A bio-inspired understanding of complex colour vision.

The spectacular diversity of butterfly wing colouration is easy for us to appreciate, yet relatively little is known about how butterflies themselves perceive different colours. The eyes of most butterfly species contain three different colour receptors, thereby affording the ability for trichromatic colour vision (akin to humans, albeit with a different range of colour sensitivity). Recent findings have however revealed that some butterflies possess an additional red colour receptor, and therefore have the ability for tetrachromatic vision. Compared to trichromatic colour vision, tetrachromacy allows for finer-scale judgements across a broader range of colours. It is likely, however, that this ability for enhanced colour vision will come at a cost to other features of eye performance, such as visual resolution and eye speed. Additionally, a tetrachromatic eye may be more energetically costly to run, and will produce outputs that require greater neural capacity to process. These considerations imply that a species should only invest in tetrachromacy if colour vision is paramount to their ability for survival and/or reproduction.

We set out to explore the occurrence of tetrachromacy across Australian members the nymphaline subfamily of butterflies, and to investigate whether its presence has been driven by characteristic features of ecology and/or behaviour. Butterflies in this group reside in diverse habitats and showcase a great diversity of wing colouration. Importantly, the males of different nymphaline species also characteristically pursue one of two different strategies for locating mates. The males of “perching” species seek to locate females from a stationary position, either on the ground or on fringing vegetation, whereas the males of “patrolling” species actively search by flying around their mating habitat.

Theoretically, these two different strategies are likely to demand different visual abilities. Whereas the detection of females from a stationary perch should demand high visual acuity and a ‘fast’ eye, the same task for patrolling species should instead place greater priority upon colour discrimination. We therefore predicted that tetrachromatic vision should be more prevalent among patrolling species. Perching species, on the other hand, should be more likely to stick with trichromacy yet have ‘faster’ eyes which are better suited to the detection of movement. 

We sourced multiple live individuals of five perching species (Hypolimnas bolina, H. alimena, Junonia hedonia, Yoma sabina & Doleschallia bisaltide) and five patrolling species (Cethosia penthesilia, C. biblis, Cupha prosope, Tirumala hamatus & Danaus plexippus) for this study. We assessed their ability for colour vision using telemicroscopy to image eyeshine, a new high-throughput method that overcomes the limitations of traditional electrophysiological and molecular methods. This was coupled with electrophysiology to measure critical flicker-fusion frequency, which is a robust measure of eye speed and therefore the ability for motion detection. 

The balance of our work indicates that patrolling butterfly species are more likely to possess an additional class of red photoreceptors in their eyes, and therefore have the potential for tetrachromatic vision. This supports the hypothesis that patrolling male butterflies rely more heavily upon colour vision for visual mate detection than the males of perching species. Alongside this finding, the data indicate that males of perching species have high critical flicker fusion values, and therefore possess faster eyes, which is consistent with the hypothesis that these males rely more heavily upon motion vision for mate detection. These findings represent – to our knowledge – the first demonstration that adaptations for colour versus motion vision can trade-off across species in a manner determined by their ability to seek mating opportunities.