Skip to main content
SpringerLink
Log in

Use of a regulatory mechanism of sex determination in pest insect control

  • Review Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

The sexual development of an insect is defined through a hierarchical control of several sex determining genes. Of these genes, transformer (tra) and doublesex (dsx) are well characterized and functionally conserved, especially dsx. Both genes are regulated at the transcriptional level through sex-specific alternative splicing. Incorporation of a genetically engineered sexspecific splicing module derived from these genes in transgenic systems, such as RIDL (release of insects carrying a dominant lethal), would allow the production of male-only insects for control programmes without any physical intervention.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abe H., Fuji T., Tanaka N., Yokoyama T., Kakehashi H., Ajimura M. et al. 2008 Identification of the female-determining region of the W chromosome in Bombyx mori. Genetica 133, 269–282.

    Article  CAS  PubMed  Google Scholar 

  • Alphey L. and Andreasen M. H. 2002 Dominant lethality and insect population control. Mol. Biochem. Parasitol. 121, 173–178.

    Article  CAS  PubMed  Google Scholar 

  • Alphey L., Beard B., Billingsley P., Coetzee M., Crisanti A., Curtis C. F. et al. 2002 Malaria control with genetically modified vectors. Science 298, 119–121.

    Article  CAS  PubMed  Google Scholar 

  • Alphey L., Benedict M. Q., Bellini R., Clark G. G., Dame D., Service M. and Dobson S. 2010 Sterile-insect methods for control of mosquito-borne diseases—an analysis. Vector Borne Zoonotic Dis. 10, 295–311.

    Article  PubMed  Google Scholar 

  • Alphey L., Nimmo D., O’Connell S. and Alphey N. 2008 Insect population suppression using engineered insects. In Transgenesis and the management of vector-borne disease (ed. S. Aksoy), pp. 93–103. Landes Bioscience, Austin, USA.

    Chapter  Google Scholar 

  • Baker B. S. and Ridge K. A. 1980 Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94, 383–423.

    CAS  PubMed  Google Scholar 

  • Baker B. S. and Wolfner M. F. 1988 A molecular analysis of doublesex, a bifunctional gene that controls both male and female sexual differentiation in Drosophila melanogaster. Genes Dev. 2, 477–489.

    Article  CAS  PubMed  Google Scholar 

  • Beye M., Hasselmann M., Fondrk M., Page R. and Omholt S. 2003 The gene cds is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114, 419–429.

    Article  CAS  PubMed  Google Scholar 

  • Burtis K. C. and Baker B. S. 1989 Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56, 997–1010.

    Article  CAS  PubMed  Google Scholar 

  • Concha C. and Scott M. J. 2009 Sexual development in Lucilia cuprina (Diptera, Calliphoridae) is controlled by the transformer gene. Genetics 182, 785–798.

    Article  CAS  PubMed  Google Scholar 

  • Cook J. 1993 Sex determination in the Hymenoptera- a review of models and evidence. Heredity 81, 1–9.

    Google Scholar 

  • Dyck V. A., Hendrichs J. and Robinson A. S. (ed.) 2005 Sterile insect technique: principles and practice in area-wide integrated pest management. Springer, Dordrecht, The Netherlands.

    Google Scholar 

  • Dübendorfer A., Hediger M., Burghardt G. and Bopp D. 2002 Musca domestica, a window on the evolution of sex-determining mechanisms in insects. Int. J. Dev. Biol. 46, 75–79.

    PubMed  Google Scholar 

  • Erickson J. W. and Quintero J. J. 2007 Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. PLoS Biol. 5, 2821–2829.

    Article  CAS  Google Scholar 

  • Fu G., Condon K. C., Epton M. J., Gong P., Jin L., Condon G. C. et al. 2007 Female-specific insect lethality engineered using alternative splicing. Nat. Biotechnol. 25, 353–357.

    Article  CAS  PubMed  Google Scholar 

  • Fu G., Lees R., Nimmo D., Aw D., Jin L., Gray P. et al. 2010 Female-specific flightless phenotype for mosquito control. Proc. Natl. Acad. Sci. USA 107, 4550–4554.

    Article  CAS  PubMed  Google Scholar 

  • Funaguma S., Suzuki M. G., Tamura T. and Shimada T. 2005 The Bmdsx transgene including trimmed introns in sex-specifically spliced in tissues of the silkworm, Bombyx mori. J. Insect Sci. 5, 1–6.

    Google Scholar 

  • Gong P., Epton M. J., Fu G., Scaife S., Hiscox A., Condon K. C. et al. 2005 A dominant lethal genetic system for autocidal control of the Mediterranean fruitfly. Nat. Biotechnol. 23, 453–456.

    Article  CAS  PubMed  Google Scholar 

  • Hediger M., Burghardt G., Siegenthaler C., Buser N., Hilfiker-Kleiner D., Dubendorfer A. and Bopp D. 2004 Sex determination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev. Genes. Evol. 214, 29–42.

    Article  CAS  PubMed  Google Scholar 

  • 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, 155–170.

    Article  PubMed  Google Scholar 

  • Heinrich J. C. and Scott M. J. 2000 A repressible female-specific lethal genetic system for making transgenic insect strains suitable for a sterile-release program. Proc. Natl. Acad. Sci. USA 97, 8229–8232.

    Article  CAS  PubMed  Google Scholar 

  • Hendrichs J., Franz G. and Rendon P. 1995 Increased effectiveness and applicability of the sterile insect technique through maleonly release for control of Mediterranean fruit-flies during fruiting seasons. J. Appl. Entomol. 119, 371–377.

    Article  Google Scholar 

  • Koukidou M., Morgan S., Stainton K. C., Fu G., Dafa’alla T. H., Phillips C. E. and Alphey L. 2008: Female lethal RIDL strains of the Mediterranean fruit fly Ceratitis capitata and the Mexican fruit fly Anastrepha ludens. In Proceedings of the 7th Meeting of the Working Group on Fruit Flies of the Western Hemisphere (ed. P. J. M. Gerardo, F. D. Fleischer and S. F. Breceda), pp. 116–117. Mazatlán, USA.

  • Koyama J., Kakinohana H. and Miyatake T. 2004 Eradication of the melon fly, Bactrocera cucurbitae, in Japan: importance of behaviour, ecology, genetics, and evolution. Annu. Rev. Entomol. 49, 331–349.

    Article  CAS  PubMed  Google Scholar 

  • Kuhn S., Sievert V. and Traut W. 2000 The sex-determining gene doublesex in the fly Megaselia scalaris: conserved structure and sex-specific splicing. Genome 43, 1011–1020.

    Article  CAS  PubMed  Google Scholar 

  • Lagos D., Ruiz M. F., Sanchez L. and Komitopoulou K. 2005 Isolation and characterization of the Bactrocera oleae genes orthologous to the sex determining Sex-lethal and doublesex genes of Drosophila melanogaster. Gene 348, 111–121.

    Article  CAS  PubMed  Google Scholar 

  • Lagos D., Koukiduo M., Savakis C. and Komitopoulou K. 2007 The transformer gene in Bacterocera oleae, the genetic switch that determines its sex fate. Insect Mol. Biol. 16, 221–230.

    Article  CAS  PubMed  Google Scholar 

  • Lindquist D. A., Abusowa M. and Hall M. J. 1992 The New World screwworm fly in Libya: a review of its introduction and eradication. Med. Vet. Entomol. 6, 2–8.

    Article  CAS  PubMed  Google Scholar 

  • Masataka O. F., Suzuki M. G. and Shimada T. 2002 Sex determination in Bombyx mori. Curr. Sci. 83, 466–471.

    Google Scholar 

  • McAllister B. M. and McVean G. A. T. 2000 Neutral evolution of the sex-determining gene transformer in Drosophila. Genetics 154, 1711–1720.

    CAS  PubMed  Google Scholar 

  • Meise M., Hilfiker-Kleiner D., Dübendorfer A., Brunner C., Nöthinger R. and Bopp D. 1998 Sex-lethal, the master sex-determining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development 125, 1487–1494.

    CAS  PubMed  Google Scholar 

  • Niimi T., Sahara K., Oshima H., Yasukochi Y., Ikei K. and Traut W. 2006 Molecular cloning and chromosomal localization of the Bombyx sex-lethal gene. Genome 49, 263–268.

    Article  CAS  PubMed  Google Scholar 

  • Ohbayashi F., Suzuki M. G., Mita K., Okano K. and Shimada T. 2001 A homologue of the Drosophila doublesex gene is transcribed into sex-specific mRNA isoforms in the silkworm, Bombyx mori. Comp. Biochem. Physiol. 128, 145–158.

    Article  CAS  Google Scholar 

  • Oliveira D. C., 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, 315–324.

    Article  CAS  PubMed  Google Scholar 

  • O’Neil M. T. and Belote J. M. 1992 Interspecific comparison of the transformer gene of Drosophila reveals an unusually high degree of evolutionary divergence. Genetics 131, 113–128.

    PubMed  Google Scholar 

  • Pane A., Salvemini M., Delli Vovi 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.

    CAS  PubMed  Google Scholar 

  • Pane A., De Simone A., Saccone G. and Polito D. 2005 Evolutionary conservation of Ceratitis capitata transformer gene function. Genetics 171, 615–624.

    Article  CAS  PubMed  Google Scholar 

  • Phuc H. K., Andreasen M. H., Burton R. S., Vass C., Epton M. J., Pape G. et al. 2007 Late-acting dominant lethal genetic systems and mosquito control. BMC Biol. 5, 1–11.

    Article  Google Scholar 

  • Rendón P., McInnis D., Lance D. and Stewart J. 2004 Medfly (Diptera: Tephritidae) genetic sexing: large-scale field comparison of males-only and bisexual sterile insect release. J. Econ. Entomol. 97, 1547–1553.

    Article  PubMed  Google Scholar 

  • Ruiz M. F., Milano A., Salvemini M., Eirin-López J. M., Perondini A. L. P., Selivon D. et al. 2007 The gene transformer of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. PLoS ONE 11, e1239.

    Article  Google Scholar 

  • Saccone G., Peluso I., Artiaco D., Giordano E., Bopp D. and Polito L. C. 1998 The Ceratitis capitata homologue of the Drosophila sex-determining gene Sex-lethal is structurally conserved, but not sex-specifically regulated. Development 125, 1495–1500.

    CAS  PubMed  Google Scholar 

  • Saccone G., Salvemini M., Pane A. and Polito L. C. 2008 Masculinization of XX Drosophila transgenic flies expressing the Ceratitis capitata DoublesexM isoform. Int. J. Dev. Biol. 52, 1051–1057.

    Article  CAS  PubMed  Google Scholar 

  • Salvemini M., Robertson M., Aronson B., Atkinson P., Polito L. C. and Saccone G. 2009 Ceratitis capitata transformer-2 gene is required to establish and maintain the autoregulation of Cctra, the master gene for femal sex determination. Int. J. Dev. Biol. 53, 109–120.

    Article  CAS  PubMed  Google Scholar 

  • Scali C., Catteruccia F., Li Z. and Crisanti A. 2005 Identification of sex-specific transcripts of Anopheles gambiae doublesex gene. J. Exp. Biol. 208, 3701–3709.

    Article  CAS  PubMed  Google Scholar 

  • Sciabica K. S. and Hertel K. J. 2006 The splicing regulators Tra and Tra2 are unusually potent activators of pre-mRNA splicing. Nucleic Acids Res. 34, 6612–6620.

    Article  CAS  PubMed  Google Scholar 

  • Shearman D. C. and Frommer M. 1998 The Bactrocera tryoni homologue of the Drosophila melanogaster sex-determination gene doublesex. Insect Mol. Biol. 7, 355–366.

    Article  CAS  PubMed  Google Scholar 

  • Shukla J. N. and Nagaraju J. 2010 Two female-specific DSX proteins are encoded by the sex-specific transcripts of dsx, and are required for female sexual differentiation in two wild silkmoth species, Antheraea assama and Antheraea mylitta (Lepidoptera, Saturniidae). Insect Biochem. Mol. Biol. (doi: 10.1016/j.ibmb.2010.06.008).

  • Sosnowski B., Belote J. M. and Mckeown M. 1989 Sex-specific alternative splicing of RNA from the transformer gene results from sequence dependent splice site blockage. Cell 58, 449–459.

    Article  CAS  PubMed  Google Scholar 

  • Thomas D. D., Donnelly C. A., Wood R. J. and Alphey L. S. 2000 Insect population control using a dominant, repressible, lethal genetic system. Science 287, 2474–2476.

    Article  CAS  PubMed  Google Scholar 

  • Traut W., Niimi T., Ikeo K. and Sahara K. 2006 Phylogeny of the sex-determining gene Sex-lethal in insects. Genome 49, 254–262.

    Article  CAS  PubMed  Google Scholar 

  • Verhulst E. C., Beukeboom L. W. and van de Zande L. 2010 Maternal control of haplodiploid sex determination in the wasp Nasonia. Science 328, 620–623.

    Article  CAS  PubMed  Google Scholar 

  • Weber W. and Fussenegger M. 2009 Engineering of synthetic mammalian gene networks. Chem. Biol. 16, 287–297.

    Article  CAS  PubMed  Google Scholar 

  • Wilkins A. S. 1995 Moving up the hierarchy: a hypothesis on the evolution of genetic sex determination pathway. BioEssays 17, 71–77.

    Article  CAS  PubMed  Google Scholar 

  • Willhoeft U. and Franz G. 1996 Identification of the sex determining region of the Ceratitis capitata Y chromosome by deletion mapping. Genetics 144, 737–745.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Oxitec Limited, 71 Milton Park, Oxford, OX14 4RX, UK

    Tarig Dafa’alla, Guoliang Fu & Luke Alphey

  2. Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK

    Guoliang Fu & Luke Alphey

Authors
  1. Tarig Dafa’alla
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guoliang Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luke Alphey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luke Alphey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dafa’alla, T., Fu, G. & Alphey, L. Use of a regulatory mechanism of sex determination in pest insect control. J Genet 89, 301–305 (2010). https://doi.org/10.1007/s12041-010-0041-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-010-0041-y

Keywords

Search

Navigation