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Effects of Soldier-Derived Terpenes on Soldier Caste Differentiation in the Termite Reticulitermes flavipes

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Abstract

Primer pheromones play key roles in regulating division of labor, which is a fundamental and defining aspect of insect sociality. Primer pheromones are chemical messengers that transmit hormone-like messages among colony members; in recipients, these messages can either induce or suppress phenotypic caste differentiation. Here, we investigated soldier caste-derived chemicals as possible primer pheromones in the lower termite Reticulitermes flavipes, a species for which no primer pheromones have yet been identified. We determined that soldier head extracts (SHE), when provided to totipotent workers along with the insect morphogenetic juvenile hormone (JH), significantly enhanced soldier caste differentiation. When applied alone, however, SHE had no impacts on caste differentiation, survivorship, or any other aspect of worker biology. These findings support a function of soldier chemicals as primer pheromones that enhance the action of the endogenous JH. In accord with previous studies, γ-cadinene and the corresponding aldehyde, γ-cadinenal, were identified by gas chromatography–mass spectrometry and nuclear magnetic resonance analyses as the two most abundant components of R. flavipes SHE. Validative bioassays with commercially available cadinene confirmed activity. Several other terpenes, previously identified in R. flavipes soldiers, also were found to be active. These findings reveal a novel primer pheromone-like function for soldier-derived terpenes in termites and further suggest convergent evolution of terpene functions in enhancing JH-dependent soldier caste differentiation.

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References

  • Abe, T., Bignell, D. E., and Higashi, M. 2000. Termites: Evolution, sociality, symbioses, ecology. Kluwer Academic, Dordrecht, The Netherlands.

    Google Scholar 

  • Bagnères, A. G., Clément, J. L., Blum, M. S., Severson, R. F., Joulie, C., and Lange, C. 1990. Cuticular hydrocarbons and defensive compounds of Reticulitermes flavipes (Kollar) and R. santonensis (Feytaud): Polymorphism and chemotaxonomy. J. Chem. Ecol. 16:3213–3244.

    Article  Google Scholar 

  • Brey, W. W., Edison, A. S., Nast, R. E., Rocca, J. R., Saha, S., and Withers, R. S. 2006. Design, construction and validation of a 1 mm triple resonance high-temperature superconducting probe for NMR. J. Mag. Res. 179:290–293.

    Article  CAS  Google Scholar 

  • Buchli, H. 1958. L’origine des castes et les poetntialities ontogeniques des termites europeens du genre Reticulitermes holmgren. Ann. Sci. Nat. Zool. 20:261–429.

    Google Scholar 

  • Gilbert, L. I., Granger, N. A., and Roe, R. M. 2000. The juvenile hormones: Historical facts and speculations on future research directions. Insect. Biochem. Molec Biol. 30:617–644.

    Article  CAS  Google Scholar 

  • Gottlieb, H. E., Kotlyar, V., and Nudelman, A. M. 1997. NMR chemical shifts of common laboratory solvents as trace impurities. J. Org. Chem. 62:7512–7515.

    Article  PubMed  CAS  Google Scholar 

  • Greenberg, S., and Tobe, S. S. 1984. Adaptation of a radiochemical assay for juvenile hormone biosynthesis to study caste differentiation in a primitive termite. J. Insect. Physiol. 31:347–352.

    Article  Google Scholar 

  • Hartfelder, K. 2000. Insect juvenile hormone: From “status quo” to high society. Braz. J. Med. Biol. Res. 33:157–177.

    Article  PubMed  CAS  Google Scholar 

  • Heath, R. R., and Dueben, B. D. 1998. Analytical and preparative gas chromatography, pp. 85–126, in J. G. Millar, and K. F. Haynes (eds.). Methods in Chemical Ecology: Chemical Methods, vol. 1Kluwer, New York.

    Google Scholar 

  • Henderson, G. R. 1998. Primer pheromones and possible soldier caste influences on the evolution of sociality in lower termites, pp. 314–330, in R. K. Vander Meer, M. D. Breed, K. E. Espelie, and M. L. Winston (eds.). Pheromone communication in social insectsWestview, Boulder, Colodaro.

    Google Scholar 

  • Hojo, M., Morioka, M., Matsumoto, T., and Miura, T. 2005. Identification of soldier caste-specific protein in the frontal gland of nasute termite Nasuitetermes takasagoensis (Isoptera: Termitidae). Insect Biochem. Mol. Bio. 35:347–354.

    Article  CAS  Google Scholar 

  • Hojo, M., Matsumoto, T., and Miura, T. 2007. Cloning and expression of a geranylgeranyl diphosphate synthase gene: insights into the synthesis of termite defense secretion. Insect Mol. Bio. 16:121–131.

    Article  CAS  Google Scholar 

  • Kaiser, R., and Lamparsky, R. 1983. New carbonyl compounds in the high-boiling fraction of lavender oil. 1st communication. Helv. Chim. Acta 66:1835–1842.

    Article  CAS  Google Scholar 

  • Korb, J., Roux, E. A., and Lenz, M. 2003. Proximate factors influencing soldier development in the basal termite Cryptotermes secundus (Hill). Insectes Soc. 50:299–303.

    Article  Google Scholar 

  • Lainé, L. V., and Wright, D. J. 2003. The life cycle of Reticulitermes spp. (Isoptera: Rhinotermitidae): What do we know? Bull. Entomol. Res. 93:267–378.

    Article  PubMed  Google Scholar 

  • Lefeuve, P., and Bordereau, C. 1984. Soldier formation regulated by a primer pheromone from the soldier frontal gland in a higher termite, Nasutitermes lujae. Proc. Natl. Acad. Sci. U.S.A. 81:7665–7668.

    Article  PubMed  Google Scholar 

  • Lenz, M. 1976. The dependence of hormone effects in caste determination on external factors, pp. 73–90, in M. Lüscher (ed.). Phase and caste determination in insects. Endocrine aspectsPergamon, Oxford.

    Google Scholar 

  • Lewis, J. L., and Forschler, B. T. 2004. Protist communities from four castes and three species of Reticulitermes (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am. 97:1242–1251.

    Article  Google Scholar 

  • Mao, L., Henderson, G., Lui, Y., and Laine, R. A. 2005. Formosan subterranean termite (Isoptera: Rhinotermitidae) soldiers regulate juvenile hormone levels and caste differentiation in workers. Ann. Ent. Soc. Am. 98:340–345.

    Article  CAS  Google Scholar 

  • Matsumura, F., Coppel, H. C., and Tai, A. 1968. Isolation and identification of termite trail-following pheromone. Nature 219:963–964.

    Article  PubMed  CAS  Google Scholar 

  • Miura, T. 2004. Proximate mechanisms and evolution of caste polyphenism in social insects: From sociality to genes. Ecol. Res. 19:141–148.

    Article  CAS  Google Scholar 

  • Miura, T., and Matsumoto, T. 2000. Soldier morphogenesis in a nasute termite: discovery of a disc-like structure forming a soldier nasus. Proc. Roy. Soc. Lond. B. Bio. 267:1185–1189.

    Article  CAS  Google Scholar 

  • Nelson, L. J., Cool, L. G., Forschler, B. T., and Haverty, M. I. 2001. Correspondence of soldier defense secretion mixtures with cuticular hydrocarbon phenotypes for chemotaxonomy of the termite genus Reticulitermes in North America. J. Chem. Ecol. 27:1449–1479.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, L. J., Cool, L. G., Solek, C. W., and Haverty, M. I. 2008. Cuticular hydrocarbons and soldier defense secretions of Reticulitermes in southern California: A critical analysis of the taxonomy on the genus in North America. J. Chem. Ecol. 34:1452–1475.

    Article  PubMed  CAS  Google Scholar 

  • Nijhout, F. H. 2003. Development and evolution of adaptive polyphenisms. Evol. Dev. 5:9–18.

    Article  PubMed  Google Scholar 

  • Nutting, W. L. 1990. Insect: Isoptera, pp. 997–1032, in D. L. Dindal (ed.). Soil Biology GuideWiley, New York, New York.

    Google Scholar 

  • Okot-Kotber, B. M., Ujvary, I., Mollaaghababa, R., Szurdoki, F., Matolcsy, G., and Prestwich, G. D. 1991. Physiological influence on fenoxycarb pro-insecticides and soldier head extracts of various termite species on soldier differentiation in Reticulitermes flavipes (Isoptera). Sociobiology 19:77–89.

    Google Scholar 

  • Okot-Kotber, B. M., Prestwich, G. D., Strambi, A., and Strambi, C. 1993. Changes in morphogenetic hormone titers in isolated workers of the termite Reticulitermes flavipes (Kollar). Gen. Comp. Endocrinol. 90:290–295.

    Article  PubMed  CAS  Google Scholar 

  • Park, Y. I., and Raina, A. K. 2004. Juvenile hormone III titers and regulation of soldier caste in Coptotermes formosanus. J. Insect. Physiol. 50:561–566.

    Article  PubMed  CAS  Google Scholar 

  • Park, Y. I., and Raina, A. K. 2005. Regulation of juvenile hormone titers by soldiers in the Formosan subterranean termite, Coptotermes formosanus. J. Insect. Physiol. 51:358–391.

    Article  CAS  Google Scholar 

  • Prestwich, G. D. 1983. Chemical systematics of termite exocrine secretions. Annu. Rev. Eco. Syst. 14:287–311.

    Article  Google Scholar 

  • Prestwich, G. D. 1984. Defense mechanisms of termites. Annu. Rev. Entomol. 29:201–232.

    Article  CAS  Google Scholar 

  • Quintana, A., Reinhard, J., Faure, P. U., Bagnères, A.-G., Mossiot, G., and Clément, J.-L. 2003. Interspecific variation in terpenoid composition on defensive secretions of European Reticulitermes termites. J. Chem. Ecol. 29:639–652.

    Article  PubMed  CAS  Google Scholar 

  • Reinhard, J., Lacey, M. J., Ibarra, F., Schroeder, F. C., Kaib, M., and Lenz, M. 2002. Hydroquinone: a general phagostimulating pheromone in termites. J. Chem. Ecol. 28:1–14.

    Article  PubMed  CAS  Google Scholar 

  • Scharf, M. E., Ratliff, C. R., Hoteling, J. T., Pittendrigh, B. R., and Bennett, G. W. 2003. Caste differentiation responses of two sympatric Reticulitermes termite species to juvenile hormone homologs and synthetic juvenoids in two laboratory assays. Insectes Soc. 50:346–354.

    Article  Google Scholar 

  • Scharf, M. E., Ratliff, C. R., Wu-scharf, D., Zhou, X., Pittendrigh, B. R., and Bennett, G. W. 2005. Effects of juvenile hormone III on Reticulitermes flavipes: changes in hemolymph protein composition and gene expression. Insect Biochem. Molec. 35:207–215.

    Article  CAS  Google Scholar 

  • Scharf, M. E., Buckspan, C. E., Grzymala, T. F., and Zhou, X. 2007. Regulation of polyphenic differentiation in the termite Reticulitermes flavipes by interaction of intrinsic and extrinsic factors. J. Exp. Biol. 210:171–179.

    Article  CAS  Google Scholar 

  • Schmelz, E. A., Alborn, H. T., and Tumlinson, J. H. 2001. The influence of intact-plant and excised-leaf bioassay designs on volicitin- and jasmonic acid-induced sesquiterpene volatile release in Zea mays. Planta 214:171–179.

    Article  PubMed  CAS  Google Scholar 

  • Schmelz, E. A., Engelberth, J., Tumlinson, J. H., Block, A., and Alborn, H. T. 2004. The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. Plant J. 39:790–808.

    Article  PubMed  CAS  Google Scholar 

  • Szalanski, A. L., Austin, J. W., and Owens, C. B. 2003. Identification of Reticulitermes spp. (Isoptera: Reticulitermatidae) from South Central United States by PCR-RFLP. J. Econ. Entomol. 96:1514–1519.

    Article  PubMed  CAS  Google Scholar 

  • Truman, J. W., and Riddiford, L. M. 1999. The origins of insect metamorphosis. Nature 401:447–452.

    Article  PubMed  CAS  Google Scholar 

  • Vander meer, R. K., Breed, M. D., Espelie, K. E., and Winston, M. L. 1998. Pheromone communication in social insects. Westview, Boulder, Colorado.

    Google Scholar 

  • Wilson, E. O. 1971. The insect societies. The Belknap press of Harvard University, Cambridge, Massachusetts.

    Google Scholar 

  • Wilson, E. O., and Bossert, W. H. 1963. Chemical communication among animals. Recent Prog. Horm. Res. 19:673–716.

    PubMed  CAS  Google Scholar 

  • Zalkow, L. H., Howard, R. W., Gelbaum, L. T., Gordon, M. M., Deutsch, H. M., and Blum, M. S. 1981. Chemical ecology of Reticulitermes flavipes (Kollar) and R. virginicus (Banks) (Rhinotermitidae): Chemistry of the soldier cephalic secretions. J. Chem. Ecol. 7:717–731.

    Article  CAS  Google Scholar 

  • Zhou, X., Oi, F. M., and Scharf, M. E. 2006a. Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proc. Natl. Acad. Sci. U.S.A. 103:4499–4504.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, X., Tarver, M. R., Bennett, G. W., Oi, F. M., and Scharf, M. E. 2006b. Two hexamerin genes from the termite R. flavipes: sequence, evolution, expression and proposed function in caste regulation. Gene 376:47–58.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, X., Tarver, M. R., and Scharf, M. E. 2007. Hexamerin-based regulation of juvenile hormone-dependent gene expression underlies phenotypic plasticity in a social insect. Development 134:601–610.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Drs. Nancy Denslow, Daniel Hahn, Mike Haverty, Larry Cool, and Faith Oi for helpful discussions; Caitlin Buckspan for bioassay assistance; Marsha Wheeler and Jody Green for review of the manuscript; and Dr. Robert J. Bartelt (USDA-ARS NCAUR, Peoria, IL, USA) for providing an authentic sample of (+)-γ-cadinene. The authors acknowledge the National Science Foundation for financial support through the User Program of the National High Magnetic Field Laboratory, which supported our NMR studies. The 600 MHz 1-mm HTS cryogenic NMR probe used in this work was developed through a collaboration among UF, the NHMFL, and Bruker BioSpin, which was funded by a National Institutes of Health grant (P41RR016105). This work was supported by USDA-CSREES-NRI grant no. 2007-35607-17777 to M.E.S.

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Authors and Affiliations

  1. Entomology and Nematology Department, University of Florida, Gainesville, FL, 32611-0620, USA

    Matthew R. Tarver & Michael E. Scharf

  2. Center of Medical, Agricultural, and Veterinary Entomology, Agricultural Research Service, USDA, 1600/1700 Southwest 23rd Drive, Gainesville, FL, 32608, USA

    Eric A. Schmelz

  3. Advanced Magnetic Resonance and Imaging (AMRIS), McKnight Brain Institute, University of Florida, Gainesville, FL, 32610, USA

    James R. Rocca

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  1. Matthew R. Tarver
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Correspondence to Michael E. Scharf.

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Tarver, M.R., Schmelz, E.A., Rocca, J.R. et al. Effects of Soldier-Derived Terpenes on Soldier Caste Differentiation in the Termite Reticulitermes flavipes . J Chem Ecol 35, 256–264 (2009). https://doi.org/10.1007/s10886-009-9594-8

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