Skip to main content
Log in

High Incidence of Interchromosomal Transpositions in the Evolutionary History of a Subset of Or Genes in Drosophila

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

Abstract

In insects, the odorant receptor (Or) multigene family is an intermediate-sized family with genes present in all chromosomes, indicating that duplication followed by interchromosomal transposition played an important role in the early stages of the family evolution. Here, we have explored the occurrence of interchromosomal transpositions in more recent stages through the comparative analysis of a subset of Or genes in Drosophila, where the gene content of chromosomal arms is highly conserved. The studied subset consisted of 11 Or genes located on the left arm of chromosome 3 (Muller’s D element) in D. melanogaster. Our study focused on the number and chromosomal arm location of these members of the family across the 12 Drosophila species with complete genome sequences. In contrast to previous results from in situ hybridization comparative mapping that were mainly based on single-copy genes, our study, based on members of a multigene family of moderate size, revealed repeated interchromosomal transposition events and a complex history of some of the studied genes.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ayala F (1997) Vagaries of the molecular clock. Proc Natl Acad Sci USA 94:7776–7783

    Article  PubMed  CAS  Google Scholar 

  • Bartolomé C, Charlesworth B (2006) Rates and patterns of chromosomal evolution in Drosophila pseudoobscura and D. miranda. Genetics 173:779–791

    Article  PubMed  Google Scholar 

  • Bergman CM, Pfeiffer BD, Rincon-Limas DE, Hoskins RA, Gnirke A, Mungall CJ, Wang AM, Kronmiller B, Pacleb J, Park S, Stapleton M, Wan K, George RA, de Jong PJ, Botas J, Rubin GM, Celniker SE (2002) Assessing the impact of comparative genomic sequence data on the functional annotation of the Drosophila genome. Genome Biol 3:research0086

    Google Scholar 

  • Bhutkar A, Russo SM, Smith TF, Gelbart WM (2007) Genome-scale analysis of positionally relocated genes. Genome Res 17:1880–1887

    Article  PubMed  CAS  Google Scholar 

  • Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187

    Article  PubMed  CAS  Google Scholar 

  • Burland TG (2000) DNASTAR’s Lasergene sequence analysis software. Methods Mol Biol 132:71–91

    PubMed  CAS  Google Scholar 

  • Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327–338

    Article  PubMed  CAS  Google Scholar 

  • Coghlan A, Wolfe KH (2002) Fourfold faster rate of genome rearrangement in nematodes than in Drosophila. Genome Res 12:857–867

    Article  PubMed  CAS  Google Scholar 

  • Crosby MA, Goodman JL, Strelets VB, Zhang P, Gelbart WM (2007) FlyBase: genomes by the dozen. Nucleic Acids Res 35:D486–D491

    Article  PubMed  CAS  Google Scholar 

  • Do CB, Mahabhashyam MS, Brudno M, Batzoglou S (2005) ProbCons: Probabilistic consistency-based multiple sequence alignment. Genome Res 15:330–340

    Article  PubMed  CAS  Google Scholar 

  • Drosophila 12 Genome Consortium (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • Gao Q, Chess A (1999) Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60:31–39

    Article  PubMed  CAS  Google Scholar 

  • Glusman G, Yanai I, Rubin I, Lancet D (2001) The complete human olfactory subgenome. Genome Res 11:685–702

    Article  PubMed  CAS  Google Scholar 

  • González J, Casals F, Ruiz A (2004) Duplicative and conservative transpositions of larval serum protein 1 genes in the genus Drosophila. Genetics 168:253–264

    Article  PubMed  Google Scholar 

  • Guo S, Kim J (2007) Molecular evolution of Drosophila odorant receptor genes. Mol Biol Evol 24:1198–1207

    Article  PubMed  CAS  Google Scholar 

  • Jones WD, Nguyen TA, Kloss B, Lee KJ, Vosshall LB (2005) Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr Biol 15:R119–R121

    Article  PubMed  CAS  Google Scholar 

  • Krieger J, Klink O, Mohl C, Raming K, Breer H (2003) A candidate olfactory receptor subtype highly conserved across different insect orders. J Comp Physiol A 189:519–526

    Article  CAS  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 

  • Labandeira CC, Sepkoski JJ Jr (1993) Insect diversity in the fossil record. Science 261:310–315

    Article  PubMed  CAS  Google Scholar 

  • McBride CS, Arguello JR (2007) Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics 177:1395–1416

    Article  PubMed  CAS  Google Scholar 

  • Muller JH (1940) Bearings of the Drosophila work on systematics. In: Huxley J (ed) New systematics. Claredon Press, Oxford, pp 185–268

    Google Scholar 

  • Niimura Y, Nei M (2006) Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates. J Hum Genet 51:505–517

    Article  PubMed  CAS  Google Scholar 

  • Nozawa M, Nei M (2007) Evolutionary dynamics of olfactory receptor genes in Drosophila species. Proc Natl Acad Sci USA 104:7122–7127

    Article  PubMed  CAS  Google Scholar 

  • Ramos-Onsins S, Aguadé M (1998) Molecular evolution of the Cecropin multigene family in Drosophila. Functional genes vs. pseudogenes. Genetics 150:157–171

    PubMed  CAS  Google Scholar 

  • Ranz JM, Casals F, Ruiz A (2001) How malleable is the eukaryotic genome? Extreme rate of chromosomal rearrangement in the genus Drosophila. Genome Res 11:230–239

    Article  PubMed  CAS  Google Scholar 

  • Ranz JM, González J, Casals F, Ruiz A (2003) Low occurrence of gene transposition events during the evolution of the genus Drosophila. Evol Int J Org Evol 57:1325–1335

    CAS  Google Scholar 

  • Ranz JM, Maurin D, Chan YS, von Grotthuss M, Hillier LW, Roote J, Ashburner M, Bergman CM (2007) Principles of genome evolution in the Drosophila melanogaster species group. PLoS Biol 5:e152

    Article  PubMed  Google Scholar 

  • Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci USA 100(Suppl 2):14537–14542

    Article  PubMed  CAS  Google Scholar 

  • Russo CA, Takezaki N, Nei M (1995) Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol 12:391–404

    PubMed  CAS  Google Scholar 

  • Segarra C, Aguadé M (1992) Molecular organization of the X chromosome in different species of the obscura group of Drosophila. Genetics 130:513–521

    PubMed  CAS  Google Scholar 

  • Segarra C, Lozovskaya ER, Ribó G, Aguadé M, Hartl DL (1995) P1 clones from Drosophila melanogaster as markers to study the chromosomal evolution of Muller’s A element in two species of the obscura group of Drosophila. Chromosoma 104:129–136

    PubMed  CAS  Google Scholar 

  • Segarra C, Ribó G, Aguadé M (1996) Differentiation of Muller’s chromosomal elements D and E in the obscura group of Drosophila. Genetics 144:139–146

    PubMed  CAS  Google Scholar 

  • Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725–736

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Carmen Segarra and two anonymous reviewers for comments on the manuscript and David Salguero for technical assistance. I.C.C. was supported by predoctoral fellowship SFRH/BD/11107/2002 from Fundação para a Ciência e a Tecnologia, Portugal. I.C.C. dedicates this work to the memory of E. Pires. This work was supported by Grant BFU2004-02253 from Comisión Interdepartamental de Ciencia y Tecnología, Spain; Grant 2005SGR-00166 from Comissió Interdepartamental de Recerca i Innovació Tecnològica, Catalonia, Spain; and special support (Distinció per la Promoció de la Recerca Universitària) from Generalitat de Catalunya to M.A.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Montserrat Aguadé.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 67 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Conceição, I.C., Aguadé, M. High Incidence of Interchromosomal Transpositions in the Evolutionary History of a Subset of Or Genes in Drosophila . J Mol Evol 66, 325–332 (2008). https://doi.org/10.1007/s00239-008-9071-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-008-9071-y

Keywords

Navigation