Journal of Genetics

, Volume 89, Issue 3, pp 333–339 | Cite as

Genetics of sex determination in the haplodiploid wasp Nasonia vitripennis (Hymenoptera: Chalcidoidea)

Review Article


The parasitoid wasp Nasonia vitripennis reproduces by haplodiploidy; males are haploid and females are diploid. Sex determination in Nasonia is not governed by complementary alleles at one or more sex loci. As in most other insects, the sex-determining pathway consists of the basal switch doublesex that is sex-specifically regulated by transformer. Analysis of a polyploid and a mutant gynandromorphic strain, suggested a parent-specific effect (imprinting) on sex determination in Nasonia. Zygotic activity of transformer is autoregulated and depends on a combination of maternal provision of tra mRNA and a paternal genome set. This constitutes a novel way of transformer control in insect sex determination implying maternal imprinting. The nature of the maternal imprint is not yet known and it remains to be determined how broadly the Nasonia sex-determining mechanism applies to other haplodiploids.


sex-specific splicing imprinting doublesex transformer Hymenoptera Nasonia 


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  1. Beukeboom L. W. 1995 Sex determination in Hymenoptera: a need for genetic and molecular studies. BioEssays 17, 813–817.CrossRefPubMedGoogle Scholar
  2. Beukeboom L. W. and Kamping A. 2006 No patrigenes required for femaleness in the haplodiploid wasp Nasonia. Genetics 172, 981–989.CrossRefPubMedGoogle Scholar
  3. Beukeboom L. W., Kamping A. and van de Zande L. 2007a Sex determination in the haplodiploid wasp Nasonia vitripennis (Hymenoptera: Chalcidoidea): a critical consideration of models and evidence. Semin. Cell Dev. Biol. 18, 371–378.CrossRefPubMedGoogle Scholar
  4. Beukeboom L. W., Kamping A., Louter M., Pijnacker L. P., Katju V., Ferree P. M. and Werren J. H. 2007b Haploid females in the parasitic wasp Nasonia vitripennis. Science 315, 206.CrossRefPubMedGoogle Scholar
  5. Beye M. M., Hasselmann M., Fondrk M. K., Page R. E. and Omholt S.W. 2003 The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114, 419–429.CrossRefPubMedGoogle Scholar
  6. Cline T. W. and Meyer B. J. 1996 Vive la différence: males vs. females in flies vs. worms. Annu. Rev. Genet. 30, 637–702.CrossRefPubMedGoogle Scholar
  7. Concha C. and Scott M. J. 2009 Sexual development in Lucilia cuprina (Diptera, Calliphoridae) is controlled by the transformer gene. Genetics 182, 785–798.CrossRefPubMedGoogle Scholar
  8. Cook J. M. 1993 Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71, 421–435.CrossRefGoogle Scholar
  9. de Boer J. G., Ode P. J., Rendahl A. K., Vet L. E. M., Whitfield J. B. and Heimpel G. E. 2008 Experimental support for multiplelocus complementary sex determination in the parasitoid Cotesia vestalis. Genetics 180, 1525–1535.CrossRefPubMedGoogle Scholar
  10. Dobson S. and Tanouye M. 1998 Evidence for a genomic imprinting sex determination mechanism in Nasonia vitripennis (Hymenoptera; Chalcidoidea). Genetics 149, 233–242.PubMedGoogle Scholar
  11. Gempe T., Hasselmann M., Schiøtt M., Hause G., Otte M. and Beye M. 2009 Sex determination in honeybees: two separate mechanisms induce and maintain the female pathway. PLoS Biol. 7, e1000222.CrossRefPubMedGoogle Scholar
  12. Hasselmann M., Gempe T., Schiøtt M., Nunes-Silva C. G., Otte M. and Beye M. 2008 Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454, 519–522.CrossRefPubMedGoogle Scholar
  13. Hediger M., Henggeler C., Meier N., Perez R., Saccone G. and Bopp D. 2010 Molecular characterization of the key switch F provides a basis for understanding the rapid divergence of the sex-determining pathway in the housefly. Genetics 184, 1–16.CrossRefGoogle Scholar
  14. Heimpel G. E. and de Boer J. G. 2008 Sex determination in the Hymenoptera. Annu. Rev. Entomol. 53, 209–230.CrossRefPubMedGoogle Scholar
  15. Kamping A., Katju V., Beukeboom L. W. and Werren J. H. 2007 Inheritance of gynandromorphism in the parasitic wasp Nasonia vitripennis. Genetics 175, 1321–1333.CrossRefPubMedGoogle Scholar
  16. Lagos D., Koukidou M., Savakis C. and Komitopoulou K. 2007 The transformer gene in Bactrocera oleae: the genetic switch that determines its sex fate. Insect Mol. Biol. 16, 221–230.CrossRefPubMedGoogle Scholar
  17. Nöthiger R. and Steinmann-Zwicky M. 1985 A single principle for sex determination in insects. Cold Spring Harbor Symp. Quant. Genet. 50, 615–621.Google Scholar
  18. Oliveira D. C. S. G., Werren J. H., Verhulst E. C., Giebel J. D., Kamping A., Beukeboom L. W. and van de Zande L. 2009 Identification and characterization of the doublesex gene of Nasonia. Insect Mol. Biol. 18, 315–323.CrossRefPubMedGoogle Scholar
  19. Pane A., Salvemini M., Delli Bovi P., Polito C. and Saccone G. 2002 The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129, 3715–3725.PubMedGoogle Scholar
  20. Pane A., De Simone A., Saccone G. and Polito C. 2005 Evolutionary conservation of Ceratitis capitata transformer gene function. Genetics 171, 615–624.CrossRefPubMedGoogle Scholar
  21. Poirié M., Périquet G. and Beukeboom L. 1992 The hymenopteran way of determining sex. Semin. Dev. Biol. 3, 357–361.CrossRefGoogle Scholar
  22. Saccone G., Pane A. and Polito L. C. 2002 Sex determination in flies, fruitflies and butterflies. Genetica 116, 15–23.CrossRefPubMedGoogle Scholar
  23. Sánchez L. 2008 Sex-determining mechanisms in insects. Int. J. Dev. Biol. 52, 837–856.CrossRefPubMedGoogle Scholar
  24. Stenberg P. and Saura A. 2009 Cytology of asexual animals. In Lost sex: the evolutionary biology of parthenogenesis (ed. I. Schön, K. Martens and P. van Dijk), pp. 63–74. Springer, New York, USA.CrossRefGoogle Scholar
  25. The Honeybee Genome Sequencing Consortium 2006 Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931–949.CrossRefGoogle Scholar
  26. Trent C., Crosby C. and Eavey J. 2006 Additional evidence for the genomic imprinting model of sex determination in the haplodiploid wasp Nasonia vitripennis: isolation of biparental diploid male after X-ray mutagenesis. Heredity 96, 368–376.CrossRefPubMedGoogle Scholar
  27. Van Wilgenburg E., Driessen G. and Beukeboom L. W. 2006 Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Front. Zool. 3, 1.CrossRefPubMedGoogle Scholar
  28. Verhulst E. C., Beukeboom L. W. and Van de Zande L. 2010a Maternal control of haplodiploid sex determination in Nasonia. Science 328, 620–623.CrossRefPubMedGoogle Scholar
  29. Verhulst E. C., Van de Zande L. and Beukeboom L.W. 2010b Insect sex determination: it all evolves around transformer. Curr. Opin. Genetics Dev. 20, 376–383.CrossRefGoogle Scholar
  30. Werren J. H. et al. 2010 Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327, 343–348.CrossRefPubMedGoogle Scholar
  31. Whiting A. R. 1967 The biology of the parasitic wasp Mormoniella vitripennis (=Nasonia brevicornis) (Walker). Quart. Rev. Biol. 42, 333–406.CrossRefGoogle Scholar
  32. Wilkins A. S. 1995 Moving up the hierarchy. A hypothesis on the evolution of a genetic sex determination pathway. BioEssays 17, 71–77.CrossRefPubMedGoogle Scholar
  33. Whiting P. W. 1933 Selective fertilization and sex determination in Hymenoptera. Science 78, 537–538.CrossRefPubMedGoogle Scholar
  34. Whiting P. W. 1960 Polyploidy in Mormoniella. Genetics 45, 949–970.PubMedGoogle Scholar

Copyright information

© Indian Academy of Sciences 2010

Authors and Affiliations

  1. 1.Evolutionary Genetics, Center for Ecological and Evolutionary StudiesUniversity of GroningenGroningenThe Netherlands

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