Sexual Dimorphism and Retinal Mosaic Diversification following the Evolution of a Violet Receptor in Butterflies

Abstract

Numerous animal lineages have expanded and diversified the opsin-based photoreceptors in their eyes underlying color vision behavior. However, the selective pressures giving rise to new photoreceptors and their spectral tuning remain mostly obscure. Previously, we identified a violet receptor (UV2) that is the result of a UV opsin gene duplication specific to Heliconius butterflies. At the same time the violet receptor evolved, Heliconius evolved UV-yellow coloration on their wings, due to the pigment 3-hydroxykynurenine (3-OHK) and the nanostructure architecture of the scale cells. In order to better understand the selective pressures giving rise to the violet receptor, we characterized opsin expression patterns using immunostaining (14 species) and RNA-Seq (18 species), and reconstructed evolutionary histories of visual traits in five major lineages within Heliconius and one species from the genus Eueides. Opsin expression patterns are hyperdiverse within Heliconius. We identified six unique retinal mosaics and three distinct forms of sexual dimorphism based on ommatidial types within the genus Heliconius. Additionally, phylogenetic analysis revealed independent losses of opsin expression, pseudogenization events, and relaxation of selection on UVRh2 in one lineage. Despite this diversity, the newly evolved violet receptor is retained across most species and sexes surveyed. Discriminability modeling of behaviorally preferred 3-OHK yellow wing coloration suggests that the violet receptor may facilitate Heliconius color vision in the context of conspecific recognition. Our observations give insights into the selective pressures underlying the origins of new visual receptors.

The appearance of mimetic Heliconius butterflies to predators and conspecifics

“…For Heliconius vision, JND values within conspecifics were calculated only between erato clade wings, as the existing visual data is from H. erato eyes and the melpomene/cydno clade has a different retinal mosaic (McCulloch et al. ).…”

“…JND values were calculated for all pairwise comparisons within comimics and within conspecifics, separated by color and side of the wing, for Heliconius, UVS and VS vision models. For Heliconius vision, JND values within conspecifics were calculated only between erato clade wings, as the existing visual data is from H. erato eyes and the melpomene/cydno clade has a different retinal mosaic (McCulloch et al 2017).…”

“…The compound eye of H. erato is sexually dimorphic and males express only UVRh2 while females express both UV opsins in separate photoreceptors (McCulloch et al. , ). Differences in photoreceptor ratios therefore might play a role in sexual selection and identification of mates.…”

“…In H. erato, two UV opsins confer sensitivity to ß355 nm (UVRh1) and ß398 nm (UVRh2), and it has been suggested that this might allow a greater degree of discrimination of yellow patches (Briscoe et al 2010;Bybee et al 2012). The compound eye of H. erato is sexually dimorphic and males express only UVRh2 while females express both UV opsins in separate photoreceptors (McCulloch et al 2016(McCulloch et al , 2017. Differences in photoreceptor ratios therefore might play a role in sexual selection and identification of mates.…”

Evolution of Phototransduction Genes in Lepidoptera

“…Numerous studies have focused on characterizing the opsins expressed in photoreceptor cells and their arrangement across the compound eye (Spaethe & Briscoe 2005;Henze et al 2012;Futahashi et al 2015;McCulloch et al 2016;Perry et al 2016;Giraldo-Calderón et al 2017;McCulloch et al 2017). Although a large focus is on the opsins, changes in the 5 While gene trees tell the probable evolutionary history of gene families, gene expression data is a step towards inferring gene function.…”