Skip to main content
SpringerLink
Log in

Alternative Starts of Transcription, Several Paralogues, and Almost-Fixed Interspecific Differences of the Gene fruitless in a Hemimetabolous Insect

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

In fruit flies, the gene fruitless (fru) governs the establishment of the potential for male sexual behavior. We partially cloned fru from a hemimetabolous insect for the first time and we compared fru among three closely related and acoustically communicating grasshopper species: Chorthippus biguttulus, C. brunneus, and C. mollis. The fru of grasshoppers is organized similarly to fru of holometabolous insects, with a BTB and Zn-finger domains separated by a nonconserved repetitive linker. As in Drosophila, several transcripts of fru are found in grasshoppers. We also present evidence for the coexistence of several copies of fru in the grasshopper genome. Within species these copies are almost identical and carry almost-fixed species-specific differences. This suggests that the paralogous copies of fru in grasshoppers do not evolve independently from each other.

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

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Anand A, Villella A, Ryner LC, Carlo T, Goodwin SF, Song HJ, Gailey DA, Morales A, Hall JC, Baker BS, Taylor BJ (2001) Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless. Genetics 158:1569–1595

    PubMed  CAS  Google Scholar 

  • Baker BS, Taylor BJ, Hall JC (2001) Are complex bahaviors specified by dedicated regulatory genes? Reasoning from Drosophila. Cell 105:13–24

    Article  PubMed  CAS  Google Scholar 

  • Bensasson D, Petrov DA, Zhang DX, Hartl DL, Hewitt GM (2001) Genomic gigantism: DNA loss is slow in mountain grasshoppers. Mol Biol Evol 8:246–253

    Google Scholar 

  • Billeter JC, Goodwin SF (2004) Characterization of Drosophila fruitless-gal4 transgenes reveals expression in male-specific fruitless neurons and innervation of male reproductive structures. J Comp Neurol 475:270–287

    Article  PubMed  CAS  Google Scholar 

  • Brown DD, Wensink PC, Jordan E (1972) Xenopus laevis and Xenopus mulleri: the evolution of tandem genes. J Mol Biol 63:57–73

    Article  PubMed  CAS  Google Scholar 

  • Cooper SJ, Hewitt GM (1993) Nuclear DNA sequence divergence between parapatric subspecies of the grasshopper Chorthippus parallelus. Insect Mol Biol 2:185–194

    PubMed  CAS  Google Scholar 

  • Dauwalder B, Tsujimoto S, Moss J, Mattox W (2002) The Drosophila takeout gene is regulated by the somatic sex-determination pathway and affects male courtship behavior. Genes Dev 16:2879–2892

    Article  PubMed  CAS  Google Scholar 

  • Davis T, Kurihara J, Yamamoto D (2000a) Genomic organisation and characterisation of the neural sex-determination gene fruitless (fru) in the Hawaiian species Drosophila heteroneura. Gene 246:143–149

    Article  CAS  Google Scholar 

  • Davis T, Kurihara J, Yoshino E, Yamamoto D (2000b) Genomic organisation of the neural sex determination gene fruitless (fru) in the Hawaiian species Drosophila silvestris and the conservation of the fru BTB protein-protein-binding domain throughout evolution. Hereditas 132:67–78

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Drapeau MD, Radovic A, Wittkopp PJ, Long AD (2003) A gene necessary for normal male courtship, yellow, acts downstream of fruitless in the Drosophila melanogaster larval brain. J Neurobiol 55:53–72

    Article  PubMed  CAS  Google Scholar 

  • Gailey DA, Ohshima S, Santiago SJ, Montez JM, Arellano AR, Robillo J, Villarimo CA, Roberts L, Fine E, Villella A, Hall JC (1997) The muscle of lawrence in Drosophila: a case of repeated evolutionary loss. Proc Natl Acad Sci USA 94:4543–4547

    Article  PubMed  CAS  Google Scholar 

  • Gailey DA, Ho SK, Ohshima S, Liu JH, Eyassu M, Washington MA, Yamamoto D, Davis T (2000) A phylogeny of the Drosophilidae using the sex-behaviour gene fruitless. Hereditas 133:81–83

    Article  PubMed  CAS  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 million years of insect evolution. Mol Biol Evol 23(3):633–643

    Article  PubMed  CAS  Google Scholar 

  • Goodwin SF, Taylor BJ, Villella A, Foss M, Ryner LC, Baker BS, Hall JC (2000) Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics 154:725–745

    PubMed  CAS  Google Scholar 

  • Greenspan RJ, Ferveur JF (2000) Courtship in Drosophila. Annu Rev Genet 34:205–232

    Article  PubMed  CAS  Google Scholar 

  • Heinrichs V, Ryner LC, Baker BS (1998) Regulation of sex-specific selection of fruitless 5’ splice sites by transformer and transformer-2. Mol Cell Biol 18:450–458

    PubMed  CAS  Google Scholar 

  • Helversen Ov, Helversen Dv (1994) Forces driving coevolution of song and song recognition in grasshoppers. In: Schildberger K, Elsner N (eds) Neural basis of behavioural adaptations. Gustav Fischer Verlag, Stuttgart, pp 253–284

    Google Scholar 

  • Innan H (2004) Theories for analyzing polymorphism data in duplicated genes. Genes Genet Syst 79:65–75

    Article  PubMed  CAS  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 USA 93:9687–9692

    Article  PubMed  CAS  Google Scholar 

  • Jacobs W (1953) Verhaltensbiologische Studien an Feldheuschrecken. Z Tierpsychol Beiheft 1:1–228

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Kyriacou CP (2002) Single gene mutations in Drosophila: What can they tell us about the evolution of sexual behaviour? Genetica 116:197–203

    Article  PubMed  CAS  Google Scholar 

  • Lawrence PA, Johnston P (1986) The muscle pattern of a segment of Drosophila may be determined by neurons and not by contributing myoblasts. Cell 45:505–513

    Article  PubMed  CAS  Google Scholar 

  • Lee G, Hall JC (2000) A newly uncovered phenotype associated with the fruitless gene of Drosophila melanogaster: aggression-like head interactions between mutant males. Behav Genet 30:263–275

    Article  PubMed  CAS  Google Scholar 

  • Lee G, Foss M, Goodwin SF, Carlo T, Taylor BJ, Hall JC (2000) Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J Neurobiol 43:404–426

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  PubMed  CAS  Google Scholar 

  • Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, Baker BS (2005) Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436:395–400

    PubMed  CAS  Google Scholar 

  • Marchler-Bauer A, Anderson JB, Cherukuri PF, DeWeese-Scott C, Geer LY, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Marchler GH, Mullokandov M, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Yamashita RA, Yin JJ, Zhang D, Bryant SH (2005) CDD: a Conserved Domain Database for protein classification. Nucleic Acids Res 33:D192–D196

    Article  PubMed  CAS  Google Scholar 

  • Mason DJ, Butlin RK, Gacesa P (1995) An unusual mitochondrial DNA polymorphism in the Chorthippus biguttulus species group (Orthoptera: Acrididae). Mol Ecol 4:121–126

    Google Scholar 

  • Mount SM, Burks C, Hertz G, Stormo GD, White O, Fields C (1992) Splicing signals in Drosophila: intron size, information content, and consensus sequences. Nucleic Acids Res 20:4255–4262

    PubMed  CAS  Google Scholar 

  • Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Rogozin IB, Piontkivska H (2000) Purifying selection and birth-and-death evolution in the ubiquitin gene family. Proc Natl Acad Sci USA 97:10866–10871

    Article  PubMed  CAS  Google Scholar 

  • Parkin EJ, Butlin RK (2004) Within- and between-individual sequence variation among ITS1 copies in the meadow grasshopper Chorthippus parallelus indicates frequent intrachromosomal gene conversion. Mol Biol Evol 21:1595–1601

    Article  PubMed  CAS  Google Scholar 

  • Petrov DA, Sangster TA, Johnston JS, Hartl DL, Shaw KL (2000) Evidence for DNA loss as a determinant of genome size. Science 287:1060–1062

    Article  PubMed  CAS  Google Scholar 

  • Piontkivska H, Nei M (2003) Birth-and-death evolution in primate MHC class I genes: divergence time estimates. Mol Biol Evol 20:601–609

    Article  PubMed  CAS  Google Scholar 

  • Piontkivska H, Rooney AP, Nei M (2002) Purifying selection and birth-and-death evolution in the histone H4 gene family. Mol Biol Evol 19:689–697

    PubMed  CAS  Google Scholar 

  • Ragge DR (1987) Speciation and biogeography of some southern european Orthoptera, as revealed by their songs. In: Baccetti B (ed) Evolutionary biology of orthopteroid insects. Ellis Horwood, Chichester, UK, pp 418–426

    Google Scholar 

  • Rooney AP (2004) Mechanisms underlying the evolution and maintenance of functionally heterogeneous 18S rRNA genes in Apicomplexans. Mol Biol Evol 21:1704–1711

    Article  PubMed  CAS  Google Scholar 

  • Rooney AP, Ward TJ (2005) Evolution of a large ribosomal RNA multigene family in filamentous fungi: birth and death of a concerted evolution paradigm. Proc Natl Acad Sci USA 102:5084–5089

    Article  PubMed  CAS  Google Scholar 

  • Rooney AP, Piontkivska H, Nei M (2002). Molecular evolution of the nontandemly repeated genes of the histone 3 multigene family. Mol Biol Evol 19:68–75

    PubMed  CAS  Google Scholar 

  • Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079–1089

    Article  PubMed  CAS  Google Scholar 

  • Song HJ, Taylor BJ (2003) fruitless gene is required to maintain neuronal identity in evenskipped-expressing neurons in the embryonic CNS of Drosophila. J Neurobiol 55:115–133

    Article  PubMed  CAS  Google Scholar 

  • Song HJ, Billeter JC, Reynaud E, Carlo T, Spana EP, Perrimon N, Goodwin SF, Baker BS, Taylor BJ (2002) The fruitless gene is required for the proper formation of axonal tracts in the embryonic central nervous system of Drosophila. Genetics 162:1703–1724

    PubMed  CAS  Google Scholar 

  • Swofford DL (2000) PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Sinauer, Sunderland: MA

    Google Scholar 

  • Usui-Aoki K, Ito H, Ui-Tei K, Takahashi K, Lukacsovich T, Awano W, Nakata H, Piao ZF, Nilsson EE, Tomida J, Yamamoto D (2000) Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol 2:500–506

    Article  PubMed  CAS  Google Scholar 

  • Villella A, Gailey DA, Berwald B, Ohshima S, Barnes PT, Hall JC (1997) Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics 147:1107–1130

    PubMed  CAS  Google Scholar 

  • Yamamoto D, Nakano Y (1999) Sexual behavior mutants revisited: molecular and cellular basis of Drosophila mating. Cell Mol Life Sci 56:634–646

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto D, Usui-Aoki K, Shima S (2004) Male-specific expression of the fruitless protein is not common to all Drosophila species. Genetica 120:267–272

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Dyer KD, Rosenberg HF (2000) Evolution of the rodent eosinophil-associated RNase gene family by rapid gene sorting and positive selection. Proc Natl Acad Sci USA 97:4701–4706

    Article  PubMed  CAS  Google Scholar 

  • Zimmer EA, Martin SL, Beverley SM, Kan YW, Wilson AC (1980) Rapid duplication and loss of genes coding for the chains of hemoglobin. Proc Natl Acad Sci USA 77:2158–2162

    Article  PubMed  CAS  Google Scholar 

  • Zollman S, Godt D, Privé GG, Couderc JL, Laski FA (1994) The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci USA 91:10717–10721

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Andrea Ross for her assistance in the laboratory. We are grateful to Marc Holderied for a critical reading of the manuscript and helpful advice. We also thank two anonymous reviewers for valuable comments that significantly improved the manuscript. This work was supported by a HWP grant to J. U. and by the Deutsche Forschungsgemeinschaft (DFG) grant within the priority program “Radiations–Origins of Biological Diversity” to F.M.

Author information

Authors and Affiliations

  1. Department of Zoology, University of Erlangen, Staudtstr. 5, 91058, Erlangen, Germany

    Jana Ustinova & Frieder Mayer

Authors
  1. Jana Ustinova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Frieder Mayer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frieder Mayer.

Additional information

[Reviewing Editor: Dr. Willie Swanson]

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ustinova, J., Mayer, F. Alternative Starts of Transcription, Several Paralogues, and Almost-Fixed Interspecific Differences of the Gene fruitless in a Hemimetabolous Insect. J Mol Evol 63, 788–800 (2006). https://doi.org/10.1007/s00239-005-6230-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-005-6230-2

Keywords

Search

Navigation