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Molecular Evolution of Arthropod Color Vision Deduced from Multiple Opsin Genes of Jumping Spiders

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Abstract

Among terrestrial animals, only vertebrates and arthropods possess wavelength-discrimination ability, so-called “color vision”. For color vision to exist, multiple opsins which encode visual pigments sensitive to different wavelengths of light are required. While the molecular evolution of opsins in vertebrates has been well investigated, that in arthropods remains to be elucidated. This is mainly due to poor information about the opsin genes of non-insect arthropods. To obtain an overview of the evolution of color vision in Arthropoda, we isolated three kinds of opsins, Rh1, Rh2, and Rh3, from two jumping spider species, Hasarius adansoni and Plexippus paykulli. These spiders belong to Chelicerata, one of the most distant groups from Hexapoda (insects), and have color vision as do insects. Phylogenetic analyses of jumping spider opsins revealed a birth and death process of color vision evolution in the arthropod lineage. Phylogenetic positions of jumping spider opsins revealed that at least three opsins had already existed before the Chelicerata-Pancrustacea split. In addition, sequence comparison between jumping spider Rh3 and the shorter wavelength-sensitive opsins of insects predicted that an opsin of the ancestral arthropod had the lysine residue responsible for UV sensitivity. These results strongly suggest that the ancestral arthropod had at least trichromatic vision with a UV pigment and two visible pigments. Thereafter, in each pancrustacean and chelicerate lineage, the opsin repertoire was reconstructed by gene losses, gene duplications, and function-altering amino acid substitutions, leading to evolution of color vision.

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References

  • Berner RA, Canfield DE (1989) A new model for atmospheric oxygen over Phanerozoic time. Am J Sci 289:333–361

    Article  PubMed  CAS  Google Scholar 

  • Blest AD, Hardie RC, McIntyre P, Williams DS (1981) The spectral sensitivities of identified receptors and the function of retinal tiering in the principle eyes of a jumping spider. J Comp Physiol [A] 145:227–239

    Article  Google Scholar 

  • Briscoe AD (2000) Six opsins from the butterfly Papilio glaucus: molecular phylogenetic evidence for paralogous origins of red-sensitive visual pigments in insects. J Mol Evol 51:110–121

    PubMed  CAS  Google Scholar 

  • Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510

    Article  PubMed  CAS  Google Scholar 

  • Collin SP, Knight MA, Davies WL, Potter IC, Hunt DM, Trezise AE (2003) Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol 13:R864–865

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  PubMed  CAS  Google Scholar 

  • Giribet G, Edgecombe GD, Wheeler WC (2001) Arthropod phylogeny based on eight molecular loci and morphology. Nature 413:157–161

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hisatomi O, Iwasa T, Tokunaga F, Yasui A (1991) Isolation and characterization of lamprey rhodopsin cDNA. Biochem Biophys Res Commun 174:1125–1132

    Article  PubMed  CAS  Google Scholar 

  • Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W (2001) Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413:154–157

    Article  PubMed  CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    PubMed  CAS  Google Scholar 

  • Kasting JF (1987) Theoretical constraints on oxygen and carbon dioxide concentrations in the Precambrian atmosphere. Precambr Res 34:205–229

    Article  CAS  Google Scholar 

  • Katoh K, Kuma K, Miyata T (2001) Genetic algorithm-based maximum-likelihood analysis for molecular phylogeny. J Mol Evol 53:477–484

    Article  PubMed  CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  PubMed  CAS  Google Scholar 

  • Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 30:151–161

    Article  Google Scholar 

  • Koyanagi M, Ono K, Suga H, Iwabe N, Miyata T (1998) Phospholipase C cDNAs from sponge and hydra: antiquity of genes involved in the inositol phospholipid signaling pathway. FEBS Lett 439:66–70

    Article  PubMed  CAS  Google Scholar 

  • Koyanagi M, Kawano E, Kinugawa Y, Oishi T, Shichida Y, Tamotsu S, Terakita A (2004) Bistable UV pigment in the lamprey pineal. Proc Natl Acad Sci USA 101:6687–6691

    Article  PubMed  CAS  Google Scholar 

  • Koyanagi M, Kubokawa K, Tsukamoto H, Shichida Y, Terakita A (2005) Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr Biol 15:1065–1069

    Article  PubMed  CAS  Google Scholar 

  • Land MF (1969) Structure of the retinae of the principal eyes of jumping spiders (Salticidae: dendryphantinae) in relation to visual optics. J Exp Biol 51:443–470

    PubMed  CAS  Google Scholar 

  • Land MF, Nilsson D-E (2002) Animal eyes. Oxford University Press, New York

    Google Scholar 

  • Mallatt JM, Garey JR, Shultz JW (2004) Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Mol Phylogenet Evol 31:178–191

    Article  PubMed  CAS  Google Scholar 

  • Nakamura T, Yamashita S (2000) Learning and discrimination of colored papers in jumping spiders (Araneae, Salticidae). J Comp Physiol [A] 186:897–901

    Article  CAS  Google Scholar 

  • Nordstrom K, Larsson TA, Larhammar D (2004) Extensive duplications of phototransduction genes in early vertebrate evolution correlate with block (chromosome) duplications. Genomics 83:852–872

    Article  PubMed  CAS  Google Scholar 

  • Oakley TH, Huber DR (2004) Differential expression of duplicated opsin genes in two eyetypes of ostracod crustaceans. J Mol Evol 59:239–249

    Article  PubMed  CAS  Google Scholar 

  • Peterson KJ, Eernisse DJ (2001) Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evol Dev 3:170–205

    Article  PubMed  CAS  Google Scholar 

  • Pisani D, Poling LL, Lyons-Weiler M, Hedges SB (2004) The colonization of land by animals: molecular phylogeny and divergence times among arthropods. BMC Biol 2:1

    Article  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Salcedo E, Zheng L, Phistry M, Bagg EE, Britt SG (2003) Molecular basis for ultraviolet vision in invertebrates. J Neurosci 23:10873–10878

    PubMed  CAS  Google Scholar 

  • Shichida Y, Imai H (1998) Visual pigment: G-protein-coupled receptor for light signals. Cell Mol Life Sci 54:1299–1315

    Article  PubMed  CAS  Google Scholar 

  • Spaethe J, Briscoe AD (2004) Early duplication and functional diversification of the opsin gene family in insects. Mol Biol Evol 21:1583–1594

    Article  PubMed  CAS  Google Scholar 

  • Terakita A (2005) The opsins. Genome Biol 6:213

    Article  PubMed  Google Scholar 

  • Terakita A, Koyanagi M, Tsukamoto H, Yamashita T, Miyata T, Shichida Y (2004) Counterion displacement in the molecular evolution of the rhodopsin family. Nat Struct Mol Biol 11:284–289

    Article  PubMed  CAS  Google Scholar 

  • Yamashita S, Tateda H (1976) Spectral sensitivities of jumping spider eyes. J Comp Physiol [A] 105:29–41

    Article  Google Scholar 

  • Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39:306–314

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant-in-Aid for Scientific Research (17770060) and by a Grant-in-Aid for Scientific Research on Priority Areas “Comparative Genomics” from the Ministry of Education, Culture, Sports, Science and Technology of Japan (to M.K.).

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Correspondence to Mitsumasa Koyanagi.

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Mitsumasa Koyanagi and Takashi Nagata contributed equally to this work.

Sequence data from this article have been deposited with the DDBJ under accession nos. AB251846–AB251851.

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Koyanagi, M., Nagata, T., Katoh, K. et al. Molecular Evolution of Arthropod Color Vision Deduced from Multiple Opsin Genes of Jumping Spiders. J Mol Evol 66, 130–137 (2008). https://doi.org/10.1007/s00239-008-9065-9

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  • DOI: https://doi.org/10.1007/s00239-008-9065-9

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