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Workers do not mediate the inhibitory power of queens in a termite, Reticulitermes speratus (Isoptera, Rhinotermitidae)

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Abstract

In social insects, the caste systems are based on reproductive division of labor; queens specialize in reproduction and workers primarily maintain the colony. Recently, a volatile pheromone containing n-butyl-n-butyrate and 2-methyl-1-butanol was identified as a termite queen pheromone that inhibits the differentiation of female neotenic reproductives (secondary queens). Although this volatile inhibitory pheromone regulates caste differentiation directly, the method by which it reaches members without direct contact with the queen in large colonies is not well understood. Therefore, additional mechanisms of indirect communication must exist, such as worker-mediated queen signal transport. We found that workers exposed to female reproductives did not mediate queens’ inhibitory signal in a termite Reticulitermes speratus. The experiment assessed worker transfer from direct to indirect contact groups and determined that the differentiation of new female reproductives in the indirect contact groups was not influenced by the direct contact groups, whereas direct contact with functional female reproductives and artificial queen pheromone did suppress neotenic differentiation. This suggests that worker transfer of the queen signal is unlikely and that for colony-wide inhibition direct contact by the majority of infertile members with reproductives or eggs, which emit the same volatiles as female reproductives, is necessary within a certain time interval.

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References

  • Afzal M. 1983. Radioisotope studies of trophallaxis in the drywood termite Bifiditermes beesoni (Gardner) (Isoptera). I: effect of group size on the rate of food exchange. Mater. Org. 18: 51-63

    Google Scholar 

  • Arnold G., Leconte Y., Trouiller J., Hervet H., Chappe B. and Masson C. 1994. Inhibition of worker honeybee ovaries development by a mixture of fatty-acid esters from larvae. C.R. Acad. Sci. Paris Sci. Vie 317: 511-515

    Google Scholar 

  • Brian M. and Rigby C. 1978. The trophic eggs of Myrmica rubra L. Insect. Soc. 25: 89-110.

    Google Scholar 

  • Butler C.G., Callow R.K. and Johnston N.C. 1959. Extraction and purification of ‘queen substance’ from queen bees. Nature 184: 1871

    Google Scholar 

  • Endler A., Liebig J., Schmitt T., Parker J.E., Jones G.R., Schreier P. and Hölldobler B. 2004. Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc. Natl Acad. Sci. USA 101: 2945-2950. doi:10.1073/pnas.0308447101

    Google Scholar 

  • Fletcher D.J.C. and Ross K.G. 1985. Regulation of reproduction in eusocial Hymenoptera. Annu. Rev. Entomol. 30: 319-343. doi:doi:10.1146/annurev.en.30.010185.001535

    Google Scholar 

  • Fujita A. and Watanabe H. 2010. Inconspicuous matured males of worker form are produced in orphaned colonies of Reticulitermes speratus (Isoptera: Rhinotermitidae) and participate in reproduction. J. Insect Physiol. 56: 1510-1515

    Google Scholar 

  • Hanus R., Vrkoslav V., Hrdý I., Cvačka J. and Šobotník J. 2010. Beyond cuticular hydrocarbons: evidence of proteinaceous secretion specific to termite kings and queens. Proc. R. Soc. Lond. B 277: 995-1002. doi:10.1098/rspb.2009.1857

    Google Scholar 

  • Holman L., Jørgensen C.G., Nielsen J. and d’Ettorre P. 2010. Identification of an ant queen pheromone regulating worker sterility. Proc. R. Soc. Lond. B 277: 3793-3800. doi:10.1098/rspb.2010.0984

  • Jay S.C. 1970. The effect of various combinations of immature queen and worker bees on the ovary development of worker honeybees. Can. J. Zool. 48: 169-173

    Google Scholar 

  • Kawabata S. and Tsuji K. 2005. The policing behavior ‘immobilization’ towards ovary-developed workers in the ant, Diacamma sp. from Japan. Insect. Soc. 52: 89-95. doi:10.1007/s00040-004-0778-5

  • Keller L. and Nonacs P. 1993. The role of queen pheromones in social insects: queen control or queen signal? Anim. Behav. 45: 787-794

    Google Scholar 

  • Kikuchi T., Suwabe M. and Tsuji K. 2010. Durability of information concerning the presence of a gamergate in Diacamma sp. from Japan. Physiol. Entomol. 35: 93-97. doi:10.1111/j.1365-3032.2009.00710.x

  • Kindl J. and Hrdý I. 2005. Development of neotenics induced by a temporary absence of functional reproductives in Kalotermes flavicollis (Isoptera: Kalotermitidae). Eur. J. Entomol. 102: 307-311

    Google Scholar 

  • Lenz M. 1994. Food resources, colony growth and caste development in wood-feeding termites. In: Nourishment and Evolution in Insect Societies (Hunt J.H. and Nalepa C.A., Eds), Westview Press, Boulder, Colorado, pp 159-210

  • Liebig J., Eliyahu D. and Brent C.S. 2009. Cuticular hydrocarbon profiles indicate reproductive status in the termite Zootermopsis nevadensis. Behav. Ecol. Sociobiol. 63: 1799-1807. doi:10.1007/s00265-009-0807-5

    Google Scholar 

  • Liebig J., Monnin T. and Turillazzi S. 2005. Direct assessment of queen quality and lack of worker suppression in a paper wasp. Proc. R. Soc. Lond. B 272: 1339-1344. doi:10.1098/rspb.2005.3073

  • Liebig J., Peeters C. and Hölldobler B. 1999. Worker policing limits the number of reproductives in a ponerine ant. Proc. R. Soc. Lond. B 266: 1865-1870

    Google Scholar 

  • Lüscher M. 1960. Hormonal control of caste differentiation in termites. Annals N.Y. Acad. Sci. 89: 549-563

    Google Scholar 

  • Lüscher M. 1952. Die Produktion und Elimination von Ersatzgeschlechtstieren bei der Termite Kalotermes flavicollis Fabr. Z. Vergl. Physiol. 34: 123-141

  • Markin G.P. 1970. Food distribution within laboratory colonies of the Argentine ant, Iridomyrmex humilis (Mayr). Insect. Soc. 17: 127-158

  • Matsuura K. 2010. Sexual and asexual reproduction in termites. In: Biology of Termites: a Modern Synthesis (Bignell D.E., Roisin Y. and Lo N., Eds), Springer, Dordrecht, pp 255-277

  • Matsuura K., Himuro C., Yokoi T., Yamamoto Y., Vargo E.L. and Keller L. 2010. Identification of a pheromone regulating caste differentiation in termites. Proc. Natl Acad. Sci. USA 107: 12963-12968. doi:10.1073/pnas.1004675107

    Google Scholar 

  • Matsuura K., Kobayashi N. and Yashiro T. 2007. Seasonal patterns of egg production in field colonies of the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Pop. Ecol. 49: 179-183. doi:10.1007/s10144-006-0030-4

  • Matsuura K., Vargo E.L., Kawatsu K., Labadie P.E., Nakano H., Yashiro T. and Tsuji K. 2009. Queen succession through asexual reproduction in termites. Science 323: 1687. doi:10.1126/science.1169702

  • Mohammedi A., Paris A., Crauser D. and Le Conte Y. 1998. Effect of aliphatic esters on ovary development of queenless bees (Apis mellifera L.). Naturwissenschaften 85: 455-458. doi:10.1007/s001140050531

  • Naumann K., Winston M.L., Slessor K.N., Prestwich G.D. and Webster F.X. 1991. Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone. Behav. Ecol. Sociobiol. 29: 321-332. doi:10.1007/bf00165956

    Google Scholar 

  • Pamilo P. 1991. Evolution of colony characteristics in social insects. II. Number of reproductive individuals. Am. Nat. 138: 412-433. doi:doi:10.1086/285224

    Google Scholar 

  • Pettis J.S., Higo H.A., Pankiw T. and Winston M.L. 1997. Queen rearing suppression in the honey bee evidence for a fecundity signal. Insect. Soc. 44: 311-322

    Google Scholar 

  • Ratnieks F.L.W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132: 217-236

    Google Scholar 

  • Rosengaus R.B., Traniello J.F.A. and Levy C.K. 1986. Social transfer, elimination, and biological half-life of gamma-emitting radionuclides in the termite Reticulitermes flavipes Kol. J. Appl. Entomol. 101: 287-294

    Google Scholar 

  • Seeley T.D. 1979. Queen substance dispersal by messenger workers in honeybee colonies. Behav. Ecol. Sociobiol. 5: 391-415. doi:10.1007/bf00292527

  • Shellman-Reeve J.S. 1997. The spectrum of eusociality in termites. In: The Evolution of Social Behaviour in Insects and Arachnids (Choe J.C. and Crespi B.J., Eds), Cambridge University Press, Cambridge, UK, pp 52-93

  • Springhetti A. 1972. I reali nella differenziazione delle caste di Kalotermes flavicollis (Fabr.) (Isoptera). Boll. Zool. 39: 83-87

    Google Scholar 

  • Stuart A.M. 1979. The determination and regulation of the neotenic reproductive caste in the lower termites (Isoptera): with special reference to the genus Zootermopsis (Hagen). Sociobiology 4: 223-237

    Google Scholar 

  • Suárez M.E. and Thorne B.L. 2000. Rate, amount, and distribution pattern of alimentary fluid transfer via trophallaxis in three species of termites (Isoptera: Rhinotermitidae, Termopsidae). Ann. Entomol. Soc. Am. 93: 145-155

    Google Scholar 

  • Traniello J.F.A. 1977. Recruitment behavior, orientation, and the organization of foraging in the carpenter ant Camponotus pennsylvanicus DeGeer (Hymenoptera: Formicidae). Behav. Ecol. Sociobiol. 2: 61-79. doi:10.1007/bf00299289

  • Traniello J.F.A., Rosengaus R.B. and Levy C.K. 1985. Single and double isotope labeling of social insect colonies: gamma-emitting radionuclides as individually identifiable markers. Entomol. Exper. Appl. 38: 87-92

    Google Scholar 

  • Tsuji K., Egashira K. and Hölldobler B. 1999. Regulation of worker reproduction by direct physical contact in the ant Diacamma sp. from Japan. Anim. Behav. 58: 337-343

    Google Scholar 

  • Tsunoda K., Matsuoka H., Yoshimura T. and Tokoro M. 1999. Foraging populations and territories of Reticulitermes speratus (Isoptera: Rhinotermitidae). J. Econ. Entomol. 92: 604-609

    Google Scholar 

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Acknowledgments

We thank C. Himuro, T. Yokoi, and T. Yashiro for research assistance, and E.L. Vargo and L. Keller for helpful discussion. This work was supported by the Japan Society for the Promotion of Science (K.M.) and the Program for Promotion of Basic research Activities for Innovative Biosciences (K.M.).

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  1. Graduate School of Environmental Science, Okayama University, Okayama, 700-8530, Japan

    K. Matsuura & Y. Yamamoto

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  1. K. Matsuura
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  2. Y. Yamamoto
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Correspondence to K. Matsuura.

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Matsuura, K., Yamamoto, Y. Workers do not mediate the inhibitory power of queens in a termite, Reticulitermes speratus (Isoptera, Rhinotermitidae). Insect. Soc. 58, 513–518 (2011). https://doi.org/10.1007/s00040-011-0170-1

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