Multiple mechanisms of photoreceptor spectral tuning following loss of UV color vision inHeliconiusbutterflies

Abstract

Color vision modifications occur in animals via a process known as spectral tuning. In Heliconius butterflies, a genus-specific UVRh opsin duplication led to the evolution of UV color discrimination in Heliconius erato females, a rare trait among butterflies. In the H. melpomene and H. ismenius lineages, the UV2 receptor has been lost. Here we compare how loss of the UV2 photoreceptor has altered the visual system of these butterflies. We compare visual system evolution in three Heliconius butterfly species using a combination of intracellular recordings, ATAC-seq, and antibody staining. We identify several spectral tuning mechanisms including adaptive evolution of opsins, deployment of two types of filtering pigments, and co-expression of two distinct opsins in the same cell. Our data show that opsin gain and loss is driving rapid divergence in Heliconius visual systems via tuning of multiple spectral classes of photoreceptor in distinct lineages, potentially contributing to ongoing speciation in this genus.

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

“…Microelectrode dye injection confirmed that G+R− cells were indeed R1/2 (figure 1b; electronic supplementary material, figure S3). In D. plexippus, H. erato and M. athalia some G+ R− R1/2 cells had broadened sensitivity with two maxima, in the green and blue (figure 2b,c; electronic supplementary material, figure S2), in line with the recently found coexpression of blue and LW opsins in Heliconius R1&2 [19]. Varying levels of opsin co-expression may be the main cause for the different spectral sensitivities of G+R− cells in different species (electronic supplementary material, figure S2).…”

“…The presence of ommatidia with red screening pigments is not only correlated with the finding of G+R− cells, but seems to be a requirement for the red-shifted sensitivity of R9 and hence the implementation of the extended colour discrimination range. The red admiral ( Vanessa atalanta ) has uniform orange eyeshine [ 10 ], indicative of red screening pigment absence, and a limited ability for discrimination of red colours, while the red postman ( Heliconius erato ) has a mosaic with about 50% red-shining ommatidia, and a behaviourally confirmed extended colour discrimination range [ 7 , 10 , 17 , 19 ]. We did not find any UV- or blue-sensitive R1/2 cells receiving opponent signals from red-sensitive cells.…”

Opponent processing in the retinal mosaic of nymphalid butterflies

“…Many nymphalids have a non-uniform eye shine with red-reflecting ommatidia [25,29], which may indicate the presence of more than three ommatidial types. For instance, in some Heliconius butterflies, R1,2 can express another type of UV opsin (UV2, due to opsin duplication) [14] or a green-absorbing (G; LW) opsin [30], which leads to the expansion of possible ommatidial types and a complex retinal mosaic. The LW opsin-expressing R1,2 likely reside in the red ommatidia, which furthermore contain a functional, red-sensitive R9 that inhibits the green-sensitive vertical cells [7].…”

Opponent processing in the retinal mosaic of nymphalid butterflies

“…Many nymphalids have a non-uniform eye shine with red-reflecting ommatidia [25,29], which may indicate the presence of more than three ommatidial types. For instance, in some Heliconius butterflies, R1&2 can express another type of UV opsin (UV2, due to opsin duplication) [14] or a green-absorbing (G; long wavelength, LW) opsin [30], which leads to the expansion of possible ommatidial types and a complex retinal mosaic. Those R1&2 that express LW opsin likely reside in the red ommatidia, which furthermore contain a functional, red-sensitive R9 that inhibits the green-sensitive vertical cells [7].…”