, 96:1393 | Cite as

Diploid males, diploid sperm production, and triploid females in the ant Tapinoma erraticum

  • Laurent Cournault
  • Serge Aron


Under complementary sex determination (CSD), females of Hymenoptera arise from diploid, fertilized eggs and males from haploid, unfertilized eggs. Incidentally, fertilized eggs that inherit two identical alleles at the CSD locus will develop into diploid males. Diploid males are usually unviable or sterile. In a few species, however, they produce diploid sperm and father a triploid female progeny. Diploid males have been reported in a number of social Hymenoptera, but the occurrence of triploid females has hardly ever been documented. Here, we report the presence of triploid females, diploid males, and diploid sperm (produced by diploid males and stored in queen spermathecae) in the ant Tapinoma erraticum. Moreover, we show variations in the frequency of triploids among female castes: Triploid females are more frequent among workers than virgin queens; they are absent among mated, reproductive queens. The frequency of triploid workers also varies between populations and between nests within populations.


Complementary sex determination Diploid males Flow cytometry Formicidae Triploid females 



LC thanks N. Thurin, A. Bernadou, and A. Lenoir for their help in collecting samples. Authors gratefully acknowledge M. Pearcy for his critical reading of the manuscript and fruitful suggestions. We thank three anonymous referees for their helpful remarks on a previous version of the manuscript. Financial support was provided by the Belgian “Fonds pour la Formation à la Recherche dans l’Industrie et l’Agriculture” (research fellowship to LC), the Belgian National Fund for Scientific Research through personal (research director) and grants (to SA).


  1. Adams J, Rothman ED, Kerr WE, Paulino ZL (1977) Estimation of the number of sex alleles and queen matings from diploid male frequencies in a population of Apis mellifera. Genetics 86:538–596Google Scholar
  2. Araújo DE, Cavalli-Molina S (2001) Genetic variability and social structure of colonies in Acromyrmex heyeri and A. striatus (Hymenoptera: Formicidae). Braz J Biol 61:667–678CrossRefGoogle Scholar
  3. Aron S, de Menten L, Van Bockstaele D (2003) Brood sex determination by flow cytometry in ants. Mol Ecol Notes 3:471–475CrossRefGoogle Scholar
  4. Aron S, de Menten L, Van Bockstaele R, Blank SM, Roisin Y (2005) When hymenopteran males reinvented diploidy. Curr Biol 15:824–827CrossRefPubMedGoogle Scholar
  5. Ayabe T, Hoshiba H, Ono M (2004) Cytological evidence for triploid males and females in the bumblebee, Bombus terrestris. Chrom Res 12:215–223CrossRefPubMedGoogle Scholar
  6. Beukeboom LW (1995) Sex determination in Hymenoptera: a need for genetic and molecular studies. BioEssays 17:813–817CrossRefPubMedGoogle Scholar
  7. Boek G (2001) Current status of flow cytometry in cell and molecular biology. Int Rev Cytol 204:239–298CrossRefGoogle Scholar
  8. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton 529Google Scholar
  9. Buschinger A, Fischer K (1991) Hybridization of chromosome-polymorphic populations of the inquiline ant, Doronomyrmex kutteri (Hym., Formicidae). Insect Soc 38:95–103CrossRefGoogle Scholar
  10. Cook JM (1993) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71:421–435CrossRefGoogle Scholar
  11. Cook JM, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends Ecol Evol 10:281–286CrossRefGoogle Scholar
  12. Cournault L, Aron S (2008) Rapid determination of sperm number in ant queens by flow cytometry. Insect Soc 55:283–287CrossRefGoogle Scholar
  13. Cowan DP, Stahlhut JK (2004) Functionally reproductive diploid and haploid males in an inbreeding hymenopteran with complementary sex determination. Proc Natl Acad Sci 101:10374–10379CrossRefPubMedGoogle Scholar
  14. Crozier RH (1971) Heterozygosity and sex determination in haplo-diploidy. Am Nat 105:399–412CrossRefGoogle Scholar
  15. Crozier RH, Pamilo PP (1996) Evolution of social insect colonies—sex allocation and kin selection. Oxford University Press, New YorkGoogle Scholar
  16. de Boer JG, Ode PJ, Vet LEM, Whitfield J, Heimpel GE (2007) Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis. Heredity 99:288–294CrossRefPubMedGoogle Scholar
  17. Dobson SL, Tanouye MA (1998) Evidence for a genomic imprinting sex determination mechanism in Nasonia vitripennis (Hymenoptera: Chalcidoidea). Genetics 149:233–242PubMedGoogle Scholar
  18. Fernández-Escudero I, Pamilo P, Seppä P (2002) Biased sperm use by polyandrous queens of the ant Proformica longiseta. Behav Ecol Sociobiol 51:207–213CrossRefGoogle Scholar
  19. Foitzik S, Heinze J (2001) Microgeographic structure and intraspecific parasitism in the ant Leptothorax nylanderi. Ecol Entomol 26:449–456CrossRefGoogle Scholar
  20. Hammond RL, Bourke AFG, Bruford MW (2001) Mating frequency and mating system of the polygynous ant, Leptothorax acervorum. Mol Ecol 10:2719–2728CrossRefPubMedGoogle Scholar
  21. Herbers JM, Grieco S (1994) Population structure of Leptothorax ambiguuus, a facultatively polygynous and polydomous ant species. J Evol Biol 7:581–598CrossRefGoogle Scholar
  22. Hung ACF, Imai HT, Kubota M (1972) The chromosomes of nine ant species (Hymenoptera: Formicidae) from Taiwan, Republic of China. Ann Entomol Soc Am 65:1023–1025Google Scholar
  23. Inaba F (1939) Diploid males and triploid females of the parasitic wasp, Habrobracon pectiophorae Watanabe. Cytologia (Tokyo) 9:517–523Google Scholar
  24. Kerr WE, Nielsen RA (1967) Sex determination in bees (Apinae). J Apicult Res 6:3–9Google Scholar
  25. Krieger MJB, Ross KG, Chang CWY, Keller L (1999) Frequency and origin of triploidy in the fire ant Solenopsis invicta. Heredity 82:142–150CrossRefGoogle Scholar
  26. Kron P, Suda J, Husband BC (2007) Applications of flow cytometry to evolutionary and population biology. Annu Rev Ecol Evol Syst 38:847–876CrossRefGoogle Scholar
  27. Liebert AE, Sumana A, Starks PT (2005) Diploid males and their triploid offspring in the paper wasp Polistes dominulus. Biol Lett 1:200–203CrossRefPubMedGoogle Scholar
  28. Liebert AE, Johnson RN, Switz GT, Starks PT (2004) Triploid females and diploid males: underreported phenomena in Polistes wasps? Insect Soc 51:205–211Google Scholar
  29. Loiselle R, Francoeur A, Fischer K, Buschinger A (1990) Variations and taxonomic significance of the chromosome numbers in the nearctic species of the genus Leptothorax (s.s.)(Formicidae: Hymenoptera). Caryologia 43:321–334Google Scholar
  30. Meudec M (1973) Cycle biologique de Tapinoma erraticum (Formicidae, Dolichoderinae). Ann Soc Entomol Fra 9:381–389Google Scholar
  31. Meudec M (1979) Comportement d’émigration chez la fourmi Tapinoma erraticum (Dolichoderinae); un exemple de regulation sociale. Ph.D. thesis, Univesité F. Rabelais, ToursGoogle Scholar
  32. Naito T, Suzuki H (1991) Sex determination in the sawfly, Athalia rosae ruficornis (Hymenoptera): occurrence of triploid males. J Hered 82:101–104Google Scholar
  33. Pamilo P, Sundström L, Fortelius W, Rosengren R (1994) Diploid males and colony-level selection in Formica ants. Ethol Ecol Evol 6:221–235Google Scholar
  34. Pearson B (1982) The taxonomic status of morphologically anomalous ants of the Lasius niger/Lasius alienus taxon. Insect Soc 29:95–101CrossRefGoogle Scholar
  35. Pearson B (1983) Hybridization between the ant species Lasius niger and Lasius alienus: the genetic evidence. Insect Soc 30:402–411CrossRefGoogle Scholar
  36. Petters RM, Mettus RV (1980) Decreased diploid male viability in the parasitic wasp, Bracon hebetor. J Hered 71:353–356Google Scholar
  37. Ross KG (2001) Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Mol Ecol 10:265–284CrossRefPubMedGoogle Scholar
  38. Ross KG, Fletcher DJC (1985) Genetic origin of male diploidy in the fire ant, Solenopsis invicta (Hymenoptera: Formicidae) and its evolutionary significance. Evolution 39:888–903CrossRefGoogle Scholar
  39. Ross KG, Fletcher DJC (1986) Diploid male production—a significant colony mortality factor in the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Behav Ecol Sociobiol 19:283–291CrossRefGoogle Scholar
  40. Ross KG, Vargo EL, Keller L, Trager JC (1993) Effect of a founder event on variation in the genetic sex-determining system of the fire ant Solenopsis invicta. Genetics 135:843–854PubMedGoogle Scholar
  41. Santomauro G, Oldham NJ, Boland W, Engels W (2004) Cannibalism of diploid drone larvae in the honeybee (Apis mellifera) is released by odd pattern of cuticular substances. J Apicult Res 43:69–74Google Scholar
  42. Schrempf A, Aron S, Heinze J (2006) Sex determination and inbreeding depression in an ant with regular sib-mating. Heredity 97:75–80CrossRefPubMedGoogle Scholar
  43. Smith SG, Wallace DR (1971) Allelic sex determination in a lower hymenopteran, Neodiprion nigroscutum Midd. Canad J Genet Cytol 13:617–621Google Scholar
  44. Takahashi J, Ayabe T, Mitsuhata M, Shimizu I, Ono M (2008) Diploid male production in a rare and locally distributed bumblebee, Bombus florilegus (Hymenoptera, Apidae). Insect Soc 55:43–50CrossRefGoogle Scholar
  45. Van Wilgenburgh E, Driessen G, Beukeboom LW (2006) Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Front Zool 3:1CrossRefGoogle Scholar
  46. Ward PS (1980) Genetic variation and population differentiation in the Rhytidoponera impressa group, a species complex of ponerine ants (Hymenoptera: Formicidae). Evolution 34:1060–1076CrossRefGoogle Scholar
  47. Wedemeyer N, Potter T (2001) Flow cytometry: an ‘old’ tool for novel applications in medical genetics. Clin Genet 60:1–8CrossRefPubMedGoogle Scholar
  48. Whiting PW (1943) Multiple alleles in complementary sex determination of Habrobracon. Genetics 28:365–382PubMedGoogle Scholar
  49. Yamauchi K, Yoshida T, Ogawa T, Itoh S, Ogawa Y, Jimbo S, Imai HT (2001) Spermatogenesis of diploid males in the formicine ant, Lasius sakagamii. Insect Soc 48:28–32CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Behavioral and Evolutionary Ecology, Faculty of SciencesUniversité Libre de BruxellesBrusselsBelgium

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