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

Abstract

Color vision in insects is determined by signaling cascades, central to which are opsin proteins, resulting in sensitivity to light at different wavelengths. In certain insect groups, lineage-specific evolution of opsin genes, in terms of copy number, shifts in expression patterns, and functional amino acid substitutions, has resulted in changes in color vision with subsequent behavioral and niche adaptations. Lepidoptera are a fascinating model to address whether evolutionary change in opsin content and sequence evolution are associated with changes in vision phenotype. Until recently, the lack of high-quality genome data representing broad sampling across the lepidopteran phylogeny has greatly limited our ability to accurately address this question. Here, we annotate opsin genes in 219 lepidopteran genomes representing 33 families, reconstruct their evolutionary history, and analyze shifts in selective pressures and expression between genes and species. We discover 44 duplication events in opsin genes across ∼300 million years of lepidopteran evolution. While many duplication events are species or family specific, we find retention of an ancient long-wavelength-sensitive (LW) opsin duplication derived by retrotransposition within the speciose superfamily Noctuoidea (in the families Nolidae, Erebidae, and Noctuidae). This conserved LW retrogene shows life stage–specific expression suggesting visual sensitivities or other sensory functions specific to the early larval stage. This study provides a comprehensive order-wide view of opsin evolution across Lepidoptera, showcasing high rates of opsin duplications and changes in expression patterns.

Evolution of Opsin Genes in Caddisflies (Insecta: Trichoptera)

“…We discovered variety in the number of opsin genes across species, particularly in the LW and SW opsins. Our results suggest that caddisflies have evolved a diverse range of opsins, likely driven by life history strategies and ambient light conditions as has been hypothesized in other insect orders (Briscoe et al, 2010;Feuda et al, 2016;French et al, 2015, Futahashi et al, 2015Guignard et al, 2022;Lord et al, 2016;Mulhair et al, 2023;Sharkey et al, 2017;Sondhi et al, 2021;Suvorov et al, 2017).…”

“…Opsin evolution has been more thoroughly studied in Lepidoptera, the sister order to Trichoptera (Briscoe et al, 2010; Feuda et al, 2016; Finkbeiner & Briscoe, 2021; Frentiu et al, 2007; Guignard et al, 2022; Macias-Muñoz et al, 2019; Mulhair et al, 2023; Sison-Mangus et al, 2006; 2008; Sondhi et al, 2021; Spaethe & Briscoe, 2004). Recent work has identified several instances of family– and species-specific duplications of visual opsin genes, many of which have resulted in adaptations that extend visual capacity (Frentiu et al, 2007; Mulhair et al, 2023; Sison-Mangus et al, 2006; 2008). For example, butterflies in the family Lycaenidae use both a green-shifted SW opsin and a red-shifted LW opsin to better discriminate different wavelengths (Liénard et al, 2021; Sison-Mangus et al, 2006; 2008).…”

“…The LW opsins formed two distinct clades in the opsin gene tree, a phenomenon observed in other insect orders (Feuda et al, 2016;Futahashi et al, 2015;Guignard et al, 2022;Lord et al, 2016;Mulhair et al 2023;Sharkey et al, 2017;Sharkey et al, 2023;Sondhi et al, 2021, Suvorov et al, 2017. We labeled the larger group LW1 and the smaller one LW2, with letters (e.g.…”

Diversity and Evolution of Frog Visual Opsins: Spectral Tuning and Adaptation to Distinct Light Environments

“…We used RELAX to test for relaxation and intensification of selection on the significant partitions identified by CmC. This method has successfully been applied to test for relaxed selection on opsin genes in several lineages including cichlids, bats, butterflies, and mirid bugs ( Gutierrez et al 2018a , 2018b ; Hauser et al 2021 ; Xu et al 2021 ; Mulhair et al 2023 ). The HYPHY models each automatically inferred gene trees with the GTR model, which were rerooted on Ascaphus truei prior to analyses.…”

Looking across the gap: Understanding the evolution of eyes and vision among insects

“…(B) Connections between lamina monopolar cells (L1-L5) in adjacent lamina cartridges in D. melanogaster and the parasitoid wasp Megaphragma viggianii. [1] repertoires and their expression underlies differences in spectral sensitivities, color vision, and motion detection within and among insect species [15][16][17][18] (Box 2). For example, it was recently shown that sexlinkage of UVRh1 underlies differential UV sensitivity between male and female Heliconius butterflies.…”