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Behavioral Ecology and Sociobiology

, Volume 66, Issue 1, pp 39–46 | Cite as

Genetic influence on caste determination underlying the asexual queen succession system in a termite

  • Yuuka YamamotoEmail author
  • Kenji Matsuura
Original Paper
First Online:

Abstract

The question of how reproductives and sterile workers differentiate within eusocial groups has long been a core issue in the study of social insects. Recent studies have shown that not only environmental factors but also genetic factors affect caste differentiation. In the termite Reticulitermes speratus, queens produce their replacements (neotenics) asexually but use normal sexual reproduction to produce other colony members. Here, we demonstrate a genetic influence on caste determination underlying the asexual queen succession system in this termite species. Thelytoky in termites is accomplished by automixis with terminal fusion, yielding almost completely homozygous offspring; thus, parthenogenetically and sexually produced offspring profoundly differ in heterozygosity. An analysis of the relationship between the reproductive dominance of female neotenics obtained from experimentally orphaned colonies and their genotypes at five microsatellite loci showed that homozygosity at two loci influenced the developmental priority and/or reproductive quality of neotenics. These results suggest the existence of a multi-locus system affecting the queen fecundity and explain why parthenogens have genetic priority to become neotenics in this termite species.

Keywords

Genetic caste determination Caste differentiation Parthenogenesis Queen fecundity Social insect 
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Notes

Acknowledgements

We thank H. Nakano and T. Yashiro for research assistance; and E.L. Vargo, C. Himuro, K. Shimizu, and T. Yokoi for helpful advice. This work was supported by the Japan Society for the Promotion of Science (no.09001407) to K.M. and the Programme for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry to K.M.

References

  1. Adams ES, Atkinson L (2008) Queen fecundity and reproductive skew in the termite Nasutitermes corniger. Insectes Soc 55:28–36. doi: 10.1007/s00040-007-0970-5 CrossRefGoogle Scholar
  2. Atkinson L, Adams ES (1997) The origins and relatedness of multiple reproductives in colonies of the termite Nasutitermes corniger. Proc R Soc Lond B 264:1131–1136. doi: 10.1098/rspb.1997.0156 CrossRefGoogle Scholar
  3. Cahan SH, Parker JD, Rissing SW, Johnson RA, Polony TS, Weiser MD, Smith DR (2002) Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants. Proc R Soc Lond B 269:1871–1877. doi: 10.1098/rspb.2002.2061 CrossRefGoogle Scholar
  4. Dronnet S, Bagneres AG, Juba TR, Vargo EL (2004) Polymorphic microsatellite loci in the European subterranean termite, Reticulitermes santonensis Feytaud. Mol Ecol Notes 4:127–129. doi: 10.1111/j.1471-8286.2004.00600.x CrossRefGoogle Scholar
  5. Fletcher DJC, Ross KG (1985) Reguration of reproduction in eusocial Hymenoptera. Annu Rev Entomol 30:319–343CrossRefGoogle Scholar
  6. Fournier D, Estoup A, Orivel J, Foucaud J, Jourdan H, Le Breton J, Keller L (2005) Clonal reproduction by males and females in the little fire ant. Nature 435:1230–1234. doi: 10.1038/nature03705 PubMedCrossRefGoogle Scholar
  7. Hayashi Y, Lo N, Miyata H, Kitade O (2007) Sex-linked genetic influence on caste determination in a termite. Science 318:985–987. doi: 10.1126/science.1146711 PubMedCrossRefGoogle Scholar
  8. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, CambridgeGoogle Scholar
  9. Hughes WOH, Boomsma J (2008) Genetic royal cheats in leaf-cutting ant societies. Proc Natl Acad Sci USA 105:5150–5153. doi: 10.1073/pnas.0710262105 PubMedCrossRefGoogle Scholar
  10. Julian GE, Fewell JH, Gadau J, Johnson RA, Larrabee D (2002) Genetic determination of the queen caste in an ant hybrid zone. Proc Natl Acad Sci USA 99:8157–8160. doi: 10.1073/pnas.112222099 PubMedCrossRefGoogle Scholar
  11. Kerr WE (1950) Genetic determination of castes in genus Melipona. Genetics 35:143–152PubMedGoogle Scholar
  12. Korb J, Weil T, Hoffmann K, Foster KR, Rehli M (2009) A gene necessary for reproductive suppression in termites. Science 324:758. doi: 10.1126/science.1170660 PubMedCrossRefGoogle Scholar
  13. Lüscher M (1960) Hormonal control of caste differentiation in termites. Ann N Y Acad Sci 89:549–563CrossRefGoogle Scholar
  14. Matsuura K (2010) Sexual and asexual reproduction in termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Heidelberg, pp 255–277Google Scholar
  15. Matsuura K, Fujimoto M, Goka K (2004) Sexual and asexual colony foundation and the mechanism of facultative parthenogenesis in the termite Reticulitermes speratus (Isoptera, Rhinotermitidae). Insectes Soc 51:325–332. doi: 10.1007/s00040-004-0746-0 CrossRefGoogle Scholar
  16. Matsuura K, Vargo EL, Kawatsu K, Labadie PE, Nakano H, Yashiro T, Tsuji K (2009) Queen succession through asexual reproduction in termites. Science 323:1687. doi: 10.1126/science.1169702 PubMedCrossRefGoogle Scholar
  17. Matsuura K, Himuro C, Yokoi T, Yamamoto Y, Vargo EL, Keller L (2010) Identification of a pheromone regulating caste differentiation in termites. Proc Natl Acad Sci USA 107:12963–12968. doi: 10.1073/pnas.1004675107 PubMedCrossRefGoogle Scholar
  18. 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 24:13874–13879CrossRefGoogle Scholar
  19. Ohkawara K, Nakayama M, Satoh A, Trindl A, Heinze J (2006) Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi. Biol Lett 2:359–363. doi: 10.1098/rsbl.2006.0491 PubMedCrossRefGoogle Scholar
  20. Pearcy M, Aron S, Doums C, Keller L (2004) Conditional use of sex and parthenogenesis for worker and queen production in ants. Science 306:1780–1783. doi: 10.1126/science.1105453 PubMedCrossRefGoogle Scholar
  21. Robinson GE, Page RE (1988) Genetic determination of gurding and undertaking in honeybee colonies. Nature 333:356–358CrossRefGoogle Scholar
  22. Roisin Y, Pasteels JM (1986) Reproductive mechanisms in termites: polycalism and polygyny in Nasutitermes polygynus and N. costalis. Insectes Soc 33:149–167CrossRefGoogle Scholar
  23. Smith CR, Anderson KE, Tillberg CV, Gadau J, Suarez AV (2008) Caste determination in a polymorphic social insect: nutritional, social, and genetic factors. Am Nat 172:497–507. doi: 10.1086/590961 PubMedCrossRefGoogle Scholar
  24. Thorne BL (1984) Polygyny in the neotropical termite Nasutitermes corniger: life history consequences of queen mutualism. Behav Ecol Sociobiol 14:117–136CrossRefGoogle Scholar
  25. Thorne BL, Traniello JFA, Adams ES, Bulmer M (1999) Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera Rhinotermitidae): a review of the evidence from behavioral, ecological, and genetic studies. Ethol Ecol Evol 11:149–169CrossRefGoogle Scholar
  26. Vargo EL (2000) Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Mol Ecol 9:817–820PubMedCrossRefGoogle Scholar
  27. Vargo EL, Husseneder C (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu Rev Entomol 54:379–403. doi: 10.1146/annurev.ento.54.110807.090443 PubMedCrossRefGoogle Scholar
  28. Vargo EL, Labadie PE, Matsuura K (2011) Asexual queen succession in the subterranean termite Reticulitermes virginicus. Proc R Soc Lond B. doi: 10.1098/rspb.2011.1030
  29. Volny VP, Gordon DM (2002) Genetic basis for queen-worker dimorphism in a social insect. Proc Natl Acad Sci USA 99:6108–6111. doi: 10.1073/pnas.092066699 PubMedCrossRefGoogle Scholar
  30. Weil T, Korb J, Rehli M (2009) Comparison of queen-specific gene expression in related lower termite species. Mol Biol Evol 26:1841–1850. doi: 10.1093/molbev/msp095 PubMedCrossRefGoogle Scholar
  31. Wheeler DE (1986) Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am Nat 128:13–34CrossRefGoogle Scholar
  32. Zhou X, Oi FM, Scharf ME (2006) Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proc Natl Acad Sci USA 103:4499–4504. doi: 10.1073/pnas.0508866103 PubMedCrossRefGoogle Scholar
  33. Zimet M, Stuart AM (1982) Sexual dimorphism in the immature stages of the termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 7:1–7Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Laboratory of Insect Ecology, Graduate School of Environmental ScienceOkayama UniversityOkayamaJapan

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