Evolution of Visual Performance‐associated Genes in Drosophila

Abstract

The leading model of insect vision, the fruitfly Drosophila melanogaster, is a representative of the higher Diptera (Brachycera), which excel by swift flight abilities, one of the fastest photoresponse mechanisms known and a unique form of neural superposition optics. Recent gene‐specific as well as comparative genomic investigations have begun to yield first insights into the genetic origins of Drosophila visual organisation and performance. These studies suggest discrete stages in the molecular evolution of Drosophila vision culminating in changes that enhanced the speed and versatility of diurnal vision specifically during the early evolution of the higher Diptera. Comparative genomic analysis revealed that gene duplication played an unusually important role during this final stage of Drosophila vision evolution. Select gene‐specific studies, however, also uncovered specific cis‐regulatory and coding region changes that were of key importance in the evolution the Drosophila phototransduction and retinal organisation.

Key Concepts:

  • The shared deployment of the phototransduction protein machinery in the photoreceptors of highly diversified visual organs in Drosophila (the larval eyes, ocelli and the adult compound eye) may impose adaptive constraints.

  • In contrast to the detailed mechanistic understanding of irradiance and color vision in Drosophila, the ecological role and significance of these sophisticated visual capacities is still little known in Drosophila and the related Diptera.

  • The complex retinal organisation of Drosophila is representative of all members of the species‐rich higher Diptera suggesting strong functional or developmental constraints.

  • Phylogenetic evidence indicates a correlation of significant structural and molecular changes in the visual system of Drosophila and the higher Diptera the cause of which requires further comporative research.

  • Gene duplication played a critical role in the early visual evolution of the higher Diptera.

  • The evolution of the Drosophila visual system is a paradigm example of the combined effects of cis‐regulatory and coding sequence evolution.

  • Select mechanisms of the Drosophila photoresponse are likely to differ in insect species outside the higher Diptera complicating functional gene orthology inferrences and warranting further research in other models of insect vision.

Keywords: opsin; Inac; Lazaro; Drosophila; phototransduction; gene duplication; adaptation; vision; behaviour; evolution

Figure 1.

Visual system and vision‐dependent behaviours of Drosophila. Schematic in the centre represents generic photoreceptor cell with rhabdomere pointing to the left. Single photoisomeration events leading to quantum bump formation are indicated in three microvilli.

Figure 2.

Photoreceptor mosaic of the Drosophila retina. From top to bottom: schematic overview of the retinal field, fine hatched line indicates border between the polarized light‐sensitive dorsal rim area and the main retina, heavy hatched line indicates the border between ventral and dorsal half of the retina, which contain ommatidia in mirror‐image orientation; schematic of cross‐sectional view of photoreceptor arrangement in the yellow‐ and pale‐type ommatidia, cell bodies are only indicated for R7 and R8, circles represent rhabdomeres; schematic of longitudinal view of photoreceptor arrangement in the yellow‐ and pale‐type ommatidia including projections into medulla and lamina.

Figure 3.

Phylogenetic framework of Drosophila vision evolution. The evolutionary origin of the Diptera reaches back at least 220 million years ago. At present, over 150 000 extant species have been described (for review see Courtney et al., ; Yeates and Wiegmann, ). Important phylogenetic groups for understanding the origin of Drosophila vision are the higher Diptera (Brachycera) and the lower Diptera (Nematocera). The lower Diptera represent a paraphyletic assembly of old lineages, some of which reached considerable size and significance, including the suborders crane flies (Tipulomorpha), mosquitoes (Culicomorpha) or the fungus midges (Bibionomorpha). With over 80 000 species, the Brachycera represent with distinction the largest monophyletic subgroup of the Diptera. Part of this wealth of species is occupied by old basal lineages, which include the superfamilies Tabanomorpha (horse flies) and Asiloidea (robber flies and related families). The majority of the Brachycera, however, belong to the Cyclorrhaphans and nested within it, the Schizophora, which are distinguished by the maggot type larva that is part of the Drosophila life cycle (Figure ). Drosophila itself is positioned in the Ephydroidea, which combines the families Drosophilidae (vinegar flies), Diastatidae (bog flies) and Ephydridae (shore flies), all of which comprise moderately swift flying species. The Ephydroidea are close allies to Calyptrata, which includes some of the fastest Diptera like the house fly Musca domestica (house fly) or the blowfly species Calliphora vicina and Calliphora erythrocephala, which serve as important satellite models of molecular vision research in Drosophila (for review see Katz and Minke, ). Only select animal clades are shown. Background colors indicate inclusive range of higher clades: Metazoa (dark blue), Arthropoda (light blue), Hexapoda (blue‐green), Diptera (orange) and the higher Diptera (Brachycera). Nondipteran clades are represented by terminal branches. Dipteran clades are represented by expanding grey triangles reflecting clade size in relative species numbers. Brachycera represents 80 000 species. Bottom scale bar represents time in million of years ago. Divergence times are taken from Wiegmann et al. and Wiegmann et al. .

Figure 4.

Age stratification in Drosophila phototransduction genes. Scale bar represents time in million of years ago. Widths of color bands represent relative fraction sizes of gene groups.

Figure 5.

Evolutionary diversification of opsin genes in Drosophila and honeybee. Background colours indicate wavelength absorption maxima of major Opsin gene clades. Ancestral absorption optimum of B‐opsin clade was most likely in the UV range. Scale bar represents time in million of years ago. Species: Dmel=Drosophila melanogaster; Amel=Apis mellifera (Hymenoptera).

Figure 6.

Candidate‐derived elements of the Drosophila phototransduction machinery. Schematic shows core interactions between the phototransduction proteins and the PI cycling pathway in the Drosophila photoreceptor microvillus. Proteins that have experienced modifications during the evolution of the higher Diptera are highlighted by yellow fill and red outline. The LPPlaza is part of the phospholipid metabolism machinery in the specialised Golgi vesicles, the submicrovillar cisternae (SMC).

Figure 7.

Molecular evolution of the LPPlaza. Background colours indicate association with the DrosophilaLPP family. Shared terminal color background indicates genetic linkage. Scale bar represents time in million of years ago. Species: Agam=Anopheles gambiae; Dmel=Drosophila melanogaster; Tcas=Tribolium castaneum (Coleoptera); Amel=Apis mellifera (Hymenoptera).

Figure 8.

Molecular evolution of the protein kinase CInaC. Orange indicates phylogenetic association with schizophoran species Drosophila melanogaster (Dmel) and Calliphora vicina (Cvic). Bars indicate protein domain organisation with kinase domain region coloured light blue and the PDZ‐binding domain of inaC orthologues in green. Scale bar represents time in million of years ago. Species: Agam=Anopheles gambiae; Tcas=Tribolium castaneum (Coleoptera); Amel=Apis mellifera (Hymenoptera).

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Friedrich, Markus(Nov 2010) Evolution of Visual Performance‐associated Genes in Drosophila. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022898]