Abstract
The conspicuous morphogenesis during termite soldier differentiation is one of the most remarkable examples of specialized caste development in social insects. To clarify the mechanism of morphological changes during soldier differentiation, mandibular morphogenesis prior to the presoldier moult was examined in the damp-wood termite Hodotermopsis sjoestedti. Using experimental induction of presoldier differentiation from pseudergates (7th or later instar larvae) by the application of juvenile hormone analogue (JHA), we compared mandibular morphogenesis in a presoldier moult (from pseudergate to presoldier) with that of a stationary moult (from pseudergate to pseudergate). Future presoldier mandibles were formed under the old mandibular cuticle of the pseudergates just prior to the presoldier moult. Multiple folds of both epidermis and new cuticle were observed in the developing mandible, and large concavities between teeth were formed on the mandibular surface. While in the stationary moult, the future mandibles were formed with a smooth surface. The process of the mandibular morphogenesis in soldier differentiation explains the allometry of soldier mandibles. The morphological differences in mouth parts between castes arise from a switching mechanism that triggers caste-specific mandibular epithelial growth during development.
References
Condic ML, Fristrom D, Fristrom JW (1990) Apical cell shape changes during Drosophila imaginal leg disc elongation: a novel morphogenetic mechanism. Development 111:23–33
Deligne J (1970) Recherches sur la transformation des jeunes en soldats dans la société de termites (Insectes, Isoptères). PhD thesis, University Library, Brussels, Belgium
Deligne J, Quennedey A, Blum MS (1981) The enemies and defense mechanisms of termites. In: Hermann HR (ed) Social insects, vol 2. Academic Press, New York, pp 1–76
Eggleton P (2001) Termites and trees: a review of recent advances in termite phylogenetics. Insectes Soc 48:187–193
Gilbert SF (2000) Developmental biology, 6th edn. Sinauer Associates, Sunderland, Mass.
Grassé PP (1984) Les castes et leurs caractéristiques: le polyéthisme. Termitologia, vol 2, Fondation des societés. Masson, Paris, pp 1–34
Hare L (1937) Termite phylogeny as evidenced by soldier mandible development. Ann Entomol Soc Am 30:459–486
Holmgren N (1911) Termitenstudien. 2. Systematik der Termiten. Die Familien Mastotermitidae, Protermitidae und Mesotermitidae. K Sven Vetenskapsakad Handl 46:1-86
Huang F, Zhu S, Ping Z, He X, Li G, Gao D (2000) Fauna Sinica Insecta, vol 17, Isoptera (in Chinese). Science Press, Beijing, China
Koshikawa S, Matsumoto T, Miura T (2001) Regressive molt in the Japanese damp-wood termite Hodotermopsis japonica (Isoptera: Termopsidae). Sociobiology 38:495–500
Koshikawa S, Matsumoto T, Miura T (2002) Morphometric changes during soldier differentiation of the damp-wood termite Hodotermopsis japonica (Isoptera, Termopsidae). Insectes Soc 49:245–250
Lelis AT, Everaerts C (1993) Effects of juvenile hormone analogues upon soldier differentiation in the termite Reticulitermes santonensis (Rhinotermitidae, Heterotermitinae). J Morphol 217:239–261
Maekawa K, Miura T, Kitade O, Matsumoto T (1998) Genetic variation and molecular phylogeny based on the mitochondrial genes of the damp wood termite Hodotermopsis japonica (Isoptera: Termopsidae). Entomol Sci 1:561–571
Matsumoto T, Hirono Y (1985) On the caste composition of a primitive termite Hodotermopsis japonica Holmgren (Isoptera: Termopsidae). Sci Pap Coll Arts Sci Univ Tokyo 35:211–216
Miura T (2001) Morphogenesis and gene expression in the soldier-caste differentiation of termites. Insectes Soc 48:216–223
Miura T, Matsumoto T (2000) Soldier morphogenesis in a nasute termite: discovery of a disc-like structure forming a soldier nasus. Proc R Soc Lond B 267:1185–1189
Miura T, Roisin Y, Matsumoto T (1998) Developmental pathways and polyethism of neuter castes in the processional nasute termite Hospitalitermes medioflavus (Isoptera: Termitidae). Zool Sci 15:843–848
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 USA 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
Noirot C, Pasteels M (1987) Ontogenetic development and evolution of the worker caste in termites. Experientia 43:851–952
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
Okot-Kotber BM (1985) Mechanisms of caste determination in a higher termite, Macrotermes michaelseni (Isoptera, Macrotermitidae). In: Watson JAL, Okot-Kotber BM, Noirot C (eds) Caste differentiation in social insects. Pergamon, Oxford, pp 267–306
Quennedey A, Quennedey B (1990) Morphogenesis of the wing anlagen in the mealworm beetle Tenebrio molitor during the last larval instar. Tissue Cell 22: 721–740
Reynolds SE (1980) Integration of behaviour and physiology in ecdysis. Adv Insect Physiol 15:475–595
Roisin Y (1996) Castes in humivorous and litter-dwelling neotropical nasute termites (Isoptera, Termitidae). Insects Soc 43:375-389
Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer Academic, Dordrecht, The Netherlands, pp 95–119
Takematsu Y (1996) A taxonomic revision of the Japanese termites from a chemical approach by the cuticular hydrocarbon analysis (Isoptera). PhD thesis, Kyushu University, Japan
Truman JW, Riddiford LM (1999) The origins of insect metamorphosis. Nature 401:447-452
Weesner FM (1969) External anatomy. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic Press, New York, pp 19–47
Wilson EO (1971) The insect societies. Harvard University Press, Cambridge, Mass.
Acknowledgements
We are grateful to Dr. K. Maekawa, Dr. M. Machida, Dr. R. Cornette, Dr. J. Garcia, Mr. S. Sameshima, Mr. H. Katoh, Mr. N. Ijichi, Mr. M. Hojo and Ms. A. Gotoh for their valuable comments on the study and assistance in field sampling. We are also grateful to Dr. Y. Takematsu for her suggestions on taxonomy. Thanks are also due to Sumitomo Chemical Company for supplying the pyriproxyfen. This work was supported by a Grant-in-Aid for Scientific Research (Nos. 13440228, 13740435 and 1440513) from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and the Research for the Future Program of the Japan Society for the Promotion of Science (JSPS). The first author, S. Koshikawa, was supported by JSPS Research Fellowship for Young Scientists.
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Koshikawa, S., Matsumoto, T. & Miura, T. Mandibular morphogenesis during soldier differentiation in the damp-wood termite Hodotermopsis sjoestedti (Isoptera: Termopsidae). Naturwissenschaften 90, 180–184 (2003). https://doi.org/10.1007/s00114-003-0408-5
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DOI: https://doi.org/10.1007/s00114-003-0408-5