Phylogenomics of Opsin Genes in Diptera Reveals Lineage-Specific Events and Contrasting Evolutionary Dynamics in Anopheles and Drosophila

Abstract

Diptera is one of the biggest insect orders and displays a large diversity of visual adaptations. Similarly to other animals, the dipteran visual process is mediated by opsin genes. While the diversity and function of these genes is well studied in key model species, a comprehensive comparative genomic study across the dipteran phylogeny is missing. Here we mined the genomes of 61 dipteran species, reconstructed the evolutionary affinities of 528 opsin genes and determined the selective pressure acting in different species. We found that opsins underwent several lineage-specific events, including an independent expansion of Long Wave Sensitive opsins in flies and mosquitoes, and numerous family-specific duplications and losses. Both the Drosophila and the Anopheles complement is derived in comparison with the ancestral dipteran state. Molecular evolutionary studies suggest that gene turnover rate, overall mutation rate, and site-specific selective pressure are higher in Anopheles than in Drosophila. Overall, our findings indicate an extremely variable pattern of opsin evolution in dipterans, showcasing how two similarly aged radiations, Anopheles and Drosophila, are characterized by contrasting dynamics in the evolution of this gene family. These results provide a foundation for future studies on the dipteran visual system.

The Gluopsins: Opsins without the Retinal Binding Lysine

“…The water flea [ 85 ], the pineal shrimp [ 86 ], dragon and damselflies [ 78 , 87 ], Limulus [ 88 ], and the mantis shrimp [ 89 ] have all gained opsins. In contrast, Drosophila melanogaster has only seven opsins, which are all rhabopsins [ 90 ]. Therefore, it must have lost the xenopsins, cilopsins, and the three paralogues of the tetraopsins since it evolved from the urbilaterian, as those are present in protostomes and deuterostomes.…”

Insect opsins and evo-devo: what have we learned in 25 years?

“…A comprehensive study in Lepidoptera found that opsin duplications are more common in diurnal species and that LWRh was duplicated more often than other opsins; specifically, LWRh has had approximately 10 duplication events, while six have occurred in BRh and three in UVRh [8]. In Diptera, the current LWRh complement in mosquitoes has been produced by an estimated 18 or 19 duplication events [109,122]. At the genetic level, signatures of gene evolution mechanisms include genes located in tandem owing to unequal crossing over or a lack of introns by retrotransposition [123].…”

“…In the water strider Gerris buenoi and in Anopheles gambiae, four and five LWRh genes, respectively, are located in tandem [110,122]. Some LWRh paralogues in moths and Anopheles are intronless and are proposed to have evolved by retrotransposition [109,111,124]. In mayflies, four LWRh genes are in genomic clusters that vary in size and have undergone rearrangement between species [112] underlie sexual dimorphism in their compound eyes [98,125].…”

Molecular advances to study the function, evolution and spectral tuning of arthropod visual opsins

“…Using this method, studies have shown faster evolution of opsins in diurnal taxa, or more specifically, adaptive evolution in UV-sensitive opsins in day-flying insects and LWS opsins of day-flying Lepidoptera [6,96,100,101]. In addition, site-specific tests of dipteran, lepidopteran and stomatopod crustacean opsins have suggested positive selection at residues outside the chromophore-binding pocket; thus, hinting at adaptive roles potentially decoupled from spectral phenotypes [100,102,103]. At the population level, studies detecting genetic variants of opsins under selection have provided insights into the genetic basis of local adaptation to light environments and speciation [30,90,104,105].…”