Abstract
Sex ratio, fresh weight and nutrient contents were examined at five developmental stages of alates in the subterranean termite Reticulitermes chinensis Snyder, including sixth-instar nymphs, callow alates, dark alates, flying alates and dealates. The results showed that the sex ratio of callow alates and dark alates was highly female biased, but there were no significant differences in the percentage of females and males at sixth-instar nymphs, flying alates, and dealates. The fresh weights of alates declined with the developmental stages, suggesting a dynamic process in which the termites continue to shrink and harden. Meanwhile, the weights of female alates were significantly higher than weights of male alates in all five stages. There were no significant differences in the protein titers of the five developmental stages of alates. Flying alates were observed to have the highest triglyceride level, but a low glucose titer. This suggested that the main energy for flight of alates is provided by the breakdown of triglyceride reserves. Alates regardless of developmental stages, workers and soldiers had no significant differences in the cholesterol titers for the two extraction methods. Interestingly, there was a significantly negative linear correlation between the titer of glucose and the titer of triglyceride in both female alates and male alates during the five developmental stages, suggesting that the indirect mutual transformation between glucose and triglyceride might occur in the energy metabolism of all alates in R. chinensis.
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Beenakkers A. 1969. Carbohydrate and fat as a fuel for insect flight. A comparative study. J. Insect Physiol. 15: 353–361
Behmer S.T. and David Nes W. 2003. Insect sterol nutrition and physiology: A global overview. In: Adv. Insect Physiol. vol 31. Academic Press, London, pp 1–72
Boomsma J.J., Beekman M., Cornwallis C.K., Griffin A.S., Holman L., Hughes W.O.H., Keller L., Oldroyd B.P. and Ratnieks F.L.W. 2011. Only full-sibling families evolved eusociality. Nature 471: E4–E5
Bourguignon T., Hayashi Y. and Miura T. 2012. Skewed soldier sex ratio in termites: testing the size-threshold hypothesis. Insect. Soc. 59: 557–563
Bradford M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254
Chapman R.F. 1998. The Insects: Structure and Function. Cambridge University Press, London
Carvalho M., Sampaio J.L., Palm W., Brankatschk M., Eaton S. and Shevchenko A. 2012. Effects of diet and development on the Drosophila lipidome. Mol. Syst. Biol. 8: 1–17
Chen H., Li Z., Bu S.H. and Tian Z.Q. 2011. Flight of the Chinese white pine beetle (Coleoptera: Scolytidae) in relation to sex, body weight and energy reserve. B. Entomol. Res. 101: 53–62
Crosland M.W.J., Li G.X., Huang L.W. and Dai Z.R. 1994. Switch to single sex alate production in a colony of the termite, Coptotermes formosanus. J. Entomol. Sci. 29: 523–525
Downer R.G.H. and Matthews J.R. 1976. Patterns of lipid distribution and utilisation in insects. Am. Zool. 16: 733–745
Fisher R.A. 1929. The Genetical Theory of Natural Selection. Dover Press, New York
Foster M.T., Shi H., Seeley R.J. and Woods S.C. 2011. Removal of intra-abdominal visceral adipose tissue improves glucose tolerance in rats: Role of hepatic triglyceride storage. Physiol. Behav. 104: 845–854
Gilbert L.I. and O’Connor J.D. 1970. Lipid metabolism and transport in arthropods. In: Chemical Zoology (Florkin M. and Scheer B., Eds). Academic Press, New York, pp 229–254
Hanus R., Luxová A., Šobotník J., Kalinová B., Jiroš P., Křeček J., Bourguignon T. and Bordereau C. 2009. Sexual communication in the termite Prorhinotermes simplex (Isoptera, Rhinotermitidae) mediated by a pheromone from female tergal glands. Insect. Soc. 56: 111–118
Hayes T., Haston K., Tsui M., Hoang A., Haeffele C. and Vonk A. 2002. Herbicides: feminization of male frogs in the wild. Nature 419: 895–896
Huang Q.Y., Li G.H., Husseneder C. and Lei C.L. 2013. Genetic analysis of population structure and reproductive mode of the termite Reticulitermes chinensis Snyder. PLoS One 8: e69070
Huang Z.Y., Qian X., Zhong J.H., Hu J., Li Z.Q., Li Q.J. and Liu B.R. 2012. Swarm occurring of drywood termites Cryptotermes domesticus (Haviland) at the constant temperature and humidity conditions. J. Environ. Entomol. 34: 382–385 (in Chinese)
Jing X.F., Vogel H., Grebenok R.J., Zhu-Salzman K.Y. and Behmer S.T. 2012. Dietary sterols/steroids and the generalist caterpillar Helicoverpa zea: Physiology, biochemistry and midgut gene expression. Insect Biochem. Molec. 42: 835–845
Jones S., La Fage J. and Howard R. 1988. Isopteran sex ratios: phylogenetic trends. Sociobiology 14: 89–156
Jumbo-Lucioni P., Ayroles J.F., Chambers M.M., Jordan K.W., Leips J., Mackay T.F.C. and De Luca M. 2010. Systems genetics analysis of body weight and energy metabolism traits in Drosophila melanogaster. BMC Genomics 11: 297
Kinyuru J.N., Konyole S.O., Roos N., Onyango C.A., Owino V.O., Owuor B.O., Estambale B.B., Friis H., Aagaard-Hansen J. and Kenji G.M. 2013. Nutrient composition of four species of winged termites consumed in western Kenya. J. Food Compos. Anal. 30: 120–124
Kitade O., Hayashi Y., Kikuchi Y. and Kawarasaki S. 2004. Distribution and composition of colony founding associations of a subterranean termite, Reticulitermes kanmonensis. Entomol. Sci. 7: 1–8
Kolman W.A. 1960. The mechanism of natural selection for the sex ratio. Am. Nat. 94: 373–377
Lefevere K.S., Koopmanschap A.B. and De Kort C.A.D. 1989. Changes in the concentrations of metabolites in haemolymph during and after diapause in female Colorado potato beetle, Leptinotarsa decemlineata. J. Insect Physiol. 35: 121–128
Lenz M. and Runko S. 1993. Long-term impact of orphaning on field colonies of Coptotermes lacteus (Froggatt) (Isoptera: Rhinotermitidae). Insect. Soc. 40: 439–456
Li G.H., Gao Y., Sun P.D., Lei C.L. and Huang Q.Y. 2013. Factors affecting mate choice in the subterranean termite Reticulitermes chinensis (Isoptera: Rhinotermitidae). J. Ethol. 31: 159–164
Liu Y.Z., Peng X.F., Tang G.Q. and Peng X.T. 2002. Development and differentiation of various castes in the immature stage of Reticulitermes chinensis. Acta. Entomol. Sin. 45: 487–493 (in Chinese)
Luchetti A., Velonà A., Mueller M. and Mantovani B. 2013. Breeding systems and reproductive strategies in Italian Reticulitermes colonies (Isoptera: Rhinotermitidae). Insect. Soc. 60: 203–211
Matsuura K. 2006. A novel hypothesis for the origin of the sexual division of labor in termites: which sex should be soldiers? Evol. Ecol. 20: 565–574
Matsuura K. 2011. Sexual and asexual reproduction in termites. In: Biology of Termites: A Modern Synthesis (Bignell D.E., Roisin Y. and Lo N., Eds). Springer, pp 255–277
Matsuura K. and Nishida T. 2001. Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Popul. Ecol. 43: 119–124
Mitchell J.D. 2007. Swarming and pairing in the fungus-growing termite, Macrotermes natalensis (Haviland) (Isoptera: Macrotermitinae). Afr. Entomol. 15: 153–160
Montez P., Max T.A., Rodriguez R., Viscarra J., Vazquez-Medina J.P., Nakano D., Nishiyama A. and Ortiz R.M. 2012. High dietary glucose intake increases hepatic triglyceride content and oxidative stress: contributions of angiotensin receptor. Faseb J. 26: 714–718
Morgan T.D. and Chippendale G.M. 1983. Free amino acids of the haemolymph of the southwestern corn borer and the European corn borer in relation to their diapause. J. Insect Physiol. 29: 735–740
Muller H. and Korb J. 2008. Male or female soldiers? An evaluation of several factors which may influence soldier sex ratio in lower termites. Insect. Soc. 55: 213–219
Nalepa C., Miller L. and Lenz M. 2001. Flight characteristics of Mastotermes darwiniensis (Isoptera, Mastotermitidae). Insect. Soc. 48: 144–148
Paul D. and Dey S. 2011. Nutrient content of sexual and worker forms of the subterranean termite, Reticulitermes sp. Indian J. Tradit. Know. 10: 505–507
Rockett B.D., Harris M., Teague H. and Shaikh S.R. 2011. Mixed fish/flaxseed oil diets promote body weight gain by lowering whole body energy expenditure in a dose-dependent manner. Faseb J. 25: 9650
Roff D.A. and Fairbairn D.J. 2013. The costs of being dark: the genetic basis of melanism and its association with fitness-related traits in the sand cricket. J. Evol. Biol. 26: 1406–1416
Roonwal M.L. 1975. Sex ratio and sexual dimorphism in termites. J. Sci. Ind. Res. India. 34: 402–416
Sartori M., Keller L., Thomas A.G. and Passera L. 1992. Flight energetics in relation to sexual differences in the mating behaviour of a mayfly, Siphlonurus aestivalis. Oecologia 92: 172–176
Shellman-Reeve J. 1999. Courting strategies and conflicts in a monogamous, biparental termite. Proc. R. Soc. Lond. B 266: 137–144
Shellman-Reeve J.S. 1990. Dynamics of biparental care in the dampwood termite, Zootermopsis nevadensis (Hagen): response to nitrogen availability. Behav. Ecol. Sociobiol. 26: 389–397
Thorne B. 1983. Alate production and sex ratio in colonies of the Neotropical termite Nasutitermes corniger (Isoptera; Termitidae). Oecologia 58: 103–109
Visiedo F., Bugatto F., Sanchez V., Cozar-Castellano I., Bartha J.L. and Perdomo G. 2013. High glucose levels reduce fatty acid oxidation and increase triglyceride accumulation in human placenta. Am. J. Physiol. Endoc. M. 305: E205–E212
Waller D.A. and La Fage J.P. 1987. Nutritional ecology of termites. In: Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates (Slansky F.J. and Rodriguez J.G., Eds). Wiley, New York, pp 487–532
Wheeler D.E. and Buck N.A. 1992. Protein, lipid and carbohydrate use during metamophosis in the fire ant, Solenopsis xyloni. Physiol. Entomol. 17: 397–403
Winkelmann C. and Koop J.H. 2007. The management of metabolic energy storage during the life cycle of mayflies: a comparative field investigation of the collector-gatherer Ephemera danica and the scraper Rhithrogena semicolorata. J. Comp. Physiol. B 177: 119–128
You X.R., Cai M.Y., Jiang Y.H. and Wang Z.Y. 2012. Histological observation on gonadal sex differentiation in large yellow croaker (Larimichthys crocea) J. Fish. 36: 1057–1064 (in Chinese)
Acknowledgments
We are thankful to Mr. Colin Wong from USA for correcting the language of this manuscript. We thank the anonymous reviewers for providing valuable comments on earlier drafts of this manuscript. This work was supported by the Fundamental Research Funds for the Central Universities (2013PY007), the National Department Public Benefit (Agriculture) Research Foundation (201003025), and the Science and Technology Project of National General Administration of Quality Supervision, Inspection and Quarantine (2014IK006).
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Li, G.H., Lei, C.L., Wang, Z.H. et al. Dynamics of sex ratio, fresh weight and nutrient contents at five developmental stages of alates in the subterranean termite Reticulitermes chinensis . Insect. Soc. 62, 51–57 (2015). https://doi.org/10.1007/s00040-014-0373-3
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DOI: https://doi.org/10.1007/s00040-014-0373-3