Not only soldiers have weapons: evolution of the frontal gland in imagoes of the termite families Rhinotermitidae and Serritermitidae
Language English Country United States Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
21209882
PubMed Central
PMC3012694
DOI
10.1371/journal.pone.0015761
Knihovny.cz E-resources
- MeSH
- Biological Evolution MeSH
- Species Specificity MeSH
- Endocrine Glands anatomy & histology physiology MeSH
- Head anatomy & histology growth & development MeSH
- Isoptera anatomy & histology growth & development MeSH
- Skull physiology MeSH
- Microscopy, Electron, Scanning methods MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND: The frontal gland is a unique adaptation of advanced termite families. It has been intensively studied in soldiers with respect to its anatomy and chemistry, with numerous novel compounds being discovered within the tremendous richness of identified products. At the same time, the presence of the frontal gland in non-soldier castes received only negligible attention in the past. PRINCIPAL FINDINGS: Here, we report on the development of the frontal gland in alate imagoes of 10 genera and 13 species of Rhinotermitidae and Serritermitidae, in order to shed light on the evolution and function of this gland in imagoes. All investigated species possess a frontal gland. In most cases, it is well-developed and equipped with a sac-like reservoir, located in the postero-dorsal part of cranium, but reaching as far as the seventh abdominal segment in some Rhinotermitinae. The only exception is the genus Psammotermes, in which the gland is very small and devoid of the reservoir. CONCLUSIONS: Our direct observations and comparisons with soldiers suggest a defensive role of the gland in imagoes of all studied species. This functional analogy, along with the anatomic homology between the frontal gland in soldiers and imagoes, make it likely that the gland appeared once during the early evolution of rhinotermitid ancestors, and remained as a defensive organ of prime importance in both, soldiers and imagoes.
See more in PubMed
Deligne J, Quennedey A, Blum MS. The enemies and defense mechanisms of termites. In: Hermann HR, editor. Social insects. New York: Academic Press; 1981. pp. 1–76. Volume 2.
Eggleton P, Bignell DE, Sands WA, Mawdsley NA, Lawton JH, et al. The diversity, abundance and biomass of termites under differing levels of disturbance in the Mbalmayo Forest Reserve, southern Cameroon. Philos Trans R Soc Lond Ser B-Biol Sci. 1996;351:51–68.
Noirot C, Darlington JPEC. Termite Nests: Architecture, Regulation and Defence. In: Abe T, Bignell DE, Higashi M, editors. Termites: evolution, sociality, symbioses, ecology. London: Kluwer Academic Publishers; 2000. pp. 121–139.
Hare L. Termite phylogeny as evidenced by soldier mandible development. Ann Entomol Soc Am. 1937;30:459–486.
Seid MA, Scheffrahn RH, Niven JE. The rapid mandible strike of a termite soldier. Curr Biol. 2008;18:R1049–R1050. PubMed
Prestwich GD. Defense mechanisms of termites. Annu Rev Entomol. 1984;29:201–232.
Quennedey A. Morphology and ultrastructure of termite defense glands. In: Hermann HR, editor. Defensive mechanisms in social insects. New York: Praeger; 1984. pp. 151–200.
Šobotník J, Hanus R, Jirošová A. Chemical warfare in termites. J Insect Physiol. 2010;56:1012–1021. PubMed
Noirot C. Glands and secretions. In: Krishna K, Weesner FM, editors. Biology of termites, London & New York: Academic Press; 1969. pp. 89–123. vol 1.
Prestwich GD. Interspecific variation of diterpene composition of Cubitermes soldier defense secretions. J Chem Ecol. 1984;10:1219–1231. PubMed
Lelis ATD, Everaerts C. Effects of juvenile hormone analogs upon soldier differentiation in the termite Reticulitermes santonensis (Rhinotermitidae: Heterotermitinae). J Morphol. 1993;217:239–261. PubMed
Bordereau C, Robert A, Vantuyen V, Peppuy A. Suicidal defensive behaviour by frontal gland dehiscence in Globitermes sulphureus Haviland soldiers (Isoptera). Insectes Soc. 1997;44:289–297.
Šobotník J, Weyda F, Hanus R, Kyjaková P, Doubský J. Ultrastructure of the frontal gland in Prorhinotermes simplex (Isoptera: Rhinotermitidae) and quantity of the defensive substance. Eur J Entomol. 2004;101:153–163.
Holmgren N. Termitenstudien. I. Anatomische Untersuchungen. Kgl Svenska Vetenskapsakad Handl. 1909;44:1–215.
Feytaud J. Contribution à l'étude du Termite lucifuge (anatomie, fondation de colonies nouvelles). Arch Anat Microsc Morphol Exp. 1912;13:481–607.
Bugnion E. Le Termes horni Wasm. de Ceylan. Rev Suisse Zool. 1913;21:299–330.
Šobotník J, Sillam-Dussès D, Weyda F, Dejean A, Roisin Y, et al. The frontal gland in workers of Neotropical soldierless termites. Naturwissenschaften. 2010;97:495–503. PubMed
Šobotník J, Bourguignon T, Hanus R, Weyda F, Roisin Y. Structure and function of defensive glands in soldiers of Glossotermes oculatus (Isoptera: Serritermitidae). Biol J Linnean Soc. 2010;99:839–848.
Noirot C, Quennedey A. Fine structure of insect epidermal glands. Annu Rev Entomol. 1974;19:61–80.
Piskorski R, Hanus R, Kalinová B, Valterová I, Křeček J, et al. Temporal and geographic variations in the morphology and chemical composition of the frontal gland in imagoes of Prorhinotermes species (Isoptera: Rhinotermitidae). Biol J Linnean Soc. 2009;98:384–392.
Šobotník J, Hubert J. The morphology of the exocrine glands of Prorhinotermes simplex (Isoptera: Rhinotermitidae). Acta Soc Zool Bohem. 2003;67:83–98.
Lo N, Kitade O, Miura T, Constantino R, Matsumoto T. Molecular phylogeny of the Rhinotermitidae. Insectes Soc. 2004;51:365–371.
Inward DJG, Vogler AP, Eggleton P. A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol Phylogenet Evol. 2007;44:953–967. PubMed
Legendre F, Whiting MF, Bordereau C, Cancello EM, Evans TA, et al. The phylogeny of termites (Dictyoptera: Isoptera) based on mitochondrial and nuclear markers: Implications for the evolution of the worker and pseudergate castes, and foraging behaviors. Mol Phylogenet Evol. 2008;48:615–627. PubMed
Ohkuma M, Yuzawa H, Amornsak W, Sornnuwat Y, Takematsu Y, et al. Molecular phylogeny of Asian termites (Isoptera) of the families Termitidae and Rhinotermitidae based on mitochondrial COII sequences. Mol Phylogenet Evol. 2004;31:701–710. PubMed
Nutting WL. Flight and colony foundation. In: Krishna K, Weesner FM, editors. Biology of termites, London & New York: Academic Press; 1969. pp. 233–282. vol 1.
Kuldová J, Hrdý I, Svatoš A. Defense secretion of Prorhinotermes simplex: Toxicity to insecticide susceptible and resistant house fly. J Chem Ecol. 1999;25:657–662.
Evans DA, Baker R, Howse PE. Amsterdam: Elsevier/North Holland Biomedical Press; 1976. The chemical ecology of termite defence behaviour. In: Ritter FJ, editor. Chemical ecology: odour communication in animals: scientific aspects, practical uses and economic prospects. Proceedings of the Advanced Research Institute on Chemical Ecology: Odour Communication in Animals. pp. 213–224.
Mill AE. Behavioural and toxic effects of termite defensive secretions on ants. Physiol Entomol. 1983;8:413–418.