Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila

Nature volume 423, pages 715–719 (2003)Cite this article

Abstract

Speciation—the splitting of one species into two—occurs by the evolution of any of several forms of reproductive isolation between taxa, including the intrinsic sterility and inviability of hybrids. Abundant evidence shows that these hybrid fitness problems are caused by incompatible interactions between loci: new alleles that become established in one species are sometimes functionally incompatible with alleles at interacting loci from another species. However, almost nothing is known about the genes involved in such hybrid incompatibilities or the evolutionary forces that drive their divergence. Here we identify a gene that causes epistatic inviability in hybrids between two fruitfly species, Drosophila melanogaster and D. simulans. Our population genetic analysis reveals that this gene—which encodes a nuclear pore protein—evolved by positive natural selection in both species' lineages. These results show that a lethal hybrid incompatibility has evolved as a by-product of adaptive protein evolution.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Deficiency mapping hybrid lethality.
Figure 2: Nup98-Nup96 structure and evolution.
Figure 3: Evolutionary history of Nup96 with ratios of replacement to silent substitutions mapped onto the known phylogeny of the D. melanogaster group species.

Similar content being viewed by others

References

  1. Coyne, J. Genetics and speciation. Nature 355, 511–515 (1992)

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Orr, H. A. & Presgraves, D. C. Speciation by postzygotic isolation: forces, genes and molecules. Bioessays 22, 1085–1094 (2000)

    Article  CAS  PubMed  Google Scholar 

  3. Wittbrodt, J. et al. Novel putative receptor tyrosine kinase encoded by the melanoma-inducing Tu locus in Xiphophorus. Nature 341, 415–421 (1989)

    Article  ADS  CAS  PubMed  Google Scholar 

  4. Ting, C.-T., Tsaur, S.-C., Wu, M.-L. & Wu, C.-I. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282, 1501–1504 (1998)

    Article  CAS  PubMed  Google Scholar 

  5. Barbash, D. A., Siino, D. F., Tarone, A. M. & Roote, J. A rapidly evolving Myb-related protein causes species isolation in Drosophila. Proc. Natl Acad. Sci. USA 100, 5302–5307 (2003)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  6. Sturtevant, A. H. The genetics of Drosophila simulans. Yb. Carnegie Inst. Wash. 399, 1–62 (1929)

    Google Scholar 

  7. Sturtevant, A. H. Genetic studies on Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster. Genetics 5, 488–500 (1920)

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Lachaise, D., David, J. R., Lemeunier, F., Tsacas, L. & Ashburner, M. The reproductive relationships of Drosophila sechellia with D. mauritiana, D. simulans, and D. melanogaster from the Afrotropical region. Evolution 1986, 262–271 (1986)

    Google Scholar 

  9. Davis, A. W. et al. Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature 380, 157–159 (1996)

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Sawamura, K., Davis, A. W. & Wu, C.-I. Genetic analysis of speciation by means of introgression into Drosophila melanogaster. Proc. Natl Acad. Sci. USA 97, 2652–2655 (2000)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  11. Presgraves, D. C. A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163, 955–972 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Dobzhansky, T. Genetics and the Origin of Species (Columbia Univ. Press, New York, 1937)

    Google Scholar 

  13. Muller, H. J. & Pontecorvo, G. Recessive genes causing interspecific sterility and other disharmonies between Drosophila melanogaster and simulans. Genetics 27, 157 (1942)

    Google Scholar 

  14. Turelli, M. & Orr, H. A. Dominance, epistasis and the genetics of postzygotic isolation. Genetics 154, 1663–1679 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Watanabe, T. K. A gene that rescues the lethal hybrids between Drosophila melanogaster and D. simulans. Jpn. J. Genet. 54, 325–331 (1979)

    Article  Google Scholar 

  16. Ryan, K. J. & Wente, S. R. The nuclear pore complex: a protein machine bridging the nucleus and the cytoplasm. Curr. Opin. Cell Biol. 12, 361–371 (2000)

    Article  CAS  PubMed  Google Scholar 

  17. Vasu, S. K. & Forbes, D. J. Nuclear pores and nuclear assembly. Curr. Opin. Cell Biol. 13, 363–375 (2001)

    Article  CAS  PubMed  Google Scholar 

  18. Rout, M. P. et al. The yeast nuclear pore complex: composition, architecture and transport mechanism. J. Cell Biol. 148, 635–651 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Cronshaw, J. M., Krutchinsky, A. N., Zhang, W., Chait, B. T. & Matunis, M. J. Proteomic analysis of the mammalian nuclear pore complex. J. Cell Biol. 158, 915–927 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Fontoura, B. M. A., Dales, S., Blobel, G. & Zhong, H. The nucleoporin Nup98 associates with the intranuclear filamentous protein network of TPR. Proc. Natl Acad. Sci. USA 98, 3208–3213 (2001)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  21. Griffis, E. R., Altan, N., Lippincott-Schwartz, J. & Powers, M. A. Nup98 is a mobile nucleoporin with transcription dependent dynamics. Mol. Biol. Cell 13, 1282–1297 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Griffis, E. R., Xu, S. & Powers, M. A. Nup98 localizes to both nuclear and cytoplasmic sides of the nuclear pore and binds to two distinct nucleoporin subcomplexes Mol. Biol. Cell. 14, 600–610 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Belgareh, N. et al. An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J. Cell Biol. 154, 1147–1160 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Emtage, J. L. T., Bucci, M., Watkins, J. L. & Wente, S. R. Defining the essential functional regions of the nucleoporin Nup145p. J. Cell Sci. 110, 911–925 (1997)

    CAS  PubMed  Google Scholar 

  25. Powers, M. A., Forbes, D. J., Dahlberg, D. J. & Lund, E. The vertebrate GLFG nucleoporin, Nup98, is an essential component of multiple RNA export pathways. J. Cell Biol. 136, 241–250 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Fontoura, B. M. A., Blobel, G. & Matunis, M. J. A conserved biogenesis pathway for nucleoporins: proteolytic processing of a 186-Kilodalton precursor generates Nup98 and the novel nucleoporin, Nup96. J. Cell Biol. 144, 1097–1112 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rosenblum, J. S. & Blobel, G. Autoproteolysis in nucleoporin biogenesis. Proc. Natl Acad. Sci. USA 96, 11370–11375 (1999)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  28. Teixeira, M. T., Fabre, E. & Dujon, B. Self-catalyzed cleavage of the yeast nucleoporin Nup145 precursor. J. Biol. Chem. 274, 32439–32444 (1999)

    Article  CAS  PubMed  Google Scholar 

  29. Kimura, M. Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267, 275–276 (1977)

    Article  ADS  CAS  PubMed  Google Scholar 

  30. Wall, J. D., Andolfatto, P. & Przeworski, M. Testing models of selection and demography in Drosophila simulans. Genetics 162, 203–216 (2002)

    CAS  PubMed  PubMed Central  Google Scholar 

  31. McDonald, J. H. & Kreitman, M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652–654 (1991)

    Article  ADS  CAS  PubMed  Google Scholar 

  32. Hey, J. & Kliman, R. M. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol. Biol. Evol. 10, 804–822 (1993)

    CAS  PubMed  Google Scholar 

  33. Maynard Smith, J. & Haigh, J. The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23–35 (1974)

    Article  Google Scholar 

  34. Kaplan, N. L., Hudson, R. R. & Langley, C. H. The hitch-hiking effect revisited. Genetics 123, 887–899 (1989)

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Braverman, J. M., Hudson, R. R., Kaplan, N. L., Langley, C. H. & Stephan, W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140, 783–796 (1995)

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Fay, J. C. & Wu, C.-I. Hitchhiking under positive Darwinian selection. Genetics 155, 1405–1413 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Andolfatto, P. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol. Biol. Evol. 18, 279–290 (2001)

    Article  CAS  PubMed  Google Scholar 

  38. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595 (1989)

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Naveira, H. F. & Maside, X. R. in Endless Forms (eds Howard, D. J. & Berlocher, S. H.) 330–338 (Oxford Univ. Press, Oxford, 1998)

    Google Scholar 

  40. Wu, C.-I. & Hollocher, H. in Endless Forms (eds Howard, D. J. & Berlocher, S. H.) 339–351 (Oxford Univ. Press, Oxford, 1998)

    Google Scholar 

  41. Rose, M. & Doolittle, W. F. Molecular biological mechanisms of speciation. Science 220, 157–162 (1983)

    Article  ADS  CAS  PubMed  Google Scholar 

  42. Wilson, A. C. in Molecular Evolution (ed. Ayala, F. J.) 225–234 (Sinauer, Sunderland, Massachusetts, 1976)

    Google Scholar 

  43. Lynch, M. & Force, A. G. The origin of interspecific genomic incompatibility via gene duplication. Am. Nat. 156, 590–605 (2000)

    Article  PubMed  Google Scholar 

  44. Yang, Q., Rout, M. P. & Akey, C. W. Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol. Cell 1, 223–234 (1998)

    Article  CAS  PubMed  Google Scholar 

  45. Erickson, M. R. S., Galletta, B. J. & Abmayr, S. M. Drosophila myoblast city encodes a conserved protein that is essential for myoblast fusion, dorsal closure and cytoskeletal organization. J. Cell Biol. 138, 589–603 (1997)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Keller, C. A., Grill, M. A. & Abmayr, S. M. A role for nautilus in the differentiation of muscle precursors. Dev. Biol. 202, 157–171 (1998)

    Article  CAS  PubMed  Google Scholar 

  47. Comeron, J. M. K-estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15, 763–764 (1999)

    Article  CAS  PubMed  Google Scholar 

  48. Rozas, J. & Rozas, R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175 (1999)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank J. Coyne for providing the D. yakuba stock, and C. Aquadro for the Zimbabwe strains of D. melanogaster and D. simulans. We acknowledge the contribution of M. Erickson in preliminary molecular analysis of the nucleoporin locus. We thank A. Betancourt, A. Clark, J. Coyne, W. Stephan and J. Werren for helpful discussion and comments. This work was supported by funds from a Caspari Fellowship, a Messermith Fellowship, and a Dissertation Improvement Grant from the National Science Foundation to D.C.P.; from the National Institutes of Health and National Science Foundation to S.M.A.; and from the National Institutes of Health to H.A.O.

Author information

Authors and Affiliations

  1. Department of Biology, University of Rochester, Rochester, New York, 14627, USA

    Daven C. Presgraves & H. Allen Orr

  2. Department of Biochemistry and Molecular Biology, The Pennsylvania State University, 459 North Frear Lab, University Park, Pennsylvania, 16802, USA

    Lakshmi Balagopalan & Susan M. Abmayr

Authors
  1. Daven C. Presgraves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lakshmi Balagopalan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susan M. Abmayr
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H. Allen Orr
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daven C. Presgraves.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Presgraves, D., Balagopalan, L., Abmayr, S. et al. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423, 715–719 (2003). https://doi.org/10.1038/nature01679

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01679

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing