Journal of Chemical Ecology

, Volume 38, Issue 6, pp 746–754 | Cite as

Multifunctional Queen Pheromone and Maintenance of Reproductive Harmony in Termite Colonies

Review Article

Abstract

Pheromones are likely involved in all social activities of social insects including foraging, sexual behavior, defense, nestmate recognition, and caste regulation. Regulation of the number of fertile queens requires communication between reproductive and non-reproductive individuals. Queen-produced pheromones have long been believed to be the main factor inhibiting the differentiation of new reproductive individuals. However, since the discovery more than 50 years ago of the queen honeybee substance that inhibits the queen-rearing behavior of workers, little progress has been made in the chemical identification of inhibitory queen pheromones in other social insects. The recent identification of a termite queen pheromone and subsequent studies have elucidated the multifaceted roles of volatile pheromones, including functions such as a fertility signal, worker attractant, queen–queen communication signal, and antimicrobial agent. The proximate origin and evolutionary parsimony of the termite queen pheromone also are discussed.

Keywords

Termite queen pheromone Semiochemical Pheromone parsimony Caste differentiation Primer pheromone 

References

  1. Abe, T. 1987. Evolution of life types in termites, pp. 125–148, in S. Kawano, J. H. Connell, and T. Hidaka (eds.), Evolution and Coadaptation in Biotic Communities. University of Tokyo Press, Tokyo.Google Scholar
  2. 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., Ser. 3 Sci. vie 317:511–515.Google Scholar
  3. Bestmann, H. J., Vostrowsky, O., and Platz, H. 1977. Pheromone XII. Male sex pheromones of noctuids (Lepidoptera). Experientia 33:874–875.PubMedCrossRefGoogle Scholar
  4. Blum, M. S. 1996. Semiochemical parsimony in the Arthropoda. Annu. Rev. Entomol. 41:353–374.PubMedCrossRefGoogle Scholar
  5. Blum, M. S. and Brand, J. M. 1972. Social insect pheromones: their chemistry and function. Am. Zool. 12:553–576.Google Scholar
  6. Brent, C. S., Schal, C., and Vargo, E. L. 2005. Endocrine changes in maturing primary queens of Zootermopsis angusticollis. J. Ins. Physiol. 51:1200–1209.CrossRefGoogle Scholar
  7. Brian, M. and Rigby, C. 1978. The trophic eggs of Myrmica rubra L. Ins. Soc. 25:89–110.CrossRefGoogle Scholar
  8. BRUINSMA, O. H. 1979. An analysis of building behaviour of the termite Macrotermes subhyalinus. Ph.D. thesis, Lanbouwhogeschool te Wageningen.Google Scholar
  9. Butler, C. G., Callow, R. K., and Johnston, N. C. 1959. Extraction and purification of ‘queen substance’ from queen bees. Nature 184:1871–1871.CrossRefGoogle Scholar
  10. Camazine, S., Deneubourg, J.-L., Franks, N. R., Sneyd, J., Theraulaz, G. and Bonabeau, E. 2003. Self-organization in Biological Systems. Princeton University Press.Google Scholar
  11. Castle, G. B. 1934. The dampwood termites of the western United State, genus Zootermopsis (formerly Termopsis), pp. 273–310, in J. Kofoid (ed.), Termites and Termite Control. University of California Press, Berkeley, California.Google Scholar
  12. Cremer, S., Armitage, S. A. O., and Schmid-Hempel, P. 2007. Social immunity. Curr. Biol. 17:R693–R702.PubMedCrossRefGoogle Scholar
  13. Cuvillier-Hot, V., Cobb, M., Malosse, C., and Peeters, C. 2001. Sex, age and ovarian activity affect cuticular hydrocarbons in Diacamma ceylonense, a queenless ant. J. Ins. Physiol. 47:485–493.CrossRefGoogle Scholar
  14. Danty, E., Briand, L., Michard-Vanhée, C., Perez, V., Arnold, G., Gaudemer, O., Huet, D., Huet, J.-C., Ouali, C., Masson, C., and Pernollet, J.-C. 1999. Cloning and expression of a queen pheromone-binding protein in the honeybee: an olfactory-specific, developmentally regulated protein. J. Neurosci. 19:7468–7475.PubMedGoogle Scholar
  15. Dietemann, V., Peeters, C., Liebig, J., Thivet, V., and Hölldobler, B. 2003. Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. Proc. Natl. Acad. Sci. U.S.A. 100:10341–10346.PubMedCrossRefGoogle Scholar
  16. 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. U.S.A. 101:2945–2950.PubMedCrossRefGoogle Scholar
  17. Fletcher, D. J. C. and Ross, K. G. 1985. Regulation of reproduction in eusocial Hymenoptera. Annu. Rev. Entomol. 30:319–343.CrossRefGoogle Scholar
  18. Fussnecker, B., McKenzie, A., and Grozinger, C. 2011. cGMP modulates responses to queen mandibular pheromone in worker honey bees. J. Comp. Physiol. A 197:939–948.CrossRefGoogle Scholar
  19. Gilley, D. C., Degrandi-Hoffman, G., and Hooper, J. E. 2006. Volatile compounds emitted by live European honey bee (Apis mellifera L.) queens. J. Ins. Physiol. 52:520–527.CrossRefGoogle Scholar
  20. Greenberg, S. and Tobe, S. S. 1985. Adaptation of a radiochemical assay for juvenile hormone biosynthesis to study caste differentiation in a primitive termite. J. Ins. Physiol. 31:347–352.CrossRefGoogle Scholar
  21. Grozinger, C. and Robinson, G. 2007. Endocrine modulation of a pheromone-responsive gene in the honey bee brain. J. Comp. Physiol. A 193:461–470.CrossRefGoogle Scholar
  22. Hannonen, M., Sledge, M. F., Turillazzi, S., and Sundström, L. 2002. Queen reproduction, chemical signalling and worker behaviour in polygyne colonies of the ant Formica fusca. Anim. Behav. 64:477–485.CrossRefGoogle Scholar
  23. Hanus, R., Vrkoslav, V., Hrdy, I., Cvacka, J., and Sobotnik, J. 2010. Beyond cuticular hydrocarbons: evidence of proteinaceous secretion specific to termite kings and queens. Proc. Roy. Soc. Lond. B 277:995–1002.CrossRefGoogle Scholar
  24. Hartmann, A., D’ettorre, P., Jones, G. R., and Heinze, J. 2005. Fertility signalling: the proximate mechanism of worker policing in a clonal ant. Naturwissenschaften 92:282–286.PubMedCrossRefGoogle Scholar
  25. Heinze, J., Stengl, B., and Sledge, M. 2002. Worker rank, reproductive status and cuticular hydrocarbon signature in the ant, Pachycondyla inversa. Behav. Ecol. Sociobiol. 52:59–65.CrossRefGoogle Scholar
  26. Heinze, J., Trunzer, B., Oliveira, P., and Hölldobler, B. 1996. Regulation of reproduction in the neotropical ponerine ant, Pachycondyla villosa. J. Ins. Behav. 9:441–450.CrossRefGoogle Scholar
  27. Himuro, C., Yokoi, T., and Matsuura, K. 2011. Queen-specific volatile in a higher termite Nasutitermes takasagoensis (Isoptera: Termitidae). J. Ins. Physiol. 57:962–965.CrossRefGoogle Scholar
  28. Holman, L., Jorgensen, C. G., Nielsen, J., and D’Ettorre, P. 2010. Identification of an ant queen pheromone regulating worker sterility. Proc. Roy. Soc. Lond. B 277:3793–3800.CrossRefGoogle Scholar
  29. Hoover, S. R., Keeling, C., Winston, M., and Slessor, K. 2003. The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480.PubMedCrossRefGoogle Scholar
  30. Jacquin, E., Nagnan, P., and Frerot, B. 1991. Identification of hairpencil secretion from male Mamestra brassicae (L.)(Lepidoptera: Noctuidae) and electroantennogram studies. J. Chem. Ecol. 17:239–246.CrossRefGoogle Scholar
  31. Kambhampati, S. and Eggleton, P. 2000. Taxonomy and phylogeny of termites, pp. 1–25, in D. E. Bignell, T. Abe, and M. Higashi (eds.), Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer, Dordrecht.Google Scholar
  32. Keller, L. and Nonacs, P. 1993. The role of queen pheromones in social insects: queen control or queen signal? Anim. Behav. 45:787–794.CrossRefGoogle Scholar
  33. Kindl, J. and Hrdy, 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
  34. Korb, J., Weil, T., Hoffmann, K., Foster, K. R., and Rehli, M. 2009. A gene necessary for reproductive suppression in termites. Science 324:758.PubMedCrossRefGoogle Scholar
  35. Lacey, E. S., Moreira, J. A., Millar, J. G., and Hanks, L. M. 2008. A male-produced aggregation pheromone blend consisting of alkanediols, terpenoids, and an aromatic alcohol from the cerambycid beetle Megacyllene caryae. J. Chem. Ecol. 34:408–417.PubMedCrossRefGoogle Scholar
  36. le Conte, Y. and Hefetz, A. 2008. Primer pheromones in social hymenoptera. Annu. Rev. Entomol. 53:523–542.PubMedCrossRefGoogle Scholar
  37. Lenz, M. 1994. Food resources, colony growth and caste development in wood-feeding termites, pp. 159–210, in J. H. Hunt and C. A. Nalepa (eds.), Nourishment and Evolution in Insect Societies. Westview Press, Boulder, Colorado.Google Scholar
  38. 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.CrossRefGoogle Scholar
  39. Liebig, J., Peeters, C., Oldham, N. J., Markstädter, C., and Hölldobler, B. 2000. Are variations in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator? Proc. Natl. Acad. Sci. U.S.A. 97:4124–4131.PubMedCrossRefGoogle Scholar
  40. Light, S. F. 1944. Experimental studies on ectohormonal control of the development of supplementary reproductives in the termite genus Zootermopsis (formerly Termopsis). Univ. Calif. Pub. Zool. 43:413–454.Google Scholar
  41. Light, S. F. and Weesner, F. M. 1951. Further studies in the production of supplementary reproductives in Zootermopsis (Isoptera). J. Exp. Zool. 117:397–414.CrossRefGoogle Scholar
  42. Lüscher, M. 1952. Die produktion und elimination von ersatzgeschlechtstieren bei der termite Kalotermes flavicollis Fabr. Z. Vergl. Physiol. 34:123–141.Google Scholar
  43. Lüscher, M. 1961. Social control of polymorphism in termites. Symp. Roy. Entomol. Soc. Lond. 1:57–67.Google Scholar
  44. Maekawa, K., Ishitani, K., Gotoh, H., Cornette, R., and Miura, T. 2010. Juvenile Hormone titre and vitellogenin gene expression related to ovarian development in primary reproductives compared with nymphs and nymphoid reproductives of the termite Reticulitermes speratus. Physiol. Entomol. 35:52–58.CrossRefGoogle Scholar
  45. Maisonnasse, A., Lenoir, J. C., Beslay, D., Crauser, D., and le Conte, Y. 2010. E-beta-ocimene, a volatile brood pheromone involved in social regulation in the honey bee colony (Apis mellifera). PLos ONE 5:e13531. doi:10.1371/journal.pone.0013531.PubMedCrossRefGoogle Scholar
  46. Matsuura, K. 2006. Termite-egg mimicry by a sclerotium-forming fungus. Proc. Roy. Soc. Lond. B 273:1203–1209.CrossRefGoogle Scholar
  47. Matsuura, K. 2010. Sexual and asexual reproduction in termites, pp. 255–277, in D. E. Bignell, Y. Roisin, and N. Lo (eds.), Biology of Termites: A Modern Synthesis. Springer, Dordrecht.CrossRefGoogle Scholar
  48. Matsuura, K. and Yashiro, T. 2009. The cuckoo fungus ‘termite ball’ mimicking termite eggs: a novel insect-fungal association, pp. 242–255, in J. K. Misra and S. K. Deshmukh (eds.), Fungi from Different Environments. Science Publishers, Enfield, New Hampshire.CrossRefGoogle Scholar
  49. Matsuura, K. and Yashiro, T. 2010. Parallel evolution of termite-egg mimicry by sclerotium-forming fungi in distant termite groups. Biol. J. Linn. Soc. 100:531–537.CrossRefGoogle Scholar
  50. Matsuura, K. and Kobayashi, N. 2010. Termite queens adjust egg size according to colony development. Behav. Ecol. 21:1018–1023.CrossRefGoogle Scholar
  51. Matsuura, K. and Yamamoto, Y. 2011. Workers do not mediate the inhibitory power of queens in a termite, Reticulitermes speratus (Isoptera, Rhinotermitidae). Ins. Soc. 58:513–518.CrossRefGoogle Scholar
  52. Matsuura, K., Tanaka, C., and Nishida, T. 2000. Symbiosis of a termite and a sclerotium-forming fungus: Sclerotia mimic termite eggs. Ecol. Res. 15:405–414.CrossRefGoogle Scholar
  53. Matsuura, K., Tamura, T., Kobayashi, N., Yashiro, T., and Tatsumi, S. 2007. The antibacterial protein lysozyme identified as the termite egg recognition pheromone. PLos ONE 2:e813. doi:10.1371/journal.pone.0000813.PubMedCrossRefGoogle Scholar
  54. Matsuura, K., Vargo, E. L., Kawatsu, K., Labadie, P. E., Nakano, H., Yashiro, T., and Tsuji, K. 2009a. Queen succession through asexual reproduction in termites. Science 323:1687.CrossRefGoogle Scholar
  55. Matsuura, K., Yashiro, T., Shimizu, K., Tatsumi, S., and Tamura, T. 2009b. Cuckoo fungus mimics termite eggs by producing the cellulose-digesting enzyme beta-glucosidase. Curr. Biol. 19:30–36.CrossRefGoogle Scholar
  56. 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. U.S.A. 107:12963–12968.PubMedCrossRefGoogle Scholar
  57. Miura, T., Koshikawa, S., and Matsumoto, T. 2003. Winged presoldiers induced by a juvenile hormone analog in Zootermopsis nevadensis: Implications for plasticity and evolution of caste differentiation in termites. J. Morphol. 257:22–32.PubMedCrossRefGoogle Scholar
  58. Miura, T. and Matsumoto, T. 1996. Ergatoid reproductives in Nasutitermes takasagoensis (Isoptera: Termitidae). Sociobiology 27:223–238.Google Scholar
  59. 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.CrossRefGoogle Scholar
  60. Mori, K. 1998. Chirality and insect pheromones. Chirality 10:578–586.CrossRefGoogle Scholar
  61. Mori, K. 2007. Significance of chirality in pheromone science. Bioorg. Med. Chem. 15:7505–7523.PubMedCrossRefGoogle Scholar
  62. Myles, T. G. 1999. Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution. Sociobiology 33:1–91.Google Scholar
  63. Oldroyd, B. O., Wossler, T. W., and Ratnieks, F. R. 2001. Regulation of ovary activation in worker honey-bees (Apis mellifera): larval signal production and adult response thresholds differ between anarchistic and wild-type bees. Behav. Ecol. Sociobiol. 50:366–370.CrossRefGoogle Scholar
  64. Oster, G. F. and Wilson, E. O. 1978. Caste and Ecology in the Social Insects. Princeton University Press.Google Scholar
  65. Pankiw, T. and Garza, C. 2007. Africanized and European honey bee worker ovarian follicle development response to racial brood pheromone extracts. Apidologie 38:156–163.CrossRefGoogle Scholar
  66. Peeters, C. and Liebig, J. 2009. Fertility signaling as a general mechanism of regulating reproductive division of labor in ants, pp. 220–242, in J. Gadau and J. Fewell (eds.), Organization of Insect Societies: From Genome to Socio-complexity. Harvard University Press, Cambridge, Massachusetts.Google Scholar
  67. Peeters, C., Monnin, T., and Malosse, C. 1999. Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc. Roy. Soc. Lond. B 266:1323–1327.CrossRefGoogle Scholar
  68. Pickens, A. L. 1932. Observations on the genus Reticulitermes Holmgren. Pan-Pac. Entomol. 3:178–180.Google Scholar
  69. Roisin, Y. 1994. Intragroup conflicts and the evolution of sterile castes in termites. Am. Nat. 143:751–765.CrossRefGoogle Scholar
  70. Rosengaus, R. and Traniello, J. 2001. Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angusticollis. Behav. Ecol. Sociobiol. 50:546–556.CrossRefGoogle Scholar
  71. Sannasi, A. and Sundara Rajulu, G. 1967. Occurrence of antimicrobial substance in the exudate of physogastric queen termites, Termes redemanni Wasmann. Curr. Sci 16:436–437.Google Scholar
  72. 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. Ins. Biochem. Mol. Biol. 35:207–215.CrossRefGoogle Scholar
  73. Sledge, M. F., Boscaro, F., and Turillazzi, S. 2001. Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav. Ecol. Sociobiol. 49:401–409.CrossRefGoogle Scholar
  74. Springhetti, A. 1972. I reali nella differenziazione delle caste di Kalotermes flavicollis (Fabr.) (Isoptera). Boll. Zool. 39:83–87.CrossRefGoogle Scholar
  75. 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
  76. Thorne, B. L. 1996. Termite terminology. Sociobiology 28:253–263.Google Scholar
  77. Thorne, B. L., Traniello, J. F. A., Adams, E. S., and Bulmer, M. 1999. Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera Rhinotermitidae): a review of the evidence from behavioral, ecological, and genetic studies. Ethol. Ecol. Evol. 11:149–169.CrossRefGoogle Scholar
  78. Traniello, J. F. A., Rosengaus, R. B., and Savoie, K. 2002. The development of immunity in a social insect: Evidence for the group facilitation of disease resistance. Proc. Natl. Acad. Sci. U.S.A. 99:6838–6842.PubMedCrossRefGoogle Scholar
  79. Trouiller, J., Arnold, G., Le Conte, Y., Masson, C., and Chappe, B. 1991. Temporal pheromonal and kairomonal secretion in the brood of honeybees. Naturwissenschaften 78:368–370.Google Scholar
  80. Tschinkel, W. R. 1988. Social control of egg-laying rate in queens of the fire ant, Solenopsis invicta. Physiol. Entomol. 13:327–350.CrossRefGoogle Scholar
  81. Turillazzi, S., Dapporto, L., Pansolli, C., Boulay, R., Dani, F. R., Moneti, G., and Pieraccini, G. 2006. Habitually used hibernation sites of paper wasps are marked with venom and cuticular peptides. Curr. Biol. 16:R530–R531.PubMedCrossRefGoogle Scholar
  82. Vargo, E. L. 1992. Mutual pheromonal inhibition among queens in polygyne colonies of the fire ant Solenopsis invicta. Behav. Ecol. Sociobiol. 31:205–210.CrossRefGoogle Scholar
  83. Vargo, E. L. 1999. Reproductive development and ontogeny of queen pheromone production in the fire ant Solenopsis invicta. Physiol. Entomol. 24:370–376.CrossRefGoogle Scholar
  84. Vargo, E. L. and Husseneder, C. 2009. Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu. Rev. Entomol. 54:379–403.PubMedCrossRefGoogle Scholar
  85. Weil, T., Hoffmann, K., Kroiss, J., Strohm, E., and Korb, J. 2009. Scent of a queen: cuticular hydrocarbons specific for female reproductives in lower termites. Naturwissenschaften 96:315–319.PubMedCrossRefGoogle Scholar
  86. Wilson, E. O. 1965. Chemical communication in the social insects. Science 149:1064–1071.PubMedCrossRefGoogle Scholar
  87. Wood, W. F., Palmer, T. M., and Stanton, M. L. 2002. A comparison of volatiles in mandibular glands from three Crematogaster ant symbionts of the whistling thorn acacia. Biochem. Sys. Ecol. 30:217–222.CrossRefGoogle Scholar
  88. Yamamoto, Y., Kobayashi, T. and Matsuura, K. 2011. The lack of chiral specificity in a termite queen pheromone. Physiol. Entomol.: doi:10.1111/j.1365-3032.2011.00806.x
  89. Yamamoto, Y. and Matsuura, K. 2011. Queen pheromone regulates egg production in a termite. Biol. Lett. 7:727–729.PubMedCrossRefGoogle Scholar
  90. Yashiro, T. and Matsuura, K. 2007. Distribution and phylogenetic analysis of termite egg-mimicking fungi “termite balls” in Reticulitermes termites. Ann. Entomol. Soc. Am. 100:532–538.CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  1. 1.Laboratory of Insect Ecology, Graduate School of AgricultureKyoto UniversityKyotoJapan

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