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The molecular evolutionary basis of species formation

Abstract

All plant and animal species arise by speciation — the evolutionary splitting of one species into two reproductively incompatible species. But until recently our understanding of the molecular genetic details of speciation was slow in coming and largely limited to Drosophila species. Here, I review progress in determining the molecular identities and evolutionary histories of several new 'speciation genes' that cause hybrid dysfunction between species of yeast, flies, mice and plants. The new work suggests that, surprisingly, the first steps in the evolution of hybrid dysfunction are not necessarily adaptive.

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Figure 1: The molecular evolutionary basis of genetic incompatibilities that cause hybrid dysfunction.

References

  1. Mayr, E. Systematics and the Origin of Species (Columbia Univ. Press, New York, 1942).

    Google Scholar 

  2. Coyne, J. A. & Orr, H. A. Speciation (Sinauer, Sunderland, Massachusetts, 2004).

    Google Scholar 

  3. Dobzhansky, T. Genetics and the Origin of Species 364 (Columbia Univ. Press, New York, 1937).

    Google Scholar 

  4. Muller, H. J. Isolating mechanisms, evolution, and temperature. Biol. Symp. 6, 71–125 (1942).

    Google Scholar 

  5. Rieseberg, L. H. & Willis, J. H. Plant speciation. Science 317, 910–914 (2007).

    CAS  Article  Google Scholar 

  6. Baker, R. J. & Bickham, J. W. Speciation by monobrachial centric fusions. Proc. Natl Acad. Sci. USA 83, 8245–8248 (1986).

    CAS  Article  Google Scholar 

  7. Bordenstein, S. R., O'Hara, F. P. & Werren, J. H. Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409, 707–710 (2001).

    CAS  Article  Google Scholar 

  8. Al-Kaff, N. et al. Detailed dissection of the chromosomal region containing the Ph1 locus in wheat Triticum aestivum: with deletion mutants and expression profiling. Ann. Bot. 101, 863–872 (2008).

    CAS  Article  Google Scholar 

  9. Chen, J. et al. A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica–japonica hybrids in rice. Proc. Natl Acad. Sci. USA 105, 11436–11441 (2008).

    CAS  Article  Google Scholar 

  10. Jeuken, M. J. W. et al. Rin4 causes hybrid necrosis and race-specific resistance in an interspecific lettuce hybrid. Plant Cell23 Oct 2009 (doi:10.1105/tpc.109.070334).

    CAS  Article  Google Scholar 

  11. Long, Y. et al. Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc. Natl Acad. Sci. USA 105, 18871–18876 (2008).

    CAS  Article  Google Scholar 

  12. Schluter, D. & Conte, G. L. Genetics and ecological speciation. Proc. Natl Acad. Sci. USA 106, 9955–9962 (2009).

    CAS  Article  Google Scholar 

  13. Dettman, J. R., Sirjusingh, C., Kohn, L. M. & Anderson, J. B. Incipient speciation by divergent adaptation and antagonistic epistasis in yeast. Nature 447, 585–588 (2007).

    CAS  Article  Google Scholar 

  14. Lee, H.-Y. et al. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135, 1065–1073 (2008).

    CAS  Article  Google Scholar 

  15. Barbash, D. A. Clash of the genomes. Cell 135, 1002–1003 (2008).

    CAS  Article  Google Scholar 

  16. Jiang, H., Guan, W., Pinney, D., Wang, W. & Gu, Z. Relaxation of yeast mitochondrial functions after whole-genome duplication. Genome Res. 18, 1466–1471 (2008).

    CAS  Article  Google Scholar 

  17. Costanzo, M. C., Bonnefoy, N., Williams, E. H., Clark-Walker, G. D. & Fox, T. D. Highly diverged homologs of Saccharomyces cerevisiae mitochondrial mRNA-specific translational activators have orthologous functions in other budding yeasts. Genetics 154, 999–1012 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Ellison, C. K., Niehuis, O. & Gadau, J. Hybrid breakdown and mitochondrial dysfunction in hybrids of Nasonia parasitoid wasps. J. Evol. Biol. 21, 1844–1851 (2008).

    CAS  Article  Google Scholar 

  19. Harrison, J. S. & Burton, R. S. Tracing coadapted gene complexes to single amino acid substitutions. Mol. Biol. Evol. 23, 559–564 (2006).

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  21. Bikard, D. et al. Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323, 623–626 (2009).

    CAS  Article  Google Scholar 

  22. Masly, J. P., Jones, C. D., Noor, M. A. F., Locke, J. & Orr, H. A. Gene transposition as a novel cause of hybrid male sterility. Science 313, 1448–1450 (2006).

    CAS  Article  Google Scholar 

  23. Lynch, M. & Conery, J. S. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155 (2000).

    CAS  Google Scholar 

  24. Scannell, D., Byrne, K., Gordon, J., Wong, S. & Wolfe, K. Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440, 341–345 (2006).

    CAS  Article  Google Scholar 

  25. Bomblies, K. et al. Autoimmune response as a mechanism for a Dobzhansky–Muller-type incompatibility syndrome in plants. PLoS Biol. 5, e236 (2007).

    Article  Google Scholar 

  26. Bomblies, K. & Weigel, D. Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nature Rev. Genet. 8, 382–393 (2007).

    CAS  Article  Google Scholar 

  27. Bakker, E. G., Toomajian, C., Kreitman, M. & Bergelson, J. A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell 18, 1803–1818 (2006).

    CAS  Article  Google Scholar 

  28. Sawamura, K. & Yamamoto, M.-T. Characterization of a reproductive isolation gene, zygotic hybrid rescue, of Drosophila melanogaster by using minichromosomes. Heredity 79, 97–103 (1997).

    CAS  Article  Google Scholar 

  29. Ferree, P. M. & Barbash, D. A. Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol. 7, e1000234 (2009).

    Article  Google Scholar 

  30. Charlesworth, B., Sniegowski, P. & Stephan, W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371, 215–220 (2002).

    Article  Google Scholar 

  31. Fishman, L. & Saunders, A. Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322, 1559–1562 (2008).

    CAS  Article  Google Scholar 

  32. Henikoff, S., Ahmad, K. & Malik, H. S. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293, 1098–1102 (2001).

    CAS  Article  Google Scholar 

  33. Orr, H. A. & Irving, S. Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura. Genetics 169, 671–682 (2005).

    Article  Google Scholar 

  34. Phadnis, N. & Orr, H. A. A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323, 376–379 (2008).

    Article  Google Scholar 

  35. Tao, Y., Masly, J. P., Araripe, L., Ke, Y. & Hartl, D. L. A sex-ratio meiotic drive system in Drosophila simulan s. I: an autosomal suppressor. PLoS Biol. 5, e292 (2007).

    Article  Google Scholar 

  36. Tao, Y., Hartl, D. L. & Laurie, C. C. Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc. Natl Acad. Sci. USA 98, 13183–13188 (2001).

    CAS  Article  Google Scholar 

  37. Mihola, O., Trachtulec, Z., Vlcek, C., Schimenti, J. C. & Forejt, J. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323, 373–375 (2008).

    Article  Google Scholar 

  38. Tao, Y. et al. A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter. PLoS Biol. 5, e293 (2007).

    Article  Google Scholar 

  39. Meiklejohn, C. D. & Tao, Y. Genetic conflict and sex chromosome evolution. Trends Ecol. Evol.24 Nov 2009 (doi:10.1016/j.tree.2009.10.005).

    Article  Google Scholar 

  40. 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).

    CAS  Article  Google Scholar 

  41. Brideau, N. J. et al. Two Dobzhansky–Muller genes interact to cause hybrid lethality in Drosophila. Science 314, 1292–1295 (2006).

    CAS  Article  Google Scholar 

  42. 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).

    CAS  Article  Google Scholar 

  43. Bayes, J. J. & Malik, H. S. Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326, 1538–1541 (2009).

    CAS  Article  Google Scholar 

  44. Barbash, D. A., Awadalla, P. & Tarone, A. M. Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus. PLoS Biol. 2, 839–848 (2004).

    CAS  Article  Google Scholar 

  45. Tang, S. & Presgraves, D. C. Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science 323, 779–782 (2009).

    CAS  Article  Google Scholar 

  46. Presgraves, D. C., Balagopalan, L., Abmayr, S. M. & Orr, H. A. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423, 715–719 (2003).

    CAS  Article  Google Scholar 

  47. Presgraves, D. C. & Stephan, W. Pervasive adaptive evolution among interactors of the Drosophila hybrid inviability gene, Nup96. Mol. Biol. Evol. 24, 306–314 (2007).

    CAS  Article  Google Scholar 

  48. Presgraves, D. C. Does genetic conflict drive molecular evolution of nuclear transport genes in Drosophila? BioEssays 29, 386–391 (2007).

    CAS  Article  Google Scholar 

  49. Orr, H. A. & Turelli, M. The evolution of postzygotic isolation: accumulating Dobzhansky–Muller incompatibilities. Evolution 55, 1085–1094 (2001).

    CAS  Article  Google Scholar 

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Acknowledgements

I thank C. Meiklejohn and three anonymous reviewers for comments on the manuscript. Work in my laboratory is supported by funds from the US National Institutes of Health, the David & Lucile Packard Foundation, the Alfred P. Sloan Foundation and the University of Rochester.

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Database

Fly Base

Hmr

JYalpha

Lhr

Nup160

Ods

Ovd

tmy

Zhr

Saccharomyces genome Database

OLI1

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Presgraves, D. The molecular evolutionary basis of species formation. Nat Rev Genet 11, 175–180 (2010). https://doi.org/10.1038/nrg2718

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