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Sexual and Asexual Reproduction in Termites

  • Kenji Matsuura

Abstract

The evolution and maintenance of sexual reproduction is believed to involve important tradeoffs. Queens of social insects face a dilemma over the costs and benefits of sexual and asexual reproduction. Asexual reproduction by a queen doubles her contribution to the gene pool. However, overuse of asexual reproduction reduces the offspring’s genetic diversity and thus the colony’s ability to adapt to environmental stress. Recent investigations on breeding systems using molecular markers revealed that queens of some termites can solve this tradeoff by their conditional use of sexual and asexual reproduction, where queens produce additional (and/or subsequent) queens by parthenogenesis, but use sexual reproduction to produce workers. The asexual queen succession (AQS) system enables the primary queen to maintain her full genetic contribution to the next generation, while avoiding any loss in genetic diversity from inbreeding. In other words, this system gives, in effect, genetically eternal lives to the primary queens. In this chapter, I discuss how eusociality, with its attendant caste structure and unique life histories, can generate novel reproductive and genetic systems with mixed modes of reproduction. This provides important insights into the advantages and disadvantages of sexual reproduction.

Keywords

Sexual Reproduction Asexual Reproduction Termite Species Subterranean Termite Eusocial Insect 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The study on asexual queen succession was conducted by collaboration with Edward L. Vargo at North Carolina State University and Kazuki Tsuji at University of Ryukyus. I am grateful to L. Keller. K. Ross, N. E. Pierce, D. Haig, P. E. Labadie, D. J. C. Kronauer, K. Shimizu, T. Yashiro, K. Kawatsu and H. Nakano for helpful discussion.

References

  1. Afzal M, Salihah Z (1985) Sex ratio, occurrence of parthenogenesis, ovarian development and oviposition behaviour of the primary reproductives of Bifiditermes beesoni (Gardner) (Isoptera, Kalotermitidae). Z Angew Entomol 100:132–146CrossRefGoogle Scholar
  2. Baer B, Schmid-Hempel P (2001) Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 55:1639–1643PubMedGoogle Scholar
  3. Ball SL (2002) Population variation and ecological correlates of tychoparthenogenesis in the mayfly Stenonema femoratum. Biol J Linn Soc 75:101–123CrossRefGoogle Scholar
  4. Bartz SH (1979) Evolution of eusociality in termites. Proc Natl Acad Sci U S A 76:5764–5768PubMedCrossRefGoogle Scholar
  5. Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. University of California Press, San Francisco, CAGoogle Scholar
  6. Bergamaschi S, Dawes-Gromadzki TZ, Scali V, et al (2007) Karyology, mitochondrial DNA and the phylogeny of Australian termites. Chromosome Res 15:735–753PubMedCrossRefGoogle Scholar
  7. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton, NJGoogle Scholar
  8. Cagniant H (1979) Thelytoky and arrhenotoky in the ant Cataglyphis cursor Fonsc (Hymenoptera: Formicidae): biological cycle in laboratory rearing of colonies with a queen and colonies without a queen. Insect Soc 26:51–60CrossRefGoogle Scholar
  9. Cazemajor M, Joly D, Montchamp-Moreau C (2000) Sex-ratio meiotic drive in Drosophila simulans is related to equational nondisjunction of the Y chromosome. Genetics 154:229–236PubMedGoogle Scholar
  10. Chhotani OB (1962) Further observations on biology and parthenogenesis in the termite Kalotermes beesoni (Kalotermitidae). In: Termites in the humid tropics: proceedings of the New Delhi symposium. Paris, UNESCO, pp 73–75.Google Scholar
  11. Corley LS, Blankenship JR, Moore AJ (2001) Genetic variation and asexual reproduction in the facultatively parthenogenetic cockroach Nauphoeta cinerea: implication for the evolution of sex. J Evol Biol 14:68–74CrossRefGoogle Scholar
  12. Corley LS, Moore AJ (1999) Fitness of alternative modes of reproduction: developmental constraints and the evolutionary maintenance of sex. Proc R Soc Lond B Biol 266:471–476CrossRefGoogle Scholar
  13. Cuellar O (1977) Animal parthenogenesis. Science 197:837–843PubMedCrossRefGoogle Scholar
  14. DeHeer CJ, Vargo EL (2006) An indirect test of inbreeding depression in the termites Reticulitermes flavipes and Reticulitermes virginicus. Behav Ecol Sociobiol 59:753–761CrossRefGoogle Scholar
  15. Fei HX, Henderson G (2003) Comparative study of incipient colony development in the Formosan subterranean termite, Coptotermes formosanus Shiraki (Isoptera, Rhinotermitidae). Insect Soc 50:226–233CrossRefGoogle Scholar
  16. Fournier D, Estoup A, Orivel J, et al (2005) Clonal reproduction by males and females in the little fire ant. Nature 435:1230–1234PubMedCrossRefGoogle Scholar
  17. Goldstein DB (1994) Deleterious mutations and the evolution of male haploidy. Am Nat 144:176–183CrossRefGoogle Scholar
  18. Grasso DA, Wenseleers T, Mori A, et al (2000) Thelytokous worker reproduction and lack of Wolbachia infection in the harvesting ant Messor capitatus. Ethol Ecol Evol 12:309–314CrossRefGoogle Scholar
  19. Grassé PP (1949) Ordre des Isoptères ou termites. In: Grassé P-P (ed) Traité de zoologie, vol 9. Masson, Paris, pp 408–544Google Scholar
  20. Gruber M, Hoffmann B, Ritchie P, Lester P (2010) Crazy ant sex: genetic caste determination, clonality and inbreeding in a population of invasive yellow crazy ants. Proceedings of the 16th Congress of IUSSI: 93Google Scholar
  21. Hartmann A, Wantia J, Torres JA, Heinze J (2003) Worker policing without genetic conflicts in a clonal ant. Proc Natl Acad Sci U S A 100:12836–12840PubMedCrossRefGoogle Scholar
  22. Hartmann A, Wantia J, Heinze J (2005) Facultative sexual reproduction in the parthenogenetic ant Platythyrea punctata. Insectes Soc 52:155–162CrossRefGoogle Scholar
  23. Heinze J, Hölldobler B (1995) Thelytokous parthenogenesis and dominance hierarchies in the ponerine ant Platythyrea punctata. Naturwissenschaften 82:40–41Google Scholar
  24. Howard RW, Mallette EJ, Haverty MI, Smythe RV (1981) Laboratory evaluation of within-species, between-species, and parthenogenetic reproduction in Reticulitermes flavipes and Reticulitermes virginicus. Psyche 88:75–87CrossRefGoogle Scholar
  25. Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58:1251–1260PubMedGoogle Scholar
  26. Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213–1216PubMedCrossRefGoogle Scholar
  27. Ito F, Touyama Y, Gotoh A, Kitahiro S, Billen J (2010) Thelytokous parthenogenesis by queens in the dacetine ant Pyramica membranifera (Hymenoptera: Formicidae). Naturwissenschaften 97:725–728PubMedCrossRefGoogle Scholar
  28. Jones SC, LaFage JP, Howard RW (1988) Isopteran sex-ratios: phylogenetic trends. Sociobiology 14:89–156Google Scholar
  29. Jones JC, Myerscough MR, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404PubMedCrossRefGoogle Scholar
  30. Kondrashov AS (1993) Classification of hypotheses on the advantage of amphimixis. J Hered 84:372–387PubMedGoogle Scholar
  31. Kramer MG, Templeton AR (2001) Life-history changes that accompany the transition from sexual to parthenogenetic reproduction in Drosophila mercatorum. Evolution 55:748–761PubMedCrossRefGoogle Scholar
  32. Kurup NC, Prabhoo NR (1977) Facultative parthenogenesis in Cyphoderus javanus (Collembola: Insecta). Curr Sci India 46:168–168Google Scholar
  33. Lamb RY, Willey RB (1987) Cytological mechanism of thelytokous parthenogenesis in insects. Genome 29:367–369CrossRefGoogle Scholar
  34. Lenoir A, Querard L, Pondicq N, Berton F (1988) Reproduction and dispersal in the ant Cataglyphis cursor (Hymenoptera, Formicidae). Psyche 95:21–44CrossRefGoogle Scholar
  35. Light SF (1944) Parthenogenesis in termites of the genus Zootermopsis. Univ Calif Publ Zool 43:405–412Google Scholar
  36. Matsuura K (2002) A test of the haplodiploid analogy hypothesis in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 95:646–649CrossRefGoogle Scholar
  37. 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). Insect Soc 51:325–332CrossRefGoogle Scholar
  38. Matsuura K, Fujimoto M, Goka K, Nishida T (2002) Cooperative colony foundation by termite female pairs: altruism for survivorship in incipient colonies. Anim Behav 64:167–173CrossRefGoogle Scholar
  39. Matsuura K, Kobayashi N (2007) Size, hatching rate, and hatching period of sexually and asexually produced eggs in the facultatively parthenogenetic termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Appl Entomol Zool 42:241–246CrossRefGoogle Scholar
  40. Matsuura K, Nishida T (2001) Comparison of colony foundation success between sexual pairs and female asexual units in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Popul Ecol 43:119–124CrossRefGoogle Scholar
  41. Matsuura K, Tamura T, Kobayashi N, et al (2007) The antibacterial protein lysozyme identified as the termite egg recognition pheromone. PLos ONE 2:e813. doi:10.1371/journal.pone.0000813PubMedCrossRefGoogle Scholar
  42. Matsuura K, Tanaka C, Nishida T (2000) Symbiosis of a termite and a sclerotium-forming fungus: sclerotia mimic termite eggs. Ecol Res 15:405–414CrossRefGoogle Scholar
  43. Matsuura K, Vargo EL, Kawatsu K, et al (2009) Queen succession through asexual reproduction in termites. Science 323:1687–1687Google Scholar
  44. Modig AO (1996) Effects of body size and harem size on male reproductive behaviour in the southern elephant seal. Anim Behav 51:1295–1306CrossRefGoogle Scholar
  45. Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407PubMedCrossRefGoogle Scholar
  46. Nur U (1971) Parthenogenesis in Coccids (Homoptera). Am Zool 11:301–308Google Scholar
  47. Ohkawara K, Nakayama M, Satoh A, et al (2006) Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi. Biol Lett 2:359–363PubMedCrossRefGoogle Scholar
  48. Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends Ecol Evol 22:408–413PubMedCrossRefGoogle Scholar
  49. Pearcy M, Aron S, Doums C, Keller L (2004) Conditional use of sex and parthenogenesis for worker and queen production in ants. Science 306:1780–1783PubMedCrossRefGoogle Scholar
  50. Pearcy M, Goodisman M, Keller L (2010) Sib-mating without inbreeding in the crazy ant. Proceedings of the 16th Congress of IUSSI: 97Google Scholar
  51. Pennisi E (2003) Bickering genes shape evolution. Science 301:1837–1839PubMedCrossRefGoogle Scholar
  52. Rabeling C, Lino-Neto J, Cappellari SC, et al (2009) Thelytokous parthenogenesis in the fungus-gardening ant Mycocepurus smithii (Hymenoptera: Formicidae). PLoS ONE 4:e6781. doi:10.1371/journal.pone.0006781PubMedCrossRefGoogle Scholar
  53. Roisin Y (2001) Caste sex ratios, sex linkage, and reproductive strategies in termites. Insect Soc 48:224–230CrossRefGoogle Scholar
  54. Rosengaus RB, Guldin MR, Traniello JFA (1998) Inhibitory effect of termite fecal pellets on fungal spore germination. J Chem Ecol 24:1697–1706CrossRefGoogle Scholar
  55. Roth LM, Willis ER (1956) Parthenogenesis in cockroaches. Ann Entomol Soc Am 49:31–37Google Scholar
  56. Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within honeybee colonies. Proc R Soc Lond B Biol 274:67–72CrossRefGoogle Scholar
  57. Stansly PA, Korman AK (1993) Parthenogenetic development in Velocitermes spp (Isoptera, Nasutitermitidae). Sociobiology 23:13–24Google Scholar
  58. Syren RM, Luykx P (1977) Permanent segmental interchange complex in the termite Incisitermes schwarzi. Nature 266:167168CrossRefGoogle Scholar
  59. Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc Lond B Biol 270:99–103CrossRefGoogle Scholar
  60. Templeton A (1982) The prophecies of parthenogenesis. In: Dingle H, Hegmann JP (eds) Evolution and genetics of life histories. Springer-Verlag, Berlin, pp 75–102CrossRefGoogle Scholar
  61. Thomas RJ (1987) Factors affecting the distribution and activity of fungi in the nest of Macrotermitinae (Isoptera). Soil Biol Biochem 19:343–349CrossRefGoogle Scholar
  62. 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
  63. Timmermans I, Hefetz A, Fournier D, Aron S (2008) Population genetic structure, worker reproduction and thelytokous parthenogenesis in the desert ant Cataglyphis sabulosa. Heredity 101:490–498PubMedCrossRefGoogle Scholar
  64. Tsuji K (1988) Obligate parthenogenesis and reproductive division of labor in the Japanese queenless ant Pristomyrmex pungens: comparison of intranidal and extranidal workers. Behav Ecol Sociobiol 23:247–255CrossRefGoogle Scholar
  65. Tsuji K, Yamauchi K (1995) Production of females by parthenogenesis in the ant Cerapachys biroi. Insect Soc 42:333–336CrossRefGoogle Scholar
  66. Tucker KW (1958) Automictic parthenogenesis in the honeybee. Genetics 43:299–316PubMedGoogle Scholar
  67. Vargo EL, Husseneder C (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu Rev Entomol 54:379–403PubMedCrossRefGoogle Scholar
  68. Verma S, Ruttner F (1983) Cytological analysis of the thelytokous parthenogenesis in the cape honeybee (Apis mellifera capensis Escholts). Apidologie 14:41–57CrossRefGoogle Scholar
  69. Weesner FM (1956) The biology of colony foundation in Reticulitermes hesperus Banks. Univ Calif Publ Zool 61:253–314Google Scholar

Copyright information

© Springer Netherlands 2010

Authors and Affiliations

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

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