Abstract
The doublesex (dsx) gene of several Anastrepha species was isolated and characterised. Its molecular organisation was found to be the same in all the species examined. This gene is composed of four exons: Exons 1 and 2 are common to both sexes, exon 3 is female specific, and exon 4 is male specific. It codes for both the female DsxF and male DsxM proteins, corresponding to the sex-specific splicing product of its primary transcript; male-specific splicing is the default mode. A comparison of the Dsx proteins of different Anastrepha species with those of other insects showed them to be very similar. Molecular evolutionary analysis (both at the nucleotide and amino acid levels) of dsx in different insects revealed a topology in good agreement with their owners’ taxonomic relationships. The great majority of the nucleotide changes detected in the dsx gene of the analysed species were significantly synonymous, evidence that strong purifying selection has acted on dsx so that the functional structure of the Dsx proteins is preserved. However, the common region of DsxF and DsxM proteins appeared to be the main target for selection acting upon the long-term evolution of gene dsx.
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References
Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72:291–336
Burtis KC, Baker BS (1989) Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56:997–1010
Cho S, Wensink PC (1997) DNA binding by the male and female doublesex proteins of Drosophila melanogaster. J Biol Chem 272:3185–3189
Hediger M, Burghardt G, Siegenthaler C, Buser N, Hilfiker-Kleiner D, Dübendorfer A, Bopp D (2004) Sex determination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev Genes Evol 214:29–42
Korneyev VA (1999) Phylogeny relationships among the families of the superfamily tephritoidea. In: Aluja A, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC, Boca Ratón, FL, pp 3–37
Kuhn S, Sievert V, Traut W (2000) The sex-determining gene doublesex in the fly Megaselia scalaris: conserved structure and sex-specific splicing. Genome 43:1011–1020
Kulathinal RJ, Skwarek L, Morton RA, Singh RS (2003) Rapid evolution of the sex-determining gene, transformer: structural diversity and rate heterogeneity among sibling species of Drosophila. Mol Biol Evol 20:441–452
Lagos D, Ruiz MF, Sánchez L, Komitopoulou K (2005) Isolation and characterization of the Bactrocera oleae genes orthologous to the sex determination Sex-lethal and doublesex genes of Drosophila melanogaster. Gene 348:111–121
Norrbom AL, Zucchi RA, Hernández-Ortiz V (1999) Phylogeny of the genera Anastrepha and Toxotrypana (Trypetinae: Toxotrypanini) based on morphology. In: Aluja A, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC, Boca Ratón, FL, pp 299–342
Ohbayashi F, Suzuki MG, Mita K, Okano K, Shimada T (2001) A homologue of the Drosophila doublesex gene is transcribed into sex-specific mRNA isoforms in silkworm, Bombyx mori. Comp Biochem Physiol B 128:145–158
O’Neil MT, Belote JM (1992) Interspecific comparison of the transformer gene of Drosophila reveals an unusually high degree of evolutionary divergence. Genetics 131:113–128
Ruiz MF, Stefani RN, Mascarenhas RO, Perondini ALP, Selivon D, Sánchez L (2005) The gene doublesex of the fruit fly Anastrepha obliqua (Diptera, Tephritidae). Genetics 171:849–854
Sánchez L, Gorfinkiel N, Guerrero I (2005) Sex determination and the development of the genital disc. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science, vol. 1. Elsevier Pergamon, Oxford, UK, pp 1–38
Scali Ch, Catteruccia F, Li Q, Crisanti A (2005) Identification of sex-specific transcripts of the Anopheles gambiae doublesex gene. J Exp Biol 208:3701–3709
Selivon D, Perondini ALP, Morgante JS (2005) A genetic-morphological characterisation of two cryptic species of Anastrepha fraterculus complex (Diptera, Tephritidae). Ann Entomol Soc Amer 98:365–381
Serna E, Gorab E, Ruiz MF, Goday C, Eirín-López JM, Sánchez L (2004) The gene Sex-lethal of the Sciaridae Family (Order Diptera, Suborder Nematocera) and its phylogeny in dipteran insects. Genetics 168:907–921
Shearman DC, Frommer AM (1998) The Bactrocera tryoni homologue of the Drosophila melanogaster sex-determination gene doublesex. Insect Mol Biol 7:1–12
Acknowledgements
This work was financed by grants BMC2002-02858 and BFU2005-03000 awarded to L. Sánchez by the D.G.I.C.Y.T., by grants from a Joint Programme of the CSIC (20004BR0005 to L. Sánchez, Spain) and CNPq (690088/02-7 to A.L.P. Perondini, Brazil) and a grant to D. Selivon (FAPESP, 03/02698-3, Brazil). DS and ALPP are fellows of CNPq. J. M. Eirín-López was awarded a Postdoctoral Marie Curie International Fellowship within the 6th European Community Framework Programme.
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Communicated by: P. Simpson
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Table S1
Host fruits and collecting site of the Anastrepha species (DOC 48.5 kb)
Fig. S1
Comparison of the Dsx predicted polypeptides of Anastrepha species. a Sequence common to both sexes; b female-specific sequence; and c male-specific sequence. The OD1 and OD2 domains are shaded in grey. Points stand for the same amino acid. obl A. obliqua; sp1 A. sp. 1 aff. fraterculus, sp.2 A. sp. 2 aff. fraterculus, sp.3 A. sp. 3 aff. fraterculus, sp.4 A. sp. 4 aff. fraterculus, grd A. grandis, ser A. serpentine, sor A. sororcula, str A. striata, bis A. bistrigata and ami A. amita (PPT 21 kb)
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Ruiz, M.F., Eirín-López, J.M., Stefani, R.N. et al. The gene doublesex of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. Dev Genes Evol 217, 725–731 (2007). https://doi.org/10.1007/s00427-007-0178-8
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DOI: https://doi.org/10.1007/s00427-007-0178-8