Skip to main content
SpringerLink
Log in

Sexual and Asexual Reproduction in Termites

  • Chapter
  • First Online:
Book cover Biology of Termites: a Modern Synthesis

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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 100:132–146

    Article  Google Scholar 

  • Baer B, Schmid-Hempel P (2001) Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 55:1639–1643

    PubMed  CAS  Google Scholar 

  • Ball SL (2002) Population variation and ecological correlates of tychoparthenogenesis in the mayfly Stenonema femoratum. Biol J Linn Soc 75:101–123

    Article  Google Scholar 

  • Bartz SH (1979) Evolution of eusociality in termites. Proc Natl Acad Sci U S A 76:5764–5768

    Article  PubMed  CAS  Google Scholar 

  • Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. University of California Press, San Francisco, CA

    Google Scholar 

  • Bergamaschi S, Dawes-Gromadzki TZ, Scali V, et al (2007) Karyology, mitochondrial DNA and the phylogeny of Australian termites. Chromosome Res 15:735–753

    Article  PubMed  CAS  Google Scholar 

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton, NJ

    Google Scholar 

  • 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 26:51–60

    Article  Google Scholar 

  • 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 154:229–236

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 14:68–74

    Article  Google Scholar 

  • 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 266:471–476

    Article  Google Scholar 

  • Cuellar O (1977) Animal parthenogenesis. Science 197:837–843

    Article  PubMed  CAS  Google Scholar 

  • DeHeer CJ, Vargo EL (2006) An indirect test of inbreeding depression in the termites Reticulitermes flavipes and Reticulitermes virginicus. Behav Ecol Sociobiol 59:753–761

    Article  Google Scholar 

  • Fei HX, Henderson G (2003) Comparative study of incipient colony development in the Formosan subterranean termite, Coptotermes formosanus Shiraki (Isoptera, Rhinotermitidae). Insect Soc 50:226–233

    Article  Google Scholar 

  • Fournier D, Estoup A, Orivel J, et al (2005) Clonal reproduction by males and females in the little fire ant. Nature 435:1230–1234

    Article  PubMed  CAS  Google Scholar 

  • Goldstein DB (1994) Deleterious mutations and the evolution of male haploidy. Am Nat 144:176–183

    Article  Google Scholar 

  • 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 12:309–314

    Article  Google Scholar 

  • Grassé PP (1949) Ordre des Isoptères ou termites. In: Grassé P-P (ed) Traité de zoologie, vol 9. Masson, Paris, pp 408–544

    Google Scholar 

  • 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: 93

    Google Scholar 

  • 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 100:12836–12840

    Article  PubMed  CAS  Google Scholar 

  • Hartmann A, Wantia J, Heinze J (2005) Facultative sexual reproduction in the parthenogenetic ant Platythyrea punctata. Insectes Soc 52:155–162

    Article  Google Scholar 

  • Heinze J, Hölldobler B (1995) Thelytokous parthenogenesis and dominance hierarchies in the ponerine ant Platythyrea punctata. Naturwissenschaften 82:40–41

    CAS  Google Scholar 

  • 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 88:75–87

    Article  Google Scholar 

  • Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58:1251–1260

    PubMed  Google Scholar 

  • Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213–1216

    Article  PubMed  CAS  Google Scholar 

  • Ito F, Touyama Y, Gotoh A, Kitahiro S, Billen J (2010) Thelytokous parthenogenesis by queens in the dacetine ant Pyramica membranifera (Hymenoptera: Formicidae). Naturwissenschaften 97:725–728

    Article  PubMed  CAS  Google Scholar 

  • Jones SC, LaFage JP, Howard RW (1988) Isopteran sex-ratios: phylogenetic trends. Sociobiology 14:89–156

    Google Scholar 

  • Jones JC, Myerscough MR, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404

    Article  PubMed  CAS  Google Scholar 

  • Kondrashov AS (1993) Classification of hypotheses on the advantage of amphimixis. J Hered 84:372–387

    PubMed  CAS  Google Scholar 

  • Kramer MG, Templeton AR (2001) Life-history changes that accompany the transition from sexual to parthenogenetic reproduction in Drosophila mercatorum. Evolution 55:748–761

    Article  PubMed  CAS  Google Scholar 

  • Kurup NC, Prabhoo NR (1977) Facultative parthenogenesis in Cyphoderus javanus (Collembola: Insecta). Curr Sci India 46:168–168

    Google Scholar 

  • Lamb RY, Willey RB (1987) Cytological mechanism of thelytokous parthenogenesis in insects. Genome 29:367–369

    Article  Google Scholar 

  • Lenoir A, Querard L, Pondicq N, Berton F (1988) Reproduction and dispersal in the ant Cataglyphis cursor (Hymenoptera, Formicidae). Psyche 95:21–44

    Article  Google Scholar 

  • Light SF (1944) Parthenogenesis in termites of the genus Zootermopsis. Univ Calif Publ Zool 43:405–412

    Google Scholar 

  • Matsuura K (2002) A test of the haplodiploid analogy hypothesis in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 95:646–649

    Article  Google Scholar 

  • 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 51:325–332

    Article  Google Scholar 

  • Matsuura K, Fujimoto M, Goka K, Nishida T (2002) Cooperative colony foundation by termite female pairs: altruism for survivorship in incipient colonies. Anim Behav 64:167–173

    Article  Google Scholar 

  • 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 42:241–246

    Article  Google Scholar 

  • 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 43:119–124

    Article  Google Scholar 

  • 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.0000813

    Article  PubMed  Google Scholar 

  • Matsuura K, Tanaka C, Nishida T (2000) Symbiosis of a termite and a sclerotium-forming fungus: sclerotia mimic termite eggs. Ecol Res 15:405–414

    Article  Google Scholar 

  • Matsuura K, Vargo EL, Kawatsu K, et al (2009) Queen succession through asexual reproduction in termites. Science 323:1687–1687

    Google Scholar 

  • Modig AO (1996) Effects of body size and harem size on male reproductive behaviour in the southern elephant seal. Anim Behav 51:1295–1306

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    Article  PubMed  CAS  Google Scholar 

  • Nur U (1971) Parthenogenesis in Coccids (Homoptera). Am Zool 11:301–308

    Google Scholar 

  • Ohkawara K, Nakayama M, Satoh A, et al (2006) Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi. Biol Lett 2:359–363

    Article  PubMed  Google Scholar 

  • Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends Ecol Evol 22:408–413

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pearcy M, Goodisman M, Keller L (2010) Sib-mating without inbreeding in the crazy ant. Proceedings of the 16th Congress of IUSSI: 97

    Google Scholar 

  • Pennisi E (2003) Bickering genes shape evolution. Science 301:1837–1839

    Article  PubMed  CAS  Google Scholar 

  • 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.0006781

    Article  PubMed  Google Scholar 

  • Roisin Y (2001) Caste sex ratios, sex linkage, and reproductive strategies in termites. Insect Soc 48:224–230

    Article  Google Scholar 

  • Rosengaus RB, Guldin MR, Traniello JFA (1998) Inhibitory effect of termite fecal pellets on fungal spore germination. J Chem Ecol 24:1697–1706

    Article  CAS  Google Scholar 

  • Roth LM, Willis ER (1956) Parthenogenesis in cockroaches. Ann Entomol Soc Am 49:31–37

    Google Scholar 

  • Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within honeybee colonies. Proc R Soc Lond B Biol 274:67–72

    Article  Google Scholar 

  • Stansly PA, Korman AK (1993) Parthenogenetic development in Velocitermes spp (Isoptera, Nasutitermitidae). Sociobiology 23:13–24

    Google Scholar 

  • Syren RM, Luykx P (1977) Permanent segmental interchange complex in the termite Incisitermes schwarzi. Nature 266:167168

    Article  Google Scholar 

  • Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc Lond B Biol 270:99–103

    Article  Google Scholar 

  • Templeton A (1982) The prophecies of parthenogenesis. In: Dingle H, Hegmann JP (eds) Evolution and genetics of life histories. Springer-Verlag, Berlin, pp 75–102

    Chapter  Google Scholar 

  • Thomas RJ (1987) Factors affecting the distribution and activity of fungi in the nest of Macrotermitinae (Isoptera). Soil Biol Biochem 19:343–349

    Article  Google Scholar 

  • 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 11:149–169

    Article  Google Scholar 

  • Timmermans I, Hefetz A, Fournier D, Aron S (2008) Population genetic structure, worker reproduction and thelytokous parthenogenesis in the desert ant Cataglyphis sabulosa. Heredity 101:490–498

    Article  PubMed  CAS  Google Scholar 

  • 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 23:247–255

    Article  Google Scholar 

  • Tsuji K, Yamauchi K (1995) Production of females by parthenogenesis in the ant Cerapachys biroi. Insect Soc 42:333–336

    Article  Google Scholar 

  • Tucker KW (1958) Automictic parthenogenesis in the honeybee. Genetics 43:299–316

    PubMed  CAS  Google Scholar 

  • Vargo EL, Husseneder C (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu Rev Entomol 54:379–403

    Article  PubMed  CAS  Google Scholar 

  • Verma S, Ruttner F (1983) Cytological analysis of the thelytokous parthenogenesis in the cape honeybee (Apis mellifera capensis Escholts). Apidologie 14:41–57

    Article  Google Scholar 

  • Weesner FM (1956) The biology of colony foundation in Reticulitermes hesperus Banks. Univ Calif Publ Zool 61:253–314

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Laboratory of Insect Ecology, Graduate School of Environmental Science, Okayama University, Okayama, 700-8530, Japan

    Kenji Matsuura

Authors
  1. Kenji Matsuura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenji Matsuura .

Editor information

Editors and Affiliations

  1. School of Biological & Chemical Sciences, Queen Mary University of London, Mile End Rd., London, E1 4NS, United Kingdom

    David Edward Bignell

  2. Behavioural & Evolutionary Ecology, Université Libre de Bruxelles, Av. F.D. Roosevelt 50, Bruxelles, 1050, Belgium

    Yves Roisin

  3. School of Biological Sciences, University of Sydney, Sydney, 2006, New South Wales, Australia

    Nathan Lo

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Netherlands

About this chapter

Cite this chapter

Matsuura, K. (2010). Sexual and Asexual Reproduction in Termites. In: Bignell, D., Roisin, Y., Lo, N. (eds) Biology of Termites: a Modern Synthesis. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3977-4_10

Download citation

Publish with us

Policies and ethics

Search

Navigation