Evolution of Visual Performance‐associated Genes in Drosophila

Markus Friedrich, Wayne State University, Detroit, Michigan, USA

Published online: November 2010

DOI: 10.1002/9780470015902.a0022898

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., 2009; Yeates and Wiegmann, 2007). 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 1). 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, 2009). 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. (2009) and Wiegmann et al. (submitted).
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 LPP laza is part of the phospholipid metabolism machinery in the specialised Golgi vesicles, the submicrovillar cisternae (SMC).
Figure 7. Molecular evolution of the LPP laza. Background colours indicate association with the Drosophila LPP 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 C InaC. 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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 References
    Abd El-Aziz MM, Barragan I, O'Driscoll CA et al. (2008) EYS, encoding an ortholog of Drosophila spacemaker, is mutated in autosomal recessive retinitis pigmentosa. Nature Genetics 40: 1285–1287.
    Arendt D and Wittbrodt J (2001) Reconstructing the eyes of Urbilateria. Philosophical transactions of the Royal Society of London. Series B Biological Sciences 356: 1545–1563.
    Ballinger DG, Xue N and Harshman KD (1993) A Drosophila photoreceptor cell-specific protein, calphotin, binds calcium and contains a leucine zipper. Proceedings of the National Academy of Sciences of the USA 90: 1536–1540.
    Bao R and Friedrich M (2009) Molecular evolution of the Drosophila retinome: exceptional gene gain in the higher Diptera. Molecular Biology and Evolution 26: 1273–1287.
    Baylor DA, Lamb TD and Yau K-W (1979) Responses of retinal rods to single photons. Journal of Physiology 288: 613–634.
    Cook B, Hardy RW, McConnaughey WB and Zuker CS (2008) Preserving cell shape under environmental stress. Nature 452: 361–364.
    book Courtney GW, Pape T, Skevington JH and Sinclair BJ (2009) "Biodiversity of Diptera". In: Foottit RG and Adler PH (eds) Insect Biodiversity: Science and Society, pp. 185–222. Oxford: Blackwell Publishing.
    Dietrich W (1909) Die Facettenaugen der Dipteren. Zeitschrift für Wissenschaftliche Zoologie 92: 465–539.
    Erclik T, Hartenstein V, Lipshitz HD and McInnes RR (2008) Conserved role of the Vsx genes supports a monophyletic origin for bilaterian visual systems. Current Biology 18: 1278–1287.
    Fain GL, Hardie R and Laughlin SB (2010) Phototransduction and the evolution of photoreceptors. Current Biology 20: R114–R124.
    Friedrich M (2006) Ancient mechanisms of visual sense organ development based on comparison of the gene networks controlling larval eye, ocellus, and compound eye specification in Drosophila. Arthropod Structure & Development 35: 357–378.
    Friedrich M (2008) Opsins and cell fate in the Drosophila Bolwig organ: tricky lessons in homology inference. BioEssays 30: 980–993.
    Garcia-Murillas I, Pettitt T, Macdonald E et al. (2006) Lazaro encodes a lipid phosphate phosphohydrolase that regulates phosphatidylinositol turnover during Drosophila phototransduction. Neuron 49: 533–546.
    Hanyu-Nakamura K, Kobayashi S and Nakamura A (2004) Germ cell-autonomous Wunen2 is required for germline development in Drosophila embryos. Development 131: 4545–4553.
    Hardie RC and Raghu P (2001) Visual transduction in Drosophila. Nature 413: 186–193.
    Helfrich-Forster C (2002) The circadian system of Drosophila melanogaster and its light input pathways. Zoology 105: 297–312.
    Helfrich-Forster C, Edwards T, Yasuyama K et al. (2002) The extraretinal eyelet of Drosophila: development, ultrastructure, and putative circadian function. Journal of Neuroscience 22: 9255–9266.
    Henderson SR, Reuss H and Hardie RC (2000) Single photon responses in Drosophila photoreceptors and their regulation by Ca2+. Journal of physiology 524: 179–194.
    Huang J, Liu CH, Hughes SA et al. (2010) Activation of TRP channels by protons and phosphoinositide depletion in Drosophila photoreceptors. Current Biology 20: 189–197.
    Husain N, Pellikka M, Hong H et al. (2006) The agrin/perlecan-related protein Eyes Shut is essential for epithelial lumen formation in the Drosophila retina. Developmental Cell 11: 483–493.
    Jors S, Kazanski V, Foik A, Krautwurst D and Harteneck C (2006) Receptor-induced activation of Drosophila TRP by polyunsaturated fatty acids. Journal of Biological Chemistry 281: 29693–29702.
    Katz B and Minke B (2009) Drosophila photoreceptors and signaling mechanisms. Frontiers in Cellular Neuroscience 3: 2.
    Kelber A and Osorio D (2010) From spectral information to animal colour vision: experiments and concepts. Proceedings of the Royal Society B 277: 1617–1625.
    Kirschfeld K and Franceschini N (1969) A mechanism for the control of the light flow in the rhabdomeres of the complex eye of Musca. Kybernetik 6: 13–22.
    Kirschfeld K and Franceschini N (1977) Evidence for a sensitising pigment in fly photoreceptors. Nature 269: 386–390.
    van Kleef J, Berry R and Stange G (2008) Directional selectivity in the simple eye of an insect. Journal of Neuroscience 28: 2845–2855.
    Knox BE, Salcedo E, Mathiesz K et al. (2003) Heterologous expression of Limulus rhodopsin. Journal of Biological Chemistry 278: 40493–40502.
    Kwon Y and Montell C (2006) Dependence on the Lazaro phosphatidic acid phosphatase for the maximum light response. Current Biology 16: 723–729.
    Labhart T and Meyer EP (1999) Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microscopy Research and Technique 47: 368–379.
    book Land MF and Nilsson DE (2002) Animal eyes. Oxford: Oxford University Press.
    Landry CR, Castillo-Davis CI, Ogura A, Liu JS and Hartl DL (2007) Systems-level analysis and evolution of the phototransduction network in Drosophila. Proceedings of the National Academy of Sciences of the USA 104: 3283–3288.
    Lynch M and Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151–1155.
    Martin JH, Benzer S, Rudnicka M and Miller CA (1993) Calphotin: a Drosophila photoreceptor cell calcium-binding protein. Proceedings of the National Academy of Sciences of the USA 90: 1531–1535.
    Mazzoni EO, Celik A, Wernet MF et al. (2008) Iroquois complex genes induce co-expression of rhodopsins in Drosophila. PLoS Biology 6: e97.
    Melzer RR, Zimmermann T and Smola U (1997) Modification of dispersal patterns of branched photoreceptor axons and the evolution of neural superposition. Cellular and Molecular Life Sciences 53: 242–247.
    Menne D and Spatz HC (1977) Colour vision in Drosophila melanogaster. Journal of Comparetive Physiology 114: 301–312.
    book Menzel R (1979) "Spectral sensitivity and color vision in invertebrates". In: Autrum H (ed.) Handbook of sensory physiology, pp. 503–580. Germany: Springer.
    Mishra P, Socolich M, Wall MA et al. (2007) Dynamic scaffolding in a G protein-coupled signaling system. Cell 131: 80–92.
    Morante J, Desplan C and Celik A (2007) Generating patterned arrays of photoreceptors. Current Opinion in Genetics & Development 17: 314–319.
    Nilsson DE and Ro AI (1994) Did neural pooling for night-vision lead to the evolution of neural superposition eyes. Journal of Comparative Physiology A – Sensory Neural and Behavioral Physiology 175: 289–302.
    Osorio D (2007) Spam and the evolution of the fly's eye. BioEssays 29: 111–115.
    Osorio D, Averof M and Bacon JP (1995) Arthropod evolution: great brains, beautiful bodies. Trends in Ecology and Evolution 10: 449–454.
    Osorio D and Vorobyev M (2005) Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proceedings of the Royal Society of London, Series B. Biological Sciences 272: 1745–1752.
    Parsons MM, Krapp HG and Laughlin SB (2006) A motion-sensitive neurone responds to signals from the two visual systems of the blowfly, the compound eyes and ocelli. Journal of Experimental Biology 209: 4464–4474.
    Paulus HF (1989) Das Homologisieren in der Feinstrukturforschung: Das Bolwig-Organ der hoeheren Dipteren und seine Homologisierung mit Stemmata und Ommatidien eines urspruenglichen Facettenauges der Mandibulata. Zoologische Beitrage N. F. 32: 437–478.
    Payne R, Corson DW and Fein A (1986) Pressure injection of calcium both excites and adapts Limulus ventral photoreceptors. Journal of General Physiology 88: 107–126.
    Popescu DC, Ham AJ and Shieh BH (2006) Scaffolding protein INAD regulates deactivation of vision by promoting phosphorylation of transient receptor potential by eye protein kinase C in Drosophila. Journal of Neuroscience 26: 8570–8577.
    Raghu P, Colley NJ, Webel R et al. (2000) Normal phototransduction in Drosophila photoreceptors lacking an InsP(3) receptor gene. Molecular and Cellular Neurosciences 15: 429–445.
    Sano H, Renault AD and Lehmann R (2005) Control of lateral migration and germ cell elimination by the Drosophila melanogaster lipid phosphate phosphatases Wunen and Wunen 2. Journal of Cell Biology 171: 675–683.
    Sawin EP, Harris LR, Campos AR and Sokolowski MB (1994) Sensorimotor transformation from light reception to phototactic behavior in Drosophila larvae (Diptera: Drosophilidae). Journal of Insect Behavior 7: 553–567.
    Schmitt A, Vogt A, Friedmann K, Paulsen R and Huber A (2005) Rhodopsin patterning in central photoreceptor cells of the blowfly Calliphora vicina: cloning and characterization of Calliphora rhodopsins Rh3, Rh5 and Rh6. Journal of Experimental Biology 208: 1247–1256.
    Stavenga DG (1995) Insect retinal pigments: Spectral characteristics and physiological functions. Progress in Retinal and Eye Research 15: 231–259.
    Townson SM, Chang BSW, Salcedo E et al. (1998) Honeybee blue-and ultraviolet-sensitive opsins: cloning, heterologous expression in Drosophila, and physiological characterization. Journal of Neuroscience 18: 2412–2422.
    Wiegmann BM, Trautwein MD, Kim JW et al. (2009) Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biology 7: 34.
    other Wiegmann BM, Trautwein MD and Winkler IS (submitted) The Fly Tree of Life: Multiple lines of evidence reveal phylogenetic history in the insect order Diptera.
    Xu XZ, Chien F, Butler A, Salkoff L and Montell C (2000) TRP, a Drosophila TRP-related subunit, forms a regulated cation channel with TRPL. Neuron 26: 647–657.
    Yamaguchi S, Desplan C and Heisenberg M (2010) Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila. Proceedings of the National Academy of Sciences of the USA 107: 5634–5639.
    Yamaguchi S, Wolf R, Desplan C and Heisenberg M (2008) Motion vision is independent of color in Drosophila. Proceedings of the National Academy of Sciences of the USA 105: 4910–4915.
    Yang Y and Ballinger D (1994) Mutations in calphotin, the gene encoding a Drosophila photoreceptor cell-specific calcium-binding protein, reveal roles in cellular morphogenesis and survival. Genetics 138: 413–421.
    Yau KW and Hardie RC (2009) Phototransduction motifs and variations. Cell 139: 246–264.
    book Yeates DK and Wiegmann BM (2007) "Phylogeny and evolution of Diptera: recent insghts and new perspectives". In: Yeates DK and Wiegmann BM (eds) The Evolutionary Biology of Flies pp. 2–14. New York: Columbia Press University.
    Zelhof AC, Hardy RW, Becker A and Zuker CS (2006) Transforming the architecture of compound eyes. Nature 443: 696–699.
 Further Reading
    Borst A (2009) Drosophila's view on insect vision. Current Biology 19: R36–R47.
    book Meinertzhagen IA (1991) "Evolution of the cellular organization of the arthropod compound eye and optic lobe". In: CronlyDillon JR and Gregory RL (eds) Vision and Visual Dysfunction, pp. 341–362. Boston: Macmillan Press.
    book Warrant E and Nilsson DE (eds) (2006) Invertebrate Vision, pp. 250–290. New York: Cambridge University Press.

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Sensory Systems | Adaptive Evolution | Diversification of Plants and Animals | Evolution of Novelty | Molecular Evolution | Protein Evolution | Evolutionary Ecology | Physiological Ecology | Behavioural Ecology
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Article Title: Evolution of Visual Performance‐associated Genes in Drosophila
 
How to Cite close
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]