the theme issue 'Understanding colour vision: molecular, physiological, neuronal and behavioural studies in arthropods'.

Keywords: nymphalidae; photoreceptor; red receptor; retina; sexual dimorphism.

Figure 1.

External appearance of males (a–c) and females (d–f) of Argynnis sagana (a,d) and Argynnis paphia (b,c,e,f). (a,b,d,e) Young, (c,f) old specimens. White arrowheads indicate androconia (dark rows of scales in male forewings). Scale bar, 1 cm. Pictures by K.A. (a,d), Iain Leach (b,e), and Paul J. Raven (c,f).

Figure 2.

Eyeshine and pigments in the eyes of fritillaries. (a–d) Eyeshine in the central region of the eye of (a) Argynnis paphia female, (b) Argynnis paphia male, (c) Argynnis sagana female, and (d) Argynnis sagana male. Illumination colour/wavelength indicated on the left. (e,f) Longitudinal symbolic schemes (not to scale) of an unpigmented (e) and a red-pigmented (f) ommatidium. Schematic transverse sections of a red-pigmented ommatidium shown to the right; distal screening pigment (dp), rhabdom (rh), proximal screening pigment (pp), brown pigment (bp), tracheolar multilayer (tr). (g) Ten micrometre thick unstained distal transverse section of a single ommatidium, A. sagana female. (h) Semithin (2 µm) unstained transverse section of the proximal rhabdom of a male A. paphia, brightfield; brown pigment in the glial cells between the ommatidia; in some ommatidia (red circles), red pigments are apposed to the rhabdom from the lateral sides. (i,j,k) Same specimen, semithin (2 µm) unstained longitudinal section; pigmented ommatidium (up arrow); unpigmented ommatidium (down arrow); tracheole (asterisk); brown pigment (circle); (i) brightfield; (j) phase constrast, rhabdoms appear dark; (k) epi-fluorescence (cyan, UV excitation; magenta, blue excitation), autofluorescence of the left rhabdom is blocked by the red pigment. (l) Absorbance of the brown and the red pigment measured in 2 µm thick sections (mean ± s.e.m., n = 20 regions of interest (ROIs)); brown pigment (divided by 3, bp/3); distal red pigment (dp); proximal red pigment in transverse sections (pp-t); proximal red pigment in longitudinal sections (pp-l); peak wavelengths of green- and red-sensitive photoreceptors are indicated (green and red lines).

Figure 3.

Spectral sensitivity of the photoreceptors in female (a,d) and male (b,c,e,f), Argynnis paphia (a–c) and Argynnis sagana (d–f). (a,b,d,e) basic set of U (pink), B (blue) and G (green curve) receptors in both sexes; (c,f) expanded set of B+Y– (teal), Y (orange), G+R– (turquoise) and R (red curve) receptors in males; (f) Dotted red curve, putative sensitivity of R receptor, curve copied from (c); n indicates number of analysed cells, λ_max indicates peak sensitivity wavelength in nm.