Abstract
In many butterflies, the ancestral trichromatic insect colour vision, based on UV-, blue- and green-sensitive photoreceptors, is extended with red-sensitive cells. Physiological evidence for red receptors has been missing in nymphalid butterflies, although some species can discriminate red hues well. In eight species from genera Archaeoprepona, Argynnis, Charaxes, Danaus, Melitaea, Morpho, Heliconius and Speyeria, we found a novel class of green-sensitive photoreceptors that have hyperpolarizing responses to stimulation with red light. These green-positive, red-negative (G+R–) cells are allocated to positions R1/2, normally occupied by UV and blue-sensitive cells. Spectral sensitivity, polarization sensitivity and temporal dynamics suggest that the red opponent units (R–) are the basal photoreceptors R9, interacting with R1/2 in the same ommatidia via direct inhibitory synapses. We found the G+R– cells exclusively in butterflies with red-shining ommatidia, which contain longitudinal screening pigments. The implementation of the red colour channel with R9 is different from pierid and papilionid butterflies, where cells R5–8 are the red receptors. The nymphalid red-green opponent channel and the potential for tetrachromacy seem to have been switched on several times during evolution, balancing between the cost of neural processing and the value of extended colour information.
Highlights
A body of molecular, physiological and behavioural evidence gathered from diverse butterfly species is suggesting that butterflies possess good colour vision capabilities [1]
We have examined the retinae of 10 nymphalid species by intracellular electrophysiological measurements from single photoreceptor cells, using stimulation with narrow-band spectral light, selective adaptation and current injection
The novel green-sensitive cells (G+)R− photoreceptor class is the retinal basis for green-red colour opponency
Summary
A body of molecular, physiological and behavioural evidence gathered from diverse butterfly species is suggesting that butterflies possess good colour vision capabilities [1]. The ancestral trichromatic retinal architecture is based upon UV-, blue- and green-sensitive photoreceptors and allows for colour discrimination from UV to green, but not in the red colour range [2]. Physiological evidence for redsensitive photoreceptors in the largest butterfly family Nymphalidae has so far been missing; a single study reported red-sensitive interneurons in Heliconius [4]. While some brushfoot butterflies retain the ancestral trichromatic plan [5,6,7,8,9], behavioural evidence for colour discrimination in the red wavelength range suggests the presence of a functional red colour channel in some species such as Danaus plexippus or Heliconius erato [10,11]. We screened diverse groups of nymphalid butterflies for physiological proof of red-sensitive photoreceptors
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
