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Cryptic Color Change in a Crab Spider (Misumena vatia): Identification and Quantification of Precursors and Ommochrome Pigments by HPLC

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Abstract

Mimicry is used widely by arthropods to survive in a hostile environment. Often mimicry is associated with the production of chemical compounds such as pigments. In crab spiders, the change of color is based on a complex physiological process that still is not understood. The aim of this study was to identify and quantify the ommochrome pigments and precursors responsible for the color change in the mimetic crab spider Misumena vatia (Thomisidae). A modified high performance reverse phase ion-pair chromatography technique enabled us to separate and quantify the ommochrome pigments, their precursors, and related metabolites in individual spiders. Compounds such as tryptophan, kynurenine, and kynurenic acid occurred only or mainly in white crab spiders. In contrast, compounds such as 3-hydroxy-kynurenine, xanthommatin, and ommatin D occurred only or mainly in yellow crab spiders. Factor analysis ranked the different color forms in accordance with their metabolites. The biochemical results enabled us to associate the different phases of formation of pigment granules with specific metabolites. Yellow crab spiders contain many unknown ommochrome-like compounds not present in white crab spiders. We also found large quantities of decarboxylated xanthommatin, whose role as precursor of new pathways in ommochrome synthesis needs to be assessed. The catabolism of ommochromes, a process occurring when spiders revert from yellow to white, warrants further study.

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References

  • American Chemical Society (ACS), S. O. E. A. C. 1980. Anal. Chem. 52:2242.

  • Arnault, I., Christidès, J. P., Mandon, N., Haffner, T., Kahane, R., and Auger, J. 2003. High-performance ion-pair chromatography method for simultaneous analysis of alliin, deoxyalliin, allicin and dipeptide precursors in garlic products using multiple mass spectrometry and UV detection. J. Chromatogr. A. 991:69–75.

    Article  CAS  PubMed  Google Scholar 

  • Beard, C. B., Benedict, M. Q., Primus, J. P., Finnerty, V., and Collins, F. H. 1995. Eye pigments in wild-type and eye-color mutant strains of the African malaria vector Anopheles gambiae. J. Hered. 86:375–380.

    CAS  PubMed  Google Scholar 

  • Bhaskara, R. M., Brijesh, C. M., Ahmed, S., and Borges, R. M. 2009. Perception of ultraviolet light by crab spiders and its role in selection of hunting sites. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 195(4):409–417.

    Article  Google Scholar 

  • Brechbühl, R., Casas, J., and Bacher, S. 2009. Ineffective crypsis in a crab spider: a prey community perspective. Proc. Biol. Sci.

  • Brown, R. and Nickla, H. 1977. Simultaneous separation of pteridines and ommochrome precursors by paper chromatography. J. Chromatogr. 133:423–424.

    Article  CAS  PubMed  Google Scholar 

  • Butenandt, A. and Schaefer, W. 1962. Ommochromes, pp. 13–33, in T. S. Gore, B. S. Joshi, S. V. Sunthankar, and B. D. Tilak (eds.). Recent Progr. Chem. Nat. and Synth. Coloring Matters and Academic Press, New York.

  • Chittka, L. 2001. Camouflage of predatory crab spiders on flowers and the color perception of bees (Aranida: Thomisidae/Hymenoptera: Apidae). Entomol. Gen. 25:181–187.

    Google Scholar 

  • Chittka, L. and Osorio, D. 2007. Cognitive dimensions of predator responses to imperfect mimicry. PLoS Biol. 12:2754–2758.

    Google Scholar 

  • Fuzeau-Braesch, S. 1985. Color changes, pp. 549–589, in G. A. Kerkut and L. I. Gilbert (eds.). Comprehensive Insect Physiology Biochemistry and Pharmacology. Pergamon Press, Oxford, United Kingdom.

    Google Scholar 

  • Han, Q., Beerntsen, B. T., and Li, J. 2007. The tryptophan oxidation pathway in mosquitoes with emphasis on xanthurenic acid biosynthesis. J. Insect Physiol. 53:254–263.

    Article  CAS  PubMed  Google Scholar 

  • Heckel, E. 1891. Sur le mimétisme de Thomisus onostus. Bull. Sci. Fr. Belg. 23:347–354.

    Google Scholar 

  • Ings T. C. and Chittka L. 2008. Speed-accuracy tradeoffs and false alarms in bee responses to cryptic predators. Curr. Biol. 18:1520–1524.

    Article  CAS  PubMed  Google Scholar 

  • Insausti, T. C. and Casas, J. 2008. The functional morphology of color changing in a spider: development of ommochrome pigment granules. J. Exp. Biol. 211:780–789.

    Article  PubMed  Google Scholar 

  • Insausti, T. C. and Casas, J. 2009. Turnover of pigment granules: cyclic catabolism and anabolism of ommochromes within epidermal cells. Tissue Cell. 41:421–429

    Article  CAS  PubMed  Google Scholar 

  • Iwahashi, H. and Ishii, T. 1997. Detection of the oxidative products of 3-hydroxykynurenine using high-performance liquid chromatography-electrochemical detection-ultraviolet absorption detection-electron spin resonance spectrometry and high-performance liquid chromatography-electrochemical detection-ultraviolet absorption detection-mass spectrometry. J. Chromatogr. A. 773:23–31.

    Article  CAS  Google Scholar 

  • Kato, T., Sawada, H., Yamamoto, T., Mase, K., and Nakagoshi, M. 2006. Pigment pattern formation in the quail mutant of the silkworm, Bombyx mori: parallel increase of pteridine biosynthesis and pigmentation of melanin and ommochromes. Pigm. Cell Res. 19:337–345.

    CAS  Google Scholar 

  • Kayser, H., 1985. Pigments, pp. 367–415, in G. A. Kerkut and L. I. Gilbert (eds). Comprehensive Insect Physiology Biochemistry and Pharmacology. Pergamon Press, Oxford, United Kingdom.

    Google Scholar 

  • Koch, P. B., 1993. Production of [14C]-3-hydroxy-L-kynurenine in a butterfly, Heliconius charitonia L. (Heliconidae), and precursor studies in butterfly wing ommatins. Pigm. Cell Res. 6:85–90.

    CAS  Google Scholar 

  • Linzen, B., 1974. The tryptophan to ommochrome pathway in insects, pp. 177–246, in M. J. Berridge, J. E. Treherne, and V. B. Wigglesworth (eds.). Adv. Insect Physiol. Academic Press, London, United Kingdom.

  • Millot, J. 1926. Contribution à l’histophysiologie des Aranéides. Bull. Biol. Fr. Belg. 8:1–238.

    Google Scholar 

  • Morse, D. H. 2007. Predator upon a Flower. Life History and Fitness in a Crab Spider. Harvard University Press, Cambridge, Massachusetts, USA.

    Google Scholar 

  • Naya, Y., Ohnishi, M., Ikeda, M., Miki, W., and Nakanishi, K., 1991. Physiological role of 3-hydroxykynurenine and xanthurenic acid upon crustacean molting. Adv. Exp. Med. Biol. 294:309–318.

    CAS  PubMed  Google Scholar 

  • Needham, A. E., 1974. The Significance of Zoochromes in Zoophysiology and Ecology. Springer-Verlag, New York, USA.

    Google Scholar 

  • Nijhout, H. F. 1997. Ommochrome pigmentation of the linea and rosa seasonal forms of Precis coenia (Lepidoptera:Nymphalidae). Arch. Insect Biochem. Physiol. 36:215–222.

    Article  CAS  Google Scholar 

  • Okech, B., Arai, M., and Matsuoka, H. 2006. The effects of blood feeding and exogenous supply of tryptophan on the quantities of xanthurenic acid in the salivary glands of Anopheles stephensi (Diptera: Culicidae). Biochem. Biophys. Res. Commun. 341:1113–1118.

    Article  CAS  PubMed  Google Scholar 

  • Oxford, G. S. and Gillespie R. G. 1998. Evolution and ecology of spider coloration. Annu. Rev. Entomol. 43:619–643.

    Article  CAS  PubMed  Google Scholar 

  • Phillips, J. P., Forrest, H. S., and Kulkarni, A. D. 1973. Terminal synthesis of xanthommatin in Drosophila melanogaster. 3. Mutational pleiotropy and pigment granule association of phenoxazinone synthetase. Genetics. 73:45–56.

    Google Scholar 

  • Phillips, J. P., and Forrest, H. S., 1980. Ommochromes and pteridines, pp. 542–623, in M. Ashburmer, and T. R. F. Wright (eds.). The Genetics and Biology of Drosophila. Academic Press, London, UK.

    Google Scholar 

  • Rasgon, J. L. and Scott, T. W. 2004. Crimson: A novel sex-linked eye color mutant of Culex pipiens L. (Diptera: Culicidae). J. Med. Entomol. 41:385–391.

    Article  PubMed  Google Scholar 

  • Reed, R. D. and Nagy, L. M. 2005. Evolutionary redeployment of a biosynthetic module: Expression of eye pigment genes vermilion, cinnabar, and white in butterfly wing development. Evol. Dev. 7:301–311.

    Article  CAS  PubMed  Google Scholar 

  • Reed, R. D., McMillan, W. O., and Nagy, L. M. 2008. Gene expression underlying adaptive variation in Heliconius wing patterns: non-modular regulation of overlapping cinnabar and vermilion prepatterns. Proc. Biol. Sci. 275:37–45.

    Article  CAS  PubMed  Google Scholar 

  • Sawada, H., Yamahama, Y., Mase, K., Hirakawa, H., and Iino, T. 2006. Molecular properties and tissue distribution of 30 K proteins as ommin-binding proteins from diapause eggs of the silkworm, Bombyx mori. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 146:172–179.

    Article  Google Scholar 

  • Seligy, V. L. 1972. Ommochrome pigments of spiders. Comp. Biochem. Physiol. A Physiol. 42:699–709.

    Article  CAS  Google Scholar 

  • Taylor, R. M. and Pfannenstiel, R. S. 2008. Nectar feeding by wandering spiders on cotton plants. Environ. Entomol. 37:996–1002.

    Article  CAS  PubMed  Google Scholar 

  • Théry, M., 2007. Colors of background reflected light and of the prey’s eye affect adaptive coloration in female crab spiders. Anim. Behav. 73:797–804.

    Article  Google Scholar 

  • Théry, M. and Casas, J. 2002. Visual systems: Predator and prey views of spider camouflage. Nature. 415:133–133.

    Article  PubMed  Google Scholar 

  • Théry, M. and Casas, J. 2009. The multiple disguises of spiders: web color and decorations, body color and movement. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 364:471–480.

    Article  PubMed  Google Scholar 

  • Vogliardi, S., Bertazzo, A., Comai, S., Costa, C. V. L., Allegri, G., Seraglia, R., and Traldi, P. 2004. An investigation on the role of 3-hydroxykynurenine in pigment formation by matrix-assisted laser desorption/ionization mass spectrometry. Rapid Commun. Mass Spectrom. 18:1413–1420.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Dr. Mickaël Riou thanks Professor Jerome Casas for hosting him on his team. We thank the University François Rabelais, the CNRS and the Plate-forme d’Infectiologie (INRA) for financial support, Prof. A. Bolognese, Pr. A.G. Bagnères-Urbany, Pr. J. Auger and Dr. T. Insausti for stimulating discussions, Pr. F. Van Bambeke and Professor J. Williams for comments on the manuscript, Mr J. Defrize for rearing the crab spiders, and Miss M. Le Gall and Miss C. Boutry for technical assistance.

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  1. Mickaël Riou

    Present address: UE 1277 Plate-Forme d’Infectiologie Expérimentale (PFIE), Centre – INRA, F-37380, Nouzilly, France

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  1. IRBI, Institut de Recherche de la Biologie des Insectes, UMR CNRS 6035, Université François-Rabelais de Tours, Parc de Grandmont, F-37200, Tours, France

    Mickaël Riou & Jean-Philippe Christidès

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Riou, M., Christidès, JP. Cryptic Color Change in a Crab Spider (Misumena vatia): Identification and Quantification of Precursors and Ommochrome Pigments by HPLC. J Chem Ecol 36, 412–423 (2010). https://doi.org/10.1007/s10886-010-9765-7

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