Multiple male and female reproductive strategies and the presence of a polyandric mating system in the termite Reticulitermes labralis (Isoptera:Rhinotermitidae)


  • Jia Wu Northwest University
  • Xiaohong Su Northwest University
  • Xiaohong Kong Northwest University
  • Minghua Liu Northwest University
  • Lianxi Xing Northwest University



subterranean termite, neotenics, reproductive system, polyandry, microsatellite


Reproductive systems of termite colonies may involve the number of individuals in the reproductive caste and the copulatory selectivity of reproductive individuals (i.e., polyandry or polygamy), both of which directly impact the fertility and genetic diversity of the colony. Polygamy is widespread in the lower termites, whereas polyandry appears to be mostly absent in termites. In this paper, the differentiation of male and female neotenics were observed in orphaned experimental colonies of the subterranean termite Reticulitermes labralis. The artificial orphaned colonies began to produce neotenics a week after colony establishing, with more neotenics appearing in the same group over time. Finally, each experimental group reserved multi-neotenics that consisted of male and female neotenic individuals. Our results demonstrated that these neotenic individuals retained in the colony participated in reproduction. A genetic analysis at four microsatellite loci showed that in addition to the conspicuous morphologically male reproductives, there were inconspicuous males or workers that had copulated with the females in the orphaned colony. Multiple male and female reproductive individuals existed together in a single colony, and one female neotenic could mate with several male reproductives in a short time. Thus, multiple male and female reproductive systems and a polyandric mating system are present in R. labralis.


Download data is not yet available.

Author Biographies

Jia Wu, Northwest University

College of Life Sciences

Xiaohong Su, Northwest University

College of Life Sciences

Xiaohong Kong, Northwest University

College of Life Sciences

Minghua Liu, Northwest University

College of Life Sciences

Lianxi Xing, Northwest University

College of Life Sciences


Baer, B. (2011). The copulation biology of ants (Hymenoptera: Formicidae). Myrmecological News 14: 55-68.

Bignell, D.E., Roisin, Y. & Lo., N. (2011). Biology of Termites: A Modern Synthesis.. Springer Press, London: 477-198. DOI:

Boomsma, J.J. (1996). Split sex ratios and queen-male conflict over sperm allocation. Proceedings of the Royal Society B 263: 697-704. DOI:

Dean, S. & Gold, R. (2004). Sex ratios and development of the reproductive system in castes of Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae). Annals of the Entomological Society of America 97: 147-152. Doi:10.1603/0013-8746(2004)097[0147:SRADOT]2.0.CO;2 DOI:[0147:SRADOT]2.0.CO;2

Dronnet, S., Bagnères, A.-G. Juba, T.R., & Vargo, E.L. (2004). Polymorphic microsatellite loci in the European subterranean termite, Reticulitermes santonensis Feytaud. Molecular Ecology Notes 4: 127-129. Doi:10.1111/j.1471-8286.2004.00600.x DOI:

Dronnet, S., Chapuisat, M., Vargo, E.L., Lohou, C. & Bagnères, A-G. (2005). Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Molecular Ecology 14: 1311-1320. Doi: 10.111/j.1365-294x. 2005.02508x DOI:

Fujita, A. & Watanabe, H. (2010). Inconspicuous matured males of worker form are produced in orphanedcolonies of Reticulitermes speratus (Isoptera: Rhinotermitidae) andparticipate in reproduction. Journal of Insect Physiology 56: 1510-1515. Doi: 10.1016/j.jinsphys.2010.04.020 DOI:

Grube, S. & Forschler, B.T. (2004). Census of monogyne and polygyne laboratory colonies illuminates dynamics of population growth in Reticulitermes flavipes (Isoptera: Rhinotermitidae). Annals of the Entomological Society of America 97: 466-475. Doi: 10.1603/0013-8746(2004)097[0466:COMAPL]2.0.CO;2 DOI:[0466:COMAPL]2.0.CO;2

Hartke, T. R. & Baer, B. (2011). The mating biology of termites: a comparative review. Animal Behaviour 82: 927-936. Doi: 10.1016/j. anbehav.2011.07.022 DOI:

Haverty, M.I. & Howard, R.W. (1981). Production of soldiers and maintenance of soldier proportions by laboratory experimental groups of Reticulitermes flavipes (Kollar) and Reticulitermes virginicus (Banks) (Isoptera: Rhinotermitidae). Insectes Sociaux 28: 32-39. DOI:

Howard, R.W. & Haverty, MI. (1980). Reproductives in mature colonies of Reticulitermes flavipes: abundance, sex-ratio, and association with soldiers. Environmental Entomology 9: 458-460. DOI:

Hayashi, Y., Kitade, O. & Kojima J-I. (2003). Parthenogenetic reproduction in neotenics of the subterranean termite Reticulitermes speratus (Isoptera: Rhinotermitidae).Entomological Science 6: 253-257. Doi: 10.1046/j.1343-8786.2003.00030.x DOI:

Ishitani, K. & Maekawa K. (2010). Ovarian development of female-female pairs in the termite, Reticulitermes speratus. Journal of Insect Science 10: 1-12. Doi: 10.1673/031.010.19401 DOI:

Keller, L. & Nonacs, P. (1993). The role of queen pheromones in social insects: queen control or queen signal? Animal Behaviour 45: 787-794. DOI:

Kronauer, D.J., Schöning, C., Pedersen, J.S., Boomsma J.J. & Gadau, J. (2004). Extreme queen-mating frequency and colony fission in African army ants. Molecular Ecology 13: 2381-2388. Doi: 10.1111/j.1365-294X.2004.02262.x DOI:

Lainé, L.V. & Wright, D.J. (2003). The life cycle of Reticulitermes spp.(Isoptera: Rhinotermitidae): what do we know? Bulletin of Entomological Research 93: 267-378. Doi:10.1079/BER2003238 DOI:

Maekawa, K., Ishitani, K., Gotoh, H., Cornette, R. & Miura, T. (2010). Juvenile Hormone titre and vitellogenin gene expression related to ovarian development in primary reproductives, as compared to nymphs and nymphoid reproductives of the termite Reticulitermes speratus. Physiological Entomology 35: 52-58. Doi: 10.111/j.1365-3032.2009.00711.x DOI:

Matsuura, K. & Nishida, T. (2001). Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Population Ecology 43: 115-121. DOI:101007/PL00012022 DOI:

Matsuura, K., Fujimoto, M. & Goka, K. (2004). Sexual and asexual colony foundation and the mechanism of facultative parthenogenesis in the termite Reticulitermes speratus (Isoptera, Rhinotermitidae). Insectes Sociaux 51: 325-332. Doi: 10.1007/s00040-004-0746-0 DOI:

Matsuura, K. & Kobayashi, N. (2007). Size, hatching rate, and hatching period of sexually and asexually produced eggs in the facultatively parthenogenetic termite Reticulitermes speratus (Isoptera: Rhinotermitidae) Applied Entomology and Zoology 42: 241-246. Doi: 10.1303/aez.2007.241 DOI:

Matsuura, K., Vargo, E.L., Kawatsu, K., Labadie, P.E., Nakano, H., Yashiro, T. & Tsuji, K. (2009). Queen succession through asexual reproduction in termites. Science 323: 16-87. Doi:10.1126/science.1169702 DOI:

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.

Neoh, K.B., Lenz, M. & Lee, C.Y. (2010). Impact of orphaning on field colonies of Southeast Asian Macrotermes gilvus (Hagen) and M. carbonarius (Hagen) (Termitidae, Macrotermitinae) Insectes Sociaux 57: 431-439. Doi: 10.1007/s00040-010-0101-6 DOI:

Nutting, W.L. (1969). Flight and colony foundation. In: Biology of Termites, Vol. I (Ed. by K. Krishna and F. M. Weesner). Academic Press, New York: 233-282. DOI:

Pichon, A., Kutnik, M., Leniaud, L., Darrouzet, E., Chaline, N., Dupont, S. & Bagneres, A-G. (2007). Development of Experimentally Orphaned Termite Worker Colonies of Two Reticulitermes Species (Isoptera: Rhinotermitidae) Sociobiology 50: 1015-1034.

Roisin, Y. (1999). Philopatric reproduction, a prime mover in the evolution of termite sociality? Insectes Sociaux 46: 297-305. Doi: 10.1007/s000400050149 DOI:

Roisin, Y. (2000). Diversity and evolution of caste patterns. In: Abe, T., Bignell, D.E.,Higashi, M. (Eds.), Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers, Dordrecht: 95-119. DOI:

Snyder, T.E. (1926). The biology of the termite castes. Quarterly Review of Biology 1: 522-552. DOI:

Strassmann, J. (2001). The rarity of multiple mating by females in the social Hymenoptera. Insectes Sociaux 48: 1-13. Doi: 10.1007/PL00001737 DOI:

Su, X., Wang, Y., Wei, Y. & Zhu, R. (2010). Immunocytochemical localization of androgen receptor-like in spermatogenesis in reproductives and workers of Reticulitermes aculabialis (Isoptera:Rhinotermitidae). Acta Entomologica Sinica 53: 221-225.

Takematsu, Y. (1992). Biometrical study on the development of the castes in Reticulitermes speratus (Isoptera: Rhinotermitidae). Japanese Journal of Entomology 62: 719– 722.

Thorne, B.L. (1996). Termite terminology. Sociobiology 28: 253–261.

Thorne, B.L. (1998). Biology of subterranean termites of the genus Reticulitermes. In Thorne, B.L. and Forschler, B.T. (eds.), NPCA Research Report on Subterranean Termites. National Pest Management Association, Inc., Dunn Loring, VA: 1-30.

Thorne, B.L., Traniello, J.F.A., Adams, E.S. & Bulmer, M. (1999). Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera: Rhinotermitidae): a review of the evidence from behavioural, ecological, and genetic studies. Ethology,Ecology and Evolution 11: 149-169. Doi:10.1080/08927014.1999.9522833 DOI:

Vargo, E.L. (2000). Polymorphism at trinucleotide microsatellite loci in the subterranean termite. Reticulitermes flavipes. Molecular Ecology 9: 817-820. DOI:

Vargo, E.L., Labadie, P.E. & Matsuura, K. (2012). Reticulitermes virginicus Asexual queen succession in the subterranean termite. Proceedings of the Royal Society of London Series B-Biological Sciences 279: 813-819. Doi: 10. 1098/rsbp. 2011. 1030 DOI:

Yamamoto, Y., Kobayashi, T. & Matsuura, K. (2012). The lack of chiral specificity in a termite queen. Pheromone Physiological Entomology 37: 192-195. Doi: 10.111/j.1365-3032.00806.x DOI:

Yamamoto, Y. & Matsuura, K. (2012). Genetic influence on caste determination underlying the asexual queen succession system in a termite. Behavioral Ecology and Sociobiology 66: 39-46. Doi:10.1007/s00265-011-1249-4 DOI:

Ye, Y., Jones, S.C. & Ammar, E. (2009). Reproductive characteristics of imagos of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Annals of the Entomological Society of America 102: 889-894. Doi:10.1603/008.102.0515 DOI:




How to Cite

Wu, J., Su, X., Kong, X., Liu, M., & Xing, L. (2013). Multiple male and female reproductive strategies and the presence of a polyandric mating system in the termite Reticulitermes labralis (Isoptera:Rhinotermitidae). Sociobiology, 60(4), 459–465.



Research Article - Termites