Duplication and sub-functionalisation characterise diversification of opsin genes in the Lepidoptera

Abstract

Gene duplication is a vital process for evolutionary innovation. Functional diversification of duplicated genes is best explored in multicopy gene families such as histones, hemoglobin, and opsins. Rhodopsins are photo-sensitive proteins that respond to different wavelengths of light and contribute to diverse visual adaptations across insects. While there are several instances of gene duplications in opsin lineages, the functional diversification of duplicated copies and their ecological significance is properly characterised only in a few insect groups. We examined molecular and structural evolution that underlies diversification and sub-functionalisation of four opsin genes and their duplicated copies across 132 species of the diverse insect order-Lepidoptera. Opsins have largely evolved under purifying selection with few residues showing signs of episodic and pervasive diversifying selection. Although these do not affect overall protein structures of opsins, substitutions in key amino acids in the chromophore-binding pocket of duplicated copies might cause spectral sensitivity shifts leading to sub-functionalisation or neofunctionalisation. Duplicated copies of opsins also exhibit developmental stage-specific expression in Papilio polytes, suggesting functional partitioning during development. Together, altered spectral sensitivities owing to key substitutions and differential expression of duplicated copies across developmental stages might enable enhanced colour perception and improved discrimination across wavelengths in this highly visual insect group.

Opsin Gene Duplication in Lepidoptera: Retrotransposition, Sex Linkage, and Gene Expression

“…Differential expression of the 2 LW copies between life stages has now been shown in 2 species from different families (Noctuidae and Erebidae) and likely represents the ancestral state, although more data for species in the Nolidae family are required to confirm this. This route to subfunctionalization of opsin paralogs through changes in temporal or spatial expression has been found in other insects, for example in dragonflies, damselflies, mayflies, mosquitos, and other lepidopterans ( Futahashi et al 2015 ; Giraldo-Calderón et al 2017 ; Almudi et al 2020 ; Kuwalekar et al 2022 ; Roberts et al 2023 ). In many of these other cases, the larval and adult stages occupy very different niches and light environments (larvae are aquatic while adults are terrestrial).…”

New genome reveals molecular signatures of adaptation to nocturnality in moth-like butterflies (Hedylidae)

“…In insects, multiple cases of gene duplications and losses have been observed, owing to the strong selective pressure imposed by light availability 19,20 . Butterflies and moths (Lepidoptera) are a prime example, where duplications and color vision gene diversification is much more prevalent in diurnal species as compared to nocturnal species [21][22][23] . This diversification of color vision genes aligns with the over 100 diel transitions recorded in Lepidoptera, featuring multiple evolutionary switches between nocturnality and diurnality 24 .…”

Mimetic butterfly wings through mimetic butterfly eyes: Evidence that brightness vision helpsAdelpha fessoniaidentify potential mates

“…This is commonly found in flower foraging insects as seen in honeybees (Peitsch et al 1992), bumblebees (Spaethe and Briscoe 2005), and hawkmoths (White 2003). Typically, these photopigments are encoded by two short wave-sensitive opsin genes (UVRh and BRh) and one long wave-sensitive (LWRh) opsin gene (Briscoe 2008;Briscoe and Chittka 2001) although exceptions exist (Mulhair et al 2023;Kuwalekar et al 2022;Sondhi et al 2021). Opsin proteins together with a light-absorbing 11-cis-3-hydroxy retinal chromophore are the constituent parts of photoreceptor molecules that are sensitive to particular wavelengths of light.…”