Red-green opponency in the long visual fibre photoreceptors of brushfoot butterflies (Nymphalidae)

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 hyperpolarising
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,
polarisation 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 containing
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.