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Selective sweep of a newly evolved sperm-specific gene in Drosophila

Nature volume 396, pages 572–575 (1998)Cite this article

Abstract

The pattern of genetic variation across the genome of Drosophila melanogaster is consistent with the occurrence of frequent ‘selective sweeps’, in which new favourable mutations become incorporated into the species so quickly that linked alleles can ‘hitchhike’ and also become fixed1. Because of the hitchhiking of linked genes, it is generally difficult to identify the target of any putative selective sweep. Here, however, we identify a new gene in D. melanogaster that codes for a sperm-specific axonemal dynein subunit. The gene has a new testes-specific promoter derived from a protein-coding region in a gene encoding the cell-adhesion protein annexin X (AnnX), and it contains a new protein-coding exon derived from an intron in a gene encoding a cytoplasmic dynein intermediate chain (Cdic). The new transcription unit, designated Sdic (for sperm-specific dynein intermediate chain), has been duplicated about tenfold in a tandem array. Consistent with the selective sweep of this gene, the level of genetic polymorphism near Sdic is unusually low. The discovery of this gene supports other results that point to the rapid molecular evolution of male reproductive functions2,3,4.

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Figure 1: A model for the creation of the Sdic gene.
Figure 2: Creation of the first exon of Sdic from the sequence of intron 3 of Cdic, and a comparison of the N-terminal domain of Sdic coded by this first exon withthe N-terminal domains of axonemal dynein intermediate chains from Chlamydomonas reinhardtii (oda6, GenBank accession number X55382) and Anthocidaris crassipina (AcIC3, GenBank accession number D28863).
Figure 3: Testis specificity of Sdic transcription, demonstrated by reverse transcription and the polymerase chain reaction.
Figure 4: Testes distribution of an Sdic::GFP fusion protein, whose translation is driven by the Sdic promoter.
Figure 5: Detailed structure of the Sdic promoter formed by the junction between AnnX exon a4 and Cdic intron 3.

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Acknowledgements

This work was supported by grants from the US Public Health Service. We thank W.Gilbert and S. R. Palumbi for their valuable suggestions and careful reading of the manuscript.

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Authors and Affiliations

  1. Department of Organismic & Evolutionary Biology, Harvard University, Cambridge, 02138, Massachusetts, USA

    Dmitry I. Nurminsky, Daniel De Aguiar & Daniel L. Hartl

  2. Department of Anatomy and Cell Biology, Tufts University School of Medicine, Boston, 02111, Massachusetts, USA

    Maria V. Nurminskaya

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  1. Dmitry I. Nurminsky
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  4. Daniel L. Hartl
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Correspondence to Dmitry I. Nurminsky.

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Nurminsky, D., Nurminskaya, M., Aguiar, D. et al. Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature 396, 572–575 (1998). https://doi.org/10.1038/25126

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