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Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia

Abstract

Wolbachia are cytoplasmically inherited bacteria that cause a number of reproductive alterations in insects, including cytoplasmic incompatibility1,2, an incompatibility between sperm and egg that results in loss of sperm chromosomes following fertilization. Wolbachia are estimated to infect 15–20% of all insect species3, and also are common in arachnids, isopods and nematodes3,4. Therefore, Wolbachia-induced cytoplasmic incompatibility could be an important factor promoting rapid speciation in invertebrates5, although this contention is controversial6,7. Here we show that high levels of bidirectional cytoplasmic incompatibility between two closely related species of insects (the parasitic wasps Nasonia giraulti and Nasonia longicornis) preceded the evolution of other postmating reproductive barriers. The presence of Wolbachia severely reduces the frequency of hybrid offspring in interspecies crosses. However, antibiotic curing of the insects results in production of hybrids. Furthermore, F1 and F2 hybrids are completely viable and fertile, indicating the absence of F1 and F2 hybrid breakdown. Partial interspecific sexual isolation occurs, yet it is asymmetric and incomplete. Our results indicate that Wolbachia-induced reproductive isolation occurred in the early stages of speciation in this system, before the evolution of other postmating isolating mechanisms (for example, hybrid inviability and hybrid sterility).

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Figure 1: Number of hybrid (female) offspring produced from intra- and interspecific crosses.
Figure 2: F2 egg and adult offspring number produced from F1 hybrid and non-hybrid females.

References

  1. Werren, J. H. Biology of Wolbachia. Annu. Rev. Entomol. 423, 587–609 (1997).

    Article  Google Scholar 

  2. Hoffmann, A. A. & Turelli, M. in Influential Passengers (eds O'Neill, S. L. Hoffmann, A. A. & Werren, J. H.) (Oxford Univ. Press, New York, 1997).

    Google Scholar 

  3. Werren, J. H. & Windsor, D. M. Wolbachia infection frequencies in insects: evidence of a global equilibrium. Proc. R. Soc. Lond. B 267, 1277–1285 (2000).

    CAS  Article  Google Scholar 

  4. Werren, J. H., Windsor, D. & Guo, L. R. Distribution of Wolbachia among neotropical arthropods. Proc. R. Soc. Lond. B 262, 197–204 (2000).

    ADS  Google Scholar 

  5. Werren, J. H. in Endless Forms: Species and Speciation (eds Howard, D. J. & Berlocher, S. L.) (Oxford Univ. Press, Oxford, 1998).

    Google Scholar 

  6. Hurst, G. D. D. & Schilthuizen, M. Selfish genetic elements and speciation. Heredity 80, 2–8 (1998).

    Article  Google Scholar 

  7. Stouthamer, R., Breeuwer, J. A. J. & Hurst, G. D. D. Wolbachia pipientis: Microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53, 71–102 (1999).

    CAS  Article  PubMed  Google Scholar 

  8. Margulis, L. & Fester, R. Symbiosis as a Source of Evolutionary Innovation (MIT Press, Cambridge, Massachusetts, 1991).

    Google Scholar 

  9. Shoemaker, D. D., Katju, V. & Jaenike, J. Wolbachia and the evolution of reproductive isolation between Drosophila recens and Drosophila subquinaria. Evolution 53, 1157–1164 (1999).

    Article  PubMed  Google Scholar 

  10. Wade, M. J., Chang, N. W. & McNaughton, M. Incipient speciation in the flour beetle Tribolium confusum: partial reproductive isolation between populations. Heredity 75, 453–459 (1995).

    Article  PubMed  Google Scholar 

  11. Breeuwer, J. A. J. & Werren, J. H. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346, 558–560 (1990).

    ADS  CAS  Article  PubMed  Google Scholar 

  12. Darling, C. D. & Werren, J. H. Biosystematics of two new species of Nasonia (Hymenoptera: Pteromalidae) reared from birds’ nests in North America. Annals Enton. Soc. Amer. 83, 352–370 (1990).

    Article  Google Scholar 

  13. Campbell, B. C., Steffen-Campbell, J. D. & Werren, J. H. Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an rDNA internal transcribed spacer (ITS2). Insect Mol. Biol. 2, 255–237 (1993).

    Google Scholar 

  14. Werren, J. H., Zhang, W. & Guo, L. R. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc. R. Soc. Lond. B 251, 55–71 (1995).

    ADS  Google Scholar 

  15. Breeuwer, J. A. J. & Werren, J. H. Hybrid breakdown between two haplodiploid species: the role of nuclear and cytoplasmic genes. Evolution 49, 705–717 (1995).

    Article  PubMed  Google Scholar 

  16. Bordenstein, S. R. & Werren, J. H. Effects of A and B Wolbachia and host genotype on interspecies cytoplasmic incompatibility in Nasonia. Genetics 148, 1833–1844 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Perrot-Minnot, M. J., Guo, L. R. & Werren, J. H. Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis: effects on compatibility. Genetics 143, 961–972 (1996)

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Zhou, W. G., Rousset, F. & O'Neill, S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc. R. Soc. Lond. B 265, 509–515 (1998).

    CAS  Article  Google Scholar 

  19. Reed, K. M. & Werren, J. H. Induction of paternal genome loss by the paternal-sex-ratio chromosome and cytoplasmic incompatibility bacteria (Wolbachia): a comparative study of early embryonic events. Mol. Reprod. Dev. 40, 408–418 (1995).

    CAS  Article  PubMed  Google Scholar 

  20. Wu, C. I. & Palopoli, M. F. Genetics of postmating reproductive isolation in animals. Annu. Rev. Genet. 28, 283–308 (1994).

    CAS  Article  PubMed  Google Scholar 

  21. Orr, H. A. Haldane's rule. Annu. Rev. Ecol. Syst. 28, 195–218 (1997).

    Article  Google Scholar 

  22. Gadau, J., Page R. E. & Werren, J. H. Mapping of hybrid incompatibility loci in Nasonia. Genetics 153, 1731–1741 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Mood, A. M., Graybill, F. A. & Boes, D. C. Introduction to the Theory of Statistics (McGraw Hill, Singapore, 1974).

    MATH  Google Scholar 

  24. Palopoli, M. F. & Wu, C. I. Genetics of hybrid male sterility between Drosophila sibling species—a complex web of epistasis is revealed in interspecific studies. Genetics 138, 329–341 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. True, J. R., Weir, B. S. & Laurie, C. C. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 142, 819–837 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Noor, M. A. F. Genetics of sexual isolation and courtship dysfunction in male hybrids of Drosophila pseudoobscura and Drosophila persimilis. Evolution 51, 809–815 (1997).

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank R. Billings, M. Vaughn and B. J. Velthuis for technical assistance, and J. Bartos, A. Betancourt, J. Jaenike, J. P. Masly, T. van Opijnen and D. Presgraves for critical reading of the manuscript. This work was supported by the NSF (J.H.W.).

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Correspondence to Seth R. Bordenstein.

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Bordenstein, S., O'Hara, F. & Werren, J. Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409, 707–710 (2001). https://doi.org/10.1038/35055543

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