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The transformer gene of Ceratitis capitata: a paradigm for a conserved epigenetic master regulator of sex determination in insects

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Abstract

The transformer gene in Ceratitis capitata (Cctra ep ) is the founding member of a family of related SR genes that appear to act as the master epigenetic switch in sex determination in insects. A functional protein seems to be produced only in individuals with a female XX karyotype where it is required to maintain the productive mode of expression through a positive feedback loop and to direct female development by instructing the downstream target genes accordingly. When zygotic activation of this loop is prevented, male development follows. Recently, tra ep orthologues were isolated in more distantly related dipteran species including Musca domestica, Glossina morsitans and Lucilia cuprina and in the Hymenopterans Apis mellifera and Nasonia vitripennis. All of these tra ep orthologues seem to act as binary switches that govern all aspects of sexual development. Transient silencing leads to complete masculinization of individuals with a female karyotype. Reciprocally, in some systems it has been shown that transient expression of the functional TRA product is sufficient to transactivate the endogenous gene and implement female development in individuals with a male karyotype. Hence, a mechanism based on tra ep epigenetic autoregulation seems to represent a common and presumably ancestral single principle of sex determination in Insecta. The results of these studies will not only be important for understanding divergent evolution of basic developmental processes but also for designing new strategies to improve genetic sexing in different insect species of economical or medical importance.

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References

  • Amrein H, Gorman M, Nothiger R (1988) The sex-determining gene tra-2 of Drosophila encodes a putative RNA binding protein. Cell 55(6):1025–1035

    Article  CAS  PubMed  Google Scholar 

  • Baker SB, Burtis K, Goralski T, Mattox W, Nagoshi R (1989) Molecular genetic aspects of sex determination in Drosophila melanogaster. Genome 31(2):638–645

    CAS  PubMed  Google Scholar 

  • Baker SB, Hoff G, Kaufman CT, Wolfner FM, Hazelrigg T (1991) The doublesex locus of Drosophila melanogaster and its flanking regions: a cytogenetic analysis. Genetics 127(1):125–138

    CAS  PubMed  Google Scholar 

  • Bell EA (1954) A gene in Drosophila melanogaster that produces all male progeny. Genetics 39:958–959

    Google Scholar 

  • Bell RL, Horabin IJ, Schedl P, Cline WT (1991) Positive autoregulation of sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell 65(2):229–239

    Article  CAS  PubMed  Google Scholar 

  • Belote MJ (1989) The control of sexual development in Drosophila melanogaster: genetic and molecular analysis of a genetic regulatory hierarchy—a minireview. Gene 82(1):161–167

    Article  CAS  PubMed  Google Scholar 

  • Bertossa CR, van de Zande L, Beukeboom WL (2009) The fruitless gene in Nasonia displays complex sex-specific splicing and contains new zinc finger domains. Mol Biol Evol 26(7):1557–1569

    Article  CAS  PubMed  Google Scholar 

  • Beukeboom LW, van de Zande L (2010) Genetics of sex determination in the haplodiploid wasp Nasonia vitripennis (Hymenoptera: Chalcidoidea). J Genet 89:333–339

    Article  PubMed  Google Scholar 

  • Beye M, Hasselmann M, Fondrk KM, Page ER, Omholt WS (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114(4):419–429

    Article  CAS  PubMed  Google Scholar 

  • Billeter JC, Rideout EJ, Dornan AJ, Goodwin SF (2006) Control of male sexual behavior in Drosophila by the sex determination pathway. Curr Biol 16(17):R766–R776

    Article  CAS  PubMed  Google Scholar 

  • Boggs TR, Gregor P, Idriss S, Belote MJ, McKeown M (1987) Regulation of sexual differentiation in D. melanogaster via alternative splicing of RNA from the transformer gene. Cell 50(5):739–747

    Article  CAS  PubMed  Google Scholar 

  • Bopp D (2010) About females and males: continuity and discontinuity in flies. J Genet 89:315–323

    Article  PubMed  Google Scholar 

  • Bopp D, Calhoun G, Horabin IJ, Samuels M, Schedl P (1996) Sex-specific control of Sex-lethal is a conserved mechanism for sex determination in the genus Drosophila. Development 122(3):971–982

    CAS  PubMed  Google Scholar 

  • Bridges BC (1916) Non-disjunction as proof of the chromosome theory of heredity (concluded). Genetics 1(2):107–163

    CAS  PubMed  Google Scholar 

  • Bridges BC (1921) Triploid intersexes in Drosophila melanogaster. Science 54(1394):252–254

    Article  CAS  PubMed  Google Scholar 

  • Bridges BC, Anderson GE (1925) Crossing over in the X chromosomes of triploid females of Drosophila melanogaster. Genetics 10(5):418–441

    CAS  PubMed  Google Scholar 

  • Burghardt G, Hediger M, Siegenthaler C, Moser M, Dübendorfer A, Bopp D (2005) The transformer2 gene in Musca domestica is required for selecting and maintaining the female pathway of development. Dev Genes Evol 215(4):165–176

    Article  CAS  PubMed  Google Scholar 

  • Burtis CK, Baker SB (1989) Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56(6):997–1010

    Article  CAS  PubMed  Google Scholar 

  • Chandler D, McGuffin ME, Piskur J, Yao J, Baker BS, Mattox W (1997) Evolutionary conservation of regulatory strategies for the sex determination factor transformer-2. Mol Cell Biol 17(5):2908–2919

    CAS  PubMed  Google Scholar 

  • Cline WT (1978) Two closely linked mutations in Drosophila melanogaster that are lethal to opposite sexes and interact with daughterless. Genetics 90(4):683–698

    CAS  PubMed  Google Scholar 

  • Cline WT (1980) Maternal and zygotic sex-specific gene interactions in Drosophila melanogaster. Genetics 96(4):903–926

    CAS  PubMed  Google Scholar 

  • Cline WT, Meyer JB (1996) Vive la difference: Males vs females in flies vs worms. Annu Rev Genet 30:637–702

    Article  CAS  PubMed  Google Scholar 

  • Concha C, Scott JM (2009) Sexual development in Lucilia cuprina (Diptera, Calliphoridae) is controlled by the transformer gene. Genetics 182(3):785–798

    Article  CAS  PubMed  Google Scholar 

  • Dafa’alla T, Fu G, Alphey L (2010) Use of a regulatory mechanism of sex determination in pest insect control. J Genet 89:301–305

    Article  PubMed  Google Scholar 

  • Demir E, Dickson JB (2005) Fruitless splicing specifies male courtship behavior in Drosophila. Cell 121(5):785–794

    Article  CAS  PubMed  Google Scholar 

  • Dubendorfer A, Hediger M (1998) The female-determining gene f of the housefly, Musca domestica, acts maternally to regulate its own zygotic activity. Genetics 150(1):221–226

    CAS  PubMed  Google Scholar 

  • Erickson WJ, Quintero JJ (2007) Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. PLoS Biol 5(12):e332

    Article  PubMed  Google Scholar 

  • Estes AP, Keyes NL, Schedl P (1995) Multiple response elements in the Sex-lethal early promoter ensure its female-specific expression pattern. Mol Cell Biol 15(2):904–917

    CAS  PubMed  Google Scholar 

  • Fu G, Condon CK, Epton JM, Gong P, Jin L, Condon CG, Morrison IN, Dafa’alla HT, Alphey L (2007) Female-specific insect lethality engineered using alternative splicing. Nat Biotechnol 25(3):353–357

    Article  CAS  PubMed  Google Scholar 

  • Gabrieli P, Falaguerra A, Siciliano P, Gomulski ML, Scolari F, Zacharopoulou A, Franz G, Malacrida RA, Gasperi G (2010) Sex and the single embryo: early development in the mediterranean fruit fly, Ceratitis capitata. BMC Dev Biol 10(1):12

    Article  PubMed  Google Scholar 

  • Gailey AD, Taylor JB, Hall CJ (1991) Elements of the fruitless locus regulate development of the muscle of Lawrence, a male-specific structure in the abdomen of Drosophila melanogaster adults. Development 113(3):879–890

    CAS  PubMed  Google Scholar 

  • Gailey DA, Billeter JC, Liu JH, Bauzon F, Allendorfer JB, Goodwin SF (2006) Functional conservation of the fruitless male sex-determination gene across 250 Myr of insect evolution. Mol Biol Evol 23(3):633–643

    Article  CAS  PubMed  Google Scholar 

  • Gempe T, Hasselmann M, Schiott M, Hause G, Otte M, Beye M (2009) Sex determination in honeybees: two separate mechanisms induce and maintain the female pathway. PLoS Biol 7(10):e1000222

    Article  PubMed  Google Scholar 

  • Graham P, Penn JK, Schedl P (2003) Masters change, slaves remain. Bioessays 25(1):1–4

    Article  PubMed  Google Scholar 

  • Granadino B, Juan AS, Santamaria P, Sanchez L (1992) Evidence of a dual function in fl(2)d, a gene needed for Sex-lethal expression in Drosophila melanogaster. Genetics 130(3):597–612

    CAS  PubMed  Google Scholar 

  • Hasselmann M, Gempe T, Schiott M, Nunes-Silva GC, Otte M, Beye M (2008) Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454(7203):519–522

    Article  CAS  PubMed  Google Scholar 

  • Hediger M, Burghardt G, Siegenthaler C, Buser N, Hilfiker-Kleiner D, Dubendorfer A, Bopp D (2004) Sex determination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev Genes Evol 214(1):29–42

    Article  CAS  PubMed  Google Scholar 

  • Hediger M, Henggeler C, Meier N, Perez R, Saccone G, 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):155–170

    Article  CAS  PubMed  Google Scholar 

  • Hedley LM, Maniatis T (1991) Sex-specific splicing and polyadenylation of dsx pre-mRNA requires a sequence that binds specifically to tra-2 protein in vitro. Cell 65(4):579–586

    Article  CAS  PubMed  Google Scholar 

  • Henricson A, Forslund K, Sonnhammer LE (2010) Orthology confers intron position conservation. Bmc Genomics 11:412. doi:1471-2164-11-412

    Article  PubMed  Google Scholar 

  • Hertel JK, Lynch WK, Hsiao CE, Liu HE, Maniatis T (1996) Structural and functional conservation of the Drosophila doublesex splicing enhancer repeat elements. RNA 2(10):969–981

    CAS  PubMed  Google Scholar 

  • Hildreth EP (1965) Doublesex, recessive gene that transforms both males and females of Drosophila into intersexes. Genetics 51:659–678

    CAS  PubMed  Google Scholar 

  • Hildreth EP, Lucchesi CJ (1963) Fertilization in Drosophila. I. Evidence for the regular occurrence of monospermy. Dev Biol 6:262–278

    Article  CAS  PubMed  Google Scholar 

  • Hilfiker A, Amrein H, Dübendorfer A, Schneiter R, Nöthiger R (1995) The gene virilizer is required for female-specific splicing controlled by Sxl, the master gene for sexual development in Drosophila. Development 121(12):4017–4026

    CAS  PubMed  Google Scholar 

  • Hoshijima K, Inoue K, Higuchi I, Sakamoto H, Shimura Y (1991) Control of doublesex alternative splicing by transformer and transformer-2 in Drosophila. Science 252(5007):833–836

    Article  CAS  PubMed  Google Scholar 

  • Inoue K, Hoshijima K, Higuchi I, Sakamoto H, Shimura Y (1992) Binding of the Drosophila transformer and transformer-2 proteins to the regulatory elements of doublesex primary transcript for sex-specific RNA processing. Proc Natl Acad Sci U S A 89(17):8092–8096

    Article  CAS  PubMed  Google Scholar 

  • Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D (1996) Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a btb domain. Proc Natl Acad Sci U S A 93(18):9687–9692

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Kobayashi K, Oda S, Tatarazako N, Watanabe H, Iguchi T (2010) Sequence divergence and expression of a transformer gene in the branchiopod crustacean, Daphnia magna. Genomics 95(3):160–165

    Article  CAS  PubMed  Google Scholar 

  • Kuhn S, Sievert V, Traut W (2000) The sex-determining gene doublesex in the fly Megaselia scalaris: conserved structure and sex-specific splicing. Genome 43(6):1011–1020

    Article  CAS  PubMed  Google Scholar 

  • Lagos D, Ruiz FM, Sanchez L, 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, Koukidou M, Savakis C, Komitopoulou K (2007) The transformer gene in Bactrocera oleae: the genetic switch that determines its sex fate. Insect Mol Biol 16(2):221–230

    Article  CAS  PubMed  Google Scholar 

  • Lebedeff AG (1934) Genetics of hermaphroditism in Drosophila virilis. Proc Natl Acad Sci U S A 20(12):613–616

    Article  CAS  PubMed  Google Scholar 

  • Lebo SM, Sanders EL, Sun F, Arbeitman NM (2009) Somatic, germline and sex hierarchy regulated gene expression during Drosophila metamorphosis. BMC Genomics 10:80

    Article  PubMed  Google Scholar 

  • Lucchesi JC (2009) The structure-function link of compensated chromatin in Drosophila. Curr Opin Genet Dev 19(6):550–556

    Article  CAS  PubMed  Google Scholar 

  • Marshall-Graves JA (2008) Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Annu Rev Genet 42:565–586

    Article  CAS  PubMed  Google Scholar 

  • McKeown M, Belote MJ, Baker SB (1987) A molecular analysis of transformer, a gene in Drosophila melanogaster that controls female sexual differentiation. Cell 48(3):489–499

    Article  CAS  PubMed  Google Scholar 

  • Meise M, Hilfiker-Kleiner D, Dubendorfer A, Brunner C, Nothiger R, Bopp D (1998) Sex-lethal, the master sex-determining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development 125(8):1487–1494

    CAS  PubMed  Google Scholar 

  • Morgan HT (1910) Sex limited inheritance in Drosophila. Science 32(812):120–122

    Article  CAS  PubMed  Google Scholar 

  • Morrison NI, Koukidou M, Franz G, Miller TA, Saccone G, Alphey LS, Simmons GS, Polito LC, Nagaraju J (2010) Genetic improvements to the sterile insect technique for agricultural pests. Asia Pac J Mol Biol Biotechnol (In press)

  • Muller-Holtkamp F (1995) The Sex-lethal gene homologue in Chrysomya rufifacies is highly conserved in sequence and exon-intron organization. J Mol Evol 41(4):467–477

    Article  CAS  PubMed  Google Scholar 

  • Nagoshi NR, McKeown M, Burtis CK, Belote MJ, Baker SB (1988) The control of alternative splicing at genes regulating sexual differentiation in D. melanogaster. Cell 53(2):229–236

    Article  CAS  PubMed  Google Scholar 

  • O’Neil TM, Belote MJ (1992) Interspecific comparison of the transformer gene of Drosophila reveals an unusually high degree of evolutionary divergence. Genetics 131(1):113–128

    PubMed  Google Scholar 

  • Pane A, Salvemini M, Delli Bovi P, Polito LC, Saccone G (2002) The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129(15):3715–3725

    CAS  PubMed  Google Scholar 

  • Pane A, De Simone A, Saccone G, Polito LC (2005) Evolutionary conservation of Ceratitis capitata transformer gene function. Genetics 171(2):615–624

    Article  CAS  PubMed  Google Scholar 

  • Rabinow L, Samson M (2010) The role of the Drosophila LAMMER protein kinase DOA in somatic sex determination. J Genet 89:271–277

    Article  CAS  PubMed  Google Scholar 

  • Raymond SC, Shamu EC, Shen MM, Seifert JK, Hirsch B, Hodgkin J, Zarkower D (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391(6668):691–695

    Article  CAS  PubMed  Google Scholar 

  • Rideout JE, Billeter CJ, Goodwin FS (2007) The sex-determination genes fruitless and doublesex specify a neural substrate required for courtship song. Curr Biol 17(17):1473–1478

    Article  CAS  PubMed  Google Scholar 

  • Robinett CC, Vaughan GA, Knapp MJ, Baker SB (2010) Sex and the single cell. II. There is a time and place for sex. PLoS Biol 8(5):e1000365. doi:10.1371/journal.pbio.1000365

    Article  PubMed  Google Scholar 

  • Ruiz FM, Goday C, Gonzalez P, Sanchez L (2003) Molecular analysis and developmental expression of the Sex-lethal gene of Sciara ocellaris (diptera order, nematocera suborder). Gene Expr Patterns 3(3):341–346

    Article  CAS  PubMed  Google Scholar 

  • Ruiz FM, Milano A, Salvemini M, Eirin-Lopez MJ, Perondini LA, Selivon D, Polito LC, Saccone G, Sanchez L (2007) The gene transformer of Anastrepha fruit flies (diptera, tephritidae) and its evolution in insects. PLoS ONE 2(11):e1239

    Article  PubMed  Google Scholar 

  • Ryner CL, Goodwin FS, Castrillon HD, Anand A, Villella A, Baker SB, Hall CJ, Taylor JB, Wasserman AS (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87(6):1079–1089

    Article  CAS  PubMed  Google Scholar 

  • Saccone G (1997) L’omologo del gene doublesex di Drosophila melanogaster in Ceratitis capitata: Evidenze di una parziale conservazione evolutiva nei due ditteri di una gerarchia di regolazione genica del differenziamento sessuale. Ph. D. Thesis. Università degli Studi di Napoli, Federico II

  • Saccone G, Peluso I, Artiaco D, Giordano E, Bopp D, Polito LC (1998) The Ceratitis capitata homologue of the Drosophila sex-determining gene Sex-lethal is structurally conserved, but not sex-specifically regulated. Development 125(8):1495–1500

    CAS  PubMed  Google Scholar 

  • Saccone G, Pane A, Testa G, Santoro M, Martino GD, Di Paola F, Louis C, Polito LC (2000) Sex determination in medfly: a molecular approach. In area-wide control of fruit flies and other insect pests. Area-wide control of fruit flies and other insect pests. University Sains Malaysia, Penang, Penerbit

    Google Scholar 

  • Saccone G, Pane A, Polito LC (2002) Sex determination in flies, fruitflies and butterflies. Genetica 116(1):15–23

    Article  CAS  PubMed  Google Scholar 

  • Saccone G, Pane A, Simone A, Salvemini M, Milano A, Annunziata L, Mauro U, Polito LC (2007) New sexing strains for mediterranean fruit fly Ceratitis capitata: transforming females into males. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests, pp 95–102

  • Saccone G, Salvemini M, Pane A, Polito LC (2008) Masculinization of XX Drosophila transgenic flies expressing the Ceratitis capitata DoublesexM isoform. Int J Dev Biol 52(8):1051–1057

    Article  CAS  PubMed  Google Scholar 

  • Salvemini M, Robertson M, Aronson B, Atkinson PW, Polito LC, Saccone G (2009) Ceratitis capitata transformer-2 gene is required to establish and maintain the autoregulation of Cctra, the master gene for female sex determination. Int J Dev Biol 53(1):109–120

    Article  CAS  PubMed  Google Scholar 

  • Salvemini M, Mauro U, Lombardo F, Milano A, Polito LC, Arcà B, Saccone G (2010a) Genomic organization and splicing evolution of the doublesex gene, a Drosophila regulator of sexual differentiation, in the dengue and yellow fever mosquito Aedes aegypti. BMC Evol Biol (submitted).

  • Salvemini M, Polito LC, Saccone G (2010b) fruitless alternative splicing and sex behaviour in insects: an ancient and unforgettable love story? J Genet 89:287–299

    Article  PubMed  Google Scholar 

  • Sánchez L (2008) Sex-determining mechanisms in insects. Int J Dev Biol 52(7):837–856

    Article  PubMed  Google Scholar 

  • Scali C, Catteruccia F, Li Q, Crisanti A (2005) Identification of sex-specific transcripts of the Anopheles gambiae doublesex gene. J Exp Biol 208(Pt 19):3701–3709

    Article  CAS  PubMed  Google Scholar 

  • Sekido R, Lovell-Badge R (2008) Sex determination involves synergistic action of sry and sf1 on a specific sox9 enhancer. Nature 453(7197):930–934

    Article  CAS  PubMed  Google Scholar 

  • Serna E, Gorab E, Ruiz FM, Goday C, Eirin-Lopez MJ, Sanchez L (2004) The gene Sex-lethal of the Sciaridae family (Order Diptera, suborder Nematocera) and its phylogeny in dipteran insects. Genetics 168(2):907–921

    Article  CAS  PubMed  Google Scholar 

  • Shearman CD, Frommer M (1998) The Bactrocera tryoni homologue of the Drosophila melanogaster sex-determination gene doublesex. Insect Mol Biol 7(4):355–366

    Article  CAS  PubMed  Google Scholar 

  • Shirangi RT, McKeown M (2007) Sex in flies: what ‘body–mind’ dichotomy? Dev Biol 306(1):10–19

    Article  CAS  PubMed  Google Scholar 

  • Shukla JN, Nagaraju J (2010) Doublesex: a conserved downstream gene controlled by diverse upstream regulators. J Genet 89:341–356

    Article  CAS  PubMed  Google Scholar 

  • Siera GS, Cline WT (2008) Sexual back talk with evolutionary implications: stimulation of the Drosophila sex-determination gene Sex-lethal by its target transformer. Genetics 180(4):1963–1981

    Article  CAS  PubMed  Google Scholar 

  • Sievert V, Kuhn S, Paululat A, Traut W (2000) Sequence conservation and expression of the Sex-lethal homologue in the fly Megaselia scalaris. Genome 43(2):382–390

    Article  CAS  PubMed  Google Scholar 

  • Smith AC, Roeszler NK, Ohnesorg T, Cummins MD, Farlie GP, Doran JT, Sinclair HA (2009) The avian Z-linked gene dmrt1 is required for male sex determination in the chicken. Nature 461(7261):267–271

    Article  CAS  PubMed  Google Scholar 

  • Sturtevant HA (1945) A gene in Drosophila melanogaster that transforms females into males. Genetics 30(3):297–299

    CAS  PubMed  Google Scholar 

  • Suzuki MG (2010) Sex determination: insights from the silkworm. J Genet 89:357–363

    Article  PubMed  Google Scholar 

  • Tian M, Maniatis T (1993) A splicing enhancer complex controls alternative splicing of doublesex pre-mRNA. Cell 74(1):105–114

    Article  CAS  PubMed  Google Scholar 

  • Traut W, Niimi T, Ikeo K, Sahara K (2006) Phylogeny of the sex-determining gene Sex-lethal in insects. Genome 49(3):254–262

    Article  CAS  PubMed  Google Scholar 

  • Verhulst CE, Beukeboom WL, van de Zande L (2010) Maternal control of haplodiploid sex determination in the wasp Nasonia. Science 328(5978):620–623

    Article  CAS  PubMed  Google Scholar 

  • Volff NJ, Zarkower D, Bardwell JV, Schartl M (2003) Evolutionary dynamics of the DM domain gene family in metazoans. J Mol Evol 57(Suppl 1):S241–S249. doi:10.1007/s00239-003-0033-0

    Article  CAS  PubMed  Google Scholar 

  • Wilkins SA (1995) Moving up the hierarchy: a hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17(1):71–77

    Article  CAS  PubMed  Google Scholar 

  • Wilson BE (1905) The chromosomes in relation to the determination of sex in insects. Science 22(564):500–502

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We greatly thank Daniel Bopp for his generous help and suggestions, as well as Leonard Rabinow for his interesting inputs. This work was partially supported by Prin 2008 to L.C.P., by WHO/TDR grant no. A30289 (2004 and 2005) to G.S. and by FAO/IAEA Entomology Unit, which promoted exchanges of information and unpublished data between research teams from 10 different countries belonging to 4 different continents.

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  1. Dipartimento delle Scienze Biologiche, Sezione Genetica e Biologia Molecolare, Università degli Studi di Napoli “Federico II”, Via Mezzocannone 8, 80134, Naples, Italy

    G. Saccone, M. Salvemini & L. C. Polito

  2. Istituto di Genetica e Biofisica, Consiglio Nazionale delle Ricerche, Via Pietro Castellino 111, 80131, Naples, Italy

    L. C. Polito

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  1. G. Saccone
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Correspondence to G. Saccone.

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Saccone, G., Salvemini, M. & Polito, L.C. The transformer gene of Ceratitis capitata: a paradigm for a conserved epigenetic master regulator of sex determination in insects. Genetica 139, 99–111 (2011). https://doi.org/10.1007/s10709-010-9503-7

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