Abstract
In termites, the soldier caste possesses morphological features suitable for colony defence, despite some exceptions. Soldiers are differentiated via two moultings through a presoldier stage with dramatic morphogenesis. While a number of morphological modifications are known to occur during the presoldier moult, growth and morphogenesis seem to continue even after the moult. The present study, using the damp-wood termite Hodotermopsis sjostedti, carried out morphological and histological investigations on the developmental processes during the presoldier stage that is artificially induced by the application of a juvenile hormone analogue. Measurements of five body parameters indicated that head length significantly increased during the 14-day period after the presoldier moult, while it did not increase subsequently to the stationary moult (pseudergate moult as control). Histological observations also showed that the cuticular development played a role in the presoldier head elongation, suggesting that the soft and flexible presoldier cuticle contributed to the soldier morphogenesis in termites.
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References
Andersen SO, Højrup P, Roepstorff P (1995) Insect cuticular proteins. Insect Biochem Mol Biol 25(2):153–176
Bordereau C (1985) The role of pheromones in termite caste differentiation. In: Watson JAL, Okot-Kotber BM, Noirot C (eds) Caste differentiation in social insects. Pergamon, New York, pp 221–249
Bordereau C, Robert A, Vantuyen V, Peppuy A (1997) Suicidal defensive behaviour by frontal gland dehiscence in Globitermes sulphureus Haviland soldiers (Isoptera). Insect Soc 44:289–297
Charles JP (2010) The regulation of expression of insect cuticle protein genes. Insect Biochem Mol Biol 40:205–213
Cornette R, Gotoh H, Koshikawa S, Miura T (2008a) Juvenile hormone titers and caste differentiation in the damp-wood termite Hodotermopsis sjostedti (Isoptera, Termopsidae). J Insect Physiol 54:922–930
Cornette R, Koshikawa S, Miura T (2008b) Histology of the hormone-producing glands in the damp-wood termite Hodotermopsis sjostedti (Isoptera, Termopsidae): a focus on soldier differentiation. Insect Soc 55:407–416
Deligne J, Quennedey A, Blum MS (1981) The enemies and defense mechanisms of termites. In: Hermann HR (ed) Social insects, vol II. Academic, New York, pp 1–76
Hackman RH (1984) Cuticle: biochemistry. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument, vol I. Springer, Berlin, pp 583–610
Hanus R, Šobotník J, Valterová I, Lukáš J (2006) The ontogeny of soldiers in Prorhinotermes simplex (Isoptera, Rhinotermitidae). Insect Soc 53:249–257
Hare L (1937) Termite phylogeny as evidenced by soldier mandible development. Ann Entomol Soc Am 30:459–486
Hattori A, Sugime Y, Sasa C, Miyakawa H, Ishikawa Y, Miyazaki S, Okada Y, Cornette R, Lavine LC, Emlen DJ, Koshikawa S, Miura T (2013) Soldier morphogenesis in the damp-wood termite is regulated by the insulin signaling pathway. J Exp Zool B 320:295–306
Holmgren N (1911) Termitenstudien. 2. Systematik der Termiten. Die Familien Mastotermitidae, Protermitidae und Mesotermitidae. K Sven Vetenskapsakad Handl 46:1–86
Hopkins TL, Kramer KJ (1992) Insect cuticle sclerotization. Ann Rev Entomol 37:273–302
Ishikawa Y, Aonuma H, Miura T (2008) Soldier-specific modification of the mandibular motor neurons in termites. PLoS One 3(7):e2617
Korb J, Hartfelder K (2008) Life history and development—a framework for understanding developmental plasticity in lower termites. Biol Rev Camb Philios Soc 83:295–313
Koshikawa S, Matsumoto T, Miura T (2002) Morphometric changes during soldier differentiation of the damp-wood termite Hodotermopsis japonica (Isoptera: Termopsidae). Insect Soc 49:245–250
Koshikawa S, Matsumoto T, Miura T (2003) Mandibular morphogenesis during soldier differentiation in the damp-wood termite Hodotermopsis sjoestedti (Isoptera: Termopsidae). Naturwissenschaften 90:180–184
Koshikawa S, Cornette R, Hojo M, Maekawa K, Matsumoto T, Miura T (2005) Screening of genes expressed in developing mandibles during soldier differentiation in the termite Hodotermopsis sjostedti. FEBS Lett 579:1365–1370
Lo N, Engel MS, Cameron S, Nalepa CA, Tokuda G, Grimaldi D, Kitade O, Krishna K, Klass KD, Maekawa K, Miura T, Thompson GJ (2007) Save Isoptera: a comment on Inward et al. Biol Lett 3:562–563
Masuoka Y, Yaguchi H, Suzuki R, Maekawa K (2015) Knockdown of the juvenile hormone receptor gene inhibits soldier-specific morphogenesis in the damp-wood termite Zootermopsis nevadensis (Isoptera: Archotermopsidae). Insect Biochem Mol Biol 64:25–31
Matsumoto T, Hirono Y (1985) On the caste composition of a primitive termite Hodotermopsis japonicus Holmgren (Isoptera, Termopsidae). Sci Pap Coll Arts Sci, Univ Tokyo 35:211–216
Miller EM (1969) Caste differentiation in the lower termites. In: Krishna K, Weesner FM (eds) Biology of termites, vol I. Academic, New York, pp 283–310
Miura T (2005) Developmental regulation of caste-specific characters in social-insect polyphenism. Evol Dev 7:122–129
Miura T, Matsumoto T (2000) Soldier morphogenesis in a nasute termite: discovery of a disk-like structure forming a soldier nasus. Proc R Soc Lond B 267:1185–1189
Miura T, Scharf ME (2011) Molecular basis underlying caste differentiation in termites. In: Bignell DE, Roisin Y, Lo N (eds.) Biology of Termites: a Modern Synthesis, Springer, pp 211–253
Miura T, Kamikouchi A, Sawata M, Takeuchi H, Natori S, Kubo T, Matsumoto T (1999) Soldier caste-specific gene expression in the mandibular glands of Hodotermopsis japonica (Isoptera: Termopsidae). Proc Natl Acad Sci U S A 96:13874–13879
Miura T, Hirono Y, Machida M, Kitade O, Matsumoto T (2000) Caste developmental system of the Japanese damp-wood termite Hodotermopsis japonica (Isoptera: Termopsidae). Ecol Res 15:83–92
Miura T, Koshikawa S, Machida M, Matsumoto T (2004) Comparative studies on alate wing formation in two related species of rotten-wood termites: Hodotermopsis sjostedti and Zootermopsis nevadensis (Isoptera: Termopsidae). Insect Soc 51:247–252
Nijhout HF, Wheeler DE (1982) Juvenile hormone and the physiological basis of insect polyphenism. Q Rev Biol 57:109–133
Noirot C (1969) Formation of castes in the higher termites. In: Krishna K, Weesner FM (eds) Biology of termites, vol I. Academic, New York, pp 311–350
Noirot C (1991) Caste differentiation in Isoptera: basic features, role of pheromones. Ethol Ecol Evol 3(sup1):3–7
Noirot C, Pasteels JM (1987) Ontogenic development and evolution of the worker caste in termites. Experientia 43:851–860
Ogino K, Hirono Y, Matsumoto T, Ishikawa H (1993) Juvenile hormone analogue, S-31183, causes a high level induction of presoldier differentiation in the Japanese damp-wood termite. Zool Sci 10:361–366
Prestwich GD (1984a) Defense mechanisms of termites. Annu Rev Entomol 29(1):201–232
Prestwich GD (1984b) Interspecific variation of diterpene composition of Cubitermes soldier defense secretions. J Chem Ecol 10:1219–1231
Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DB, Higashi M (eds) Termites: evolution. Symbioses, Ecology, Kluwer Academic Press, Dordrecht Sociality, pp 95–119
Šobotník J, Weyda F, Hanus R, Kyjaková P, Doubský J (2004) Ultrastructure of the frontal gland in Prorhinotermes simplex (Isoptera: Rhinotermitidae) and quantity of the defensive substance. Eur J Entomol 101:153–163
Šobotník J, Bourguignon T, Hanus R, Sillam-Dussès D, Pflegerová J, Weyda F, Kutalová K, Vytisková B, Roisin Y (2010) Not only soldiers have weapons: evolution of the frontal gland in imagoes of the termite families Rhinotermitidae and Serritermitidae. PLoS One 5, e15761
Šobotník J, Bourguignon T, Hanus R, Demianová Z, Pytelková J, Mareš M, Foltýnová P, Preisler J, Cvačka J, Krasulová J, Roisin Y (2012) Explosive backpacks in old termite workers. Science 337:436
Toga K, Hojo M, Miura T, Maekawa K (2009) Presoldier induction by juvenile hormone analogue in the nasute termite Nasutitermes takasagoensis (Isoptera: Termitidae). Zool Sci 26:382–388
Weesner FM (1969) External anatomy. In: Krishna K, Weesner FM (eds) Biology of termites, vol I. Academic, New York, pp 19–47
Xing L, Chouvenc T, Su NY (2013) Molting process in the Formosan subterranean termite (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 106(5):619–625
Acknowledgments
We would like to express our gratitude to Tetsuo Kohyama for his advice regarding our statistical analysis. We would also like to thank Thomas Bourguignon, Kei Tanabe, Run Minoura, Masaru K. Hojo, and Chifune Sasa for their assistance in conducting the fieldwork. This work was supported by a Grant‐in‐Aid for Scientific Research A (No. 25251041) for TM and by Grant-in-Aid for JSPS Fellows for YS, from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
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Sugime, Y., Ogawa, K., Watanabe, D. et al. Expansion of presoldier cuticle contributes to head elongation during soldier differentiation in termites. Sci Nat 102, 71 (2015). https://doi.org/10.1007/s00114-015-1322-3
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DOI: https://doi.org/10.1007/s00114-015-1322-3