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The TUNEL assay suggests mandibular regression by programmed cell death during presoldier differentiation in the nasute termite Nasutitermes takasagoensis

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Abstract

Termite soldiers are the most specialized caste of social insects in terms of their morphology and function. Soldier development requires increased juvenile hormone (JH) titer and the two molts via a presoldier stage. These molts are accompanied by dramatic morphological changes, including the exaggeration and regression of certain organs. Soldiers of the most apical termitid subfamily Nasutitermitinae possess not only a horn-like frontal tube, called the nasus, for the projection of defensive chemicals from the frontal gland reservoir but also regressed mandibles. Although candidate genes regulating soldier mandibular growth were reported in a relatively basal termite species, the regulatory mechanisms of mandibular regression remain unknown. To clarify these mechanisms, we performed morphological and histological examinations of the mandibles during soldier differentiation in Nasutitermes takasagoensis. Mandibular size reduced dramatically during soldier differentiation, and mandibular regression occurred just prior to the presoldier molt. Spotted TUNEL signals were observed in regressing mandibles of presoldiers, suggesting that the regression involved programmed cell death. Because soldiers of N. takasagoensis possess exaggerated organs (nasus and frontal gland), the present results suggest that JH-dependent regressive mechanisms exist in the mandibles without interfering with the formation of the exaggerated organs.

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References

  • Chuah CH, Goh SH, Tho YP (1989) Interspecific variation in defense secretions of Malaysian termites from the genus Nasutitermes (Isoptera, Nasutitermitinae). J Chem Ecol 15:549–563

    Article  CAS  Google Scholar 

  • Cornette R, Gotoh H, Koshikawa S, Miura T (2008) Juvenile hormone titers and caste differentiation in the damp-wood termite Hodotermopsis sjostedti (Isoptera, Termopsidae). J Insect Physiol 54:922–930

    Article  PubMed  CAS  Google Scholar 

  • Deligne J, Quennedey A, Blum MS (1981) The enemies and defense mechanisms of termites. In: Hermann HR (ed) Social insects. Academic Press, New York, pp 1–76

    Google Scholar 

  • Emerson AE (1961) Vestigial characters of termites and processes of regressive evolution. Evolution 15:115–131

    Article  Google Scholar 

  • Emlen DJ (2001) Costs and the diversification of exaggerated animal structures. Science 291:1534

    Article  PubMed  CAS  Google Scholar 

  • Emlen DJ, Szafran Q, Corley DI (2006) Insulin signaling and limb-patterning: candidate pathways for the origin and evolutionary diversification of beetle ‘horns’. Heredity 97:179–191

    Article  PubMed  CAS  Google Scholar 

  • Fry CL (2006) Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies. Evol Dev 8:191–201

    Article  PubMed  CAS  Google Scholar 

  • Gotoh A, Sameshima S, Tsuji K, Matsumoto T, Miura T (2005) Apoptotic wing degeneration and formation of an altruism-regulating glandular appendage (gemma) in the ponerine ant Diacamma sp. from Japan (Hymenoptera, Formicidae, Ponerinae). Dev Genes Evol 215:69–77

    Article  PubMed  CAS  Google Scholar 

  • Hojo M, Koshikawa S, Matsumoto T, Miura T (2004) Developmental pathways and plasticity of neuter castes in Nasutitermes takasagoensis (Isoptera: Termitidae). Sociobiology 44:433–441

    Google Scholar 

  • Howard RW, Haverty MI (1979) Termites and juvenile hormone analogues: a review of methodology and observed effects. Sociobiology 4:269–278

    Google Scholar 

  • Hrdý I, Křeček J (1972) Development of superfluous soldiers induced by juvenile hormone analogues in the termite, Reticulitermes lucifugus santonensis. Insectes Soc 19:105–109

    Article  Google Scholar 

  • Kijimoto T, Andrews J, Moczek AP (2010) Programmed cell death shapes the expression of horns within and between species of horned beetles. Evol Dev 12:449–458

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Koshikawa S, Cornette R, Matsumoto T, Miura T (2010) The homolog of ciboulot in the termite (Hodotermopsis sjostedti): a multimeric β-thymosin involved in soldier-specific morphogenesis. BMC Dev Biol 10:63

    Article  PubMed  Google Scholar 

  • Lobbia S, Futahashi R, Fujiwara H (2007) Modulation of the ecdysteroid-induced cell death by juvenile hormone during pupal wing development of Lepidoptera. Arch Insect Biochem Physiol 65:152–163

    Article  PubMed  CAS  Google Scholar 

  • Manjon C, Sanchez-Herrero SM (2007) Sharp boundaries of Dpp signaling trigger local cell death required for Drosophila leg morphogenesis. Nat Cell Biol 9:57–63

    Article  PubMed  CAS  Google Scholar 

  • 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, Heidelberg, pp 211–253

    Google Scholar 

  • Moczek AP, Nijhout HF (2004) Trade-offs during the developmental primary and secondary sexual traits in a horned beetle. Am Nat 163:184–191

    Article  PubMed  Google Scholar 

  • Nijhout HF (1994) Insect hormones. Princeton University, New Jersey

    Google Scholar 

  • Nijhout HF (1999) Control mechanisms of polyphenic development in insects. Bioscience 49:181–192

    Article  Google Scholar 

  • Nijhout HF (2003) Development and evolution of adaptive polyphenisms. Evol Dev 5:9–18

    Article  PubMed  Google Scholar 

  • Nijhout HF, Wheeler DE (1982) Juvenile hormone and the physiological basis of insect polyphenism. Q Rev Biol 57:109–133

    Article  CAS  Google Scholar 

  • Noirot CH (1969) Glands and secretions. In: Krishna K, Weesner FM (eds) Biology of Termites, vol I. Academic, New York, pp 89–123

    Google Scholar 

  • Noirot C, Pasteels JM (1987) Ontogenetic development and evolution of the worker caste in termites. Experientia 43:851–952

    Article  Google Scholar 

  • Prestwich GD (1984) Defense mechanism of termite. Annu Rev Entomol 29:201–232

    Article  CAS  Google Scholar 

  • 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, pp 95–119

    Google Scholar 

  • Sameshima S, Miura T, Matsumoto T (2004) Wing disc development during caste differentiation in the ant Pheidole megacephala (Hymenoptera: Formicidae). Evol Dev 6:336–341

    Article  PubMed  Google Scholar 

  • Sands WA (1957) The soldier mandibles of the Nasutitermitinae (Isoptera, Termitidae). Insectes Soc 4:13–24

    Article  Google Scholar 

  • Šobotník J, Sillam-Dussès D, Weyda F, Dejean A, Roisin Y, Hanus R, Bourguignon T (2010a) The frontal gland in workers of neotropical soldierless termites. Naturwissenschaften 97:495–503

    Article  PubMed  Google Scholar 

  • Šobotník J, Jirošová A, Hanus R (2010b) Chemical warfare in termites. J Insect Physiol 56:1012–1021

    Article  PubMed  Google Scholar 

  • Šobotník J, Bourguignon T, Hanus R, Weyda F, Roisin Y (2010c) Structure and function of defensive glands in soldiers of Glossotermes oculatus (Isoptera: Serritermitidae). Biol J Linn Soc 99:839–848

    Article  Google Scholar 

  • Šobotník J, Hanus R, Piskorski R, Urbanová K, Wimmer Z, Weyda F, Vytisková B, Sillam-Dussès D (2010d) Impact of a juvenile hormone analogue on the anatomy and the frontal gland secretion of Prorhinotermes simplex (Isoptera: Rhinotermitidae). J Insect Physiol 56:65–72

    Article  PubMed  Google Scholar 

  • Toga K, Hojo M, Miura T, Maekawa K (2009) Presoldier induction by a juvenile hormone analog in the nasute termite Nasutitermes takasagoensis (Isoptera: Termitidae). Zool Sci 26:382–388

    Article  PubMed  Google Scholar 

  • Tsuchiya M, Watanabe D, Maekawa K (2008) Effect on mandibular length of juvenile hormones and regulation of soldier differentiation in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Appl Entomol Zool 43:307–314

    Article  Google Scholar 

  • Weesner FM (1969) External anatomy. In: Krishna K, Weesner FM (eds) Biology of Termites, Vol. I. Academic, New York, pp 19–47

    Google Scholar 

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Acknowledgments

We are grateful to Dr. Toru Miura for helpful discussions. This study was supported in part by Grant-in Aids for Young Scientists (Nos. 19770012 and 21770079 to KM), and for Scientific Research on Innovative Areas (No. 20200059 to KM) from the Japan Society for the Promotion of Science.

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Correspondence to Kiyoto Maekawa.

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Communicated by: Sven Thatje

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Toga, K., Yoda, S. & Maekawa, K. The TUNEL assay suggests mandibular regression by programmed cell death during presoldier differentiation in the nasute termite Nasutitermes takasagoensis . Naturwissenschaften 98, 801 (2011). https://doi.org/10.1007/s00114-011-0825-9

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  • DOI: https://doi.org/10.1007/s00114-011-0825-9

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