Abstract
MICROORGANISMS have been implicated in causing cytoplasmic incompatibility in a variety of insect species, including mosquitoes, fruitflies, beetles and wasps1–17. The effect is typically unidirectional: incompatible crosses produce no progeny1–11 or sterile males12–14, whereas the reciprocal crosses produce normal progeny. The parasitic wasp Nasonia vitripennis is one of the few species in which the cytogenetic mechanism of incompatibility is known. In this species the paternal chromosome set forms a tangled mass in a fertilized egg and is eventually lost16. Here we report that cytoplasmic microorganisms are associated with complete bidirectional incompatibility between N. vitripennis and a closely related sympatric species, N. giraulti. Microorganisms can be seen in the eggs of both species. Hybrid offspring are normally not produced in crosses between the two species, but do occur after elimination of the microorganisms by antibiotic treatment. A cytogenetic and genetic study shows that bidirectional interspecific incompatibility is due to improper condensation of the paternal chromosomes. Microorganism-mediated reproductive isolation is of interest because it could provide a rapid mode of speciation18,19. The mechanism of incompatibility in Nasonia is also of interest as a potential tool for studying chromosome imprinting and chromosome condensation.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
A Margulian View of Symbiosis and Speciation: the Nasonia Wasp System
Symbiosis Open Access 24 May 2022
-
Crystal Structures of Wolbachia CidA and CidB Reveal Determinants of Bacteria-induced Cytoplasmic Incompatibility and Rescue
Nature Communications Open Access 25 March 2022
-
The emergence of ecotypes in a parasitoid wasp: a case of incipient sympatric speciation in Hymenoptera?
BMC Ecology and Evolution Open Access 15 November 2021
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Get just this article for as long as you need it
$39.95
Prices may be subject to local taxes which are calculated during checkout
References
Hoffman, A. A., Turelli, M. & Simmons, G. M. Evolution 40, 692–701 (1986).
Hoffman, A. A. Entomol. Exp. Appl. 48, 61–67 (1988).
Hsiao, T. H. & Hsiao, C. Entomol. Exp. Appl. 37, 155–159 (1985).
Wade, M. J. & Stevens, L. Science 227, 527–528 (1989).
Binnington, K. C. & Hoffmann, A. A. J. invert Pathol. 54, 344–352 (1989).
Trpis, M., Perrone, J. B., Reissig, M. & Parker, K. L. J. Hered. 72, 313–317 (1981).
Yen, J. H. & Barr, A. R. Nature 232, 657–658 (1971).
Hsiao, T. H. & Hsiao, C. J. invert. Pathol. 45, 244–246 (1985).
O'Neill, S. L. J. invert. Pathol. 53, 132–134 (1989).
Yen, J. H. & Barr, A. R. J. invert. Pathol. 22, 242–250 (1973).
Kellen, W. R., Hoffman, D. F. & Kwock, R. A. J. invert. Pathol. 37, 273–283 (1981).
Dobzhansky, T. & Paulovsky, O. Genetics 55, 141–156 (1967).
Ehrman, L. & Kernaghan, R. P. J. Hered. 62, 67–71 (1971).
Williamson, D. L., Ehrman, L. & Kernaghan, R. P. Proc. natn. Acad. Sci. U.S.A 68, 2158–2160 (1971).
Richardson, P. M., Holmes, W. P. & Saul II, G. B. J. invert. Pathol. 50, 176–183 (1987).
Ryan, S. L. & Saul II, G. B. Molec. gen. Genet. 103, 29–36 (1968).
Conner, G. W. & Saul II, G. B. J. Hered. 77, 211–213 (1986).
Laven, H., Wright, J. W. & Pal, R. in Genetics of Insect Vectors of Diseases (Elsevier, Amsterdam, 1967).
Thompson, J. N. Biol. J. Linn. Soc. 32, 385–393 (1987).
Whiting, A. R. Q. Rev. Biol. 42, 333–406 (1967).
Werren, J. H. Evolution 37, 116–124 (1983).
Darling, D. C. & Werren, J. H. Ann. Entomol. Soc. Amer. 83, 352–370 (1990).
Werren, J. H., Nur, U. & Eickbush, D. Nature 327, 75–76 (1987).
Caspari, E. & Watson, G. S. Evolution 13, 568–570 (1959).
Laven, H. Z. Vererbungslehre 88, 478–516 (1957).
Subbarao, S. K., Krishnamurthy, B. S., Curtis, C. F., Adak, T. & Chandrahas, R. K. Genetics 87, 381–390 (1977).
Nur, U., Werren, J. H., Eickbush, D. G., Burke, W. B. & Eickbush, T. H. Science 240, 512–514 (1988).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Breeuwer, J., Werren, J. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346, 558–560 (1990). https://doi.org/10.1038/346558a0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/346558a0
This article is cited by
-
Quality over quantity: unraveling the contributions to cytoplasmic incompatibility caused by two coinfecting Cardinium symbionts
Heredity (2022)
-
Crystal Structures of Wolbachia CidA and CidB Reveal Determinants of Bacteria-induced Cytoplasmic Incompatibility and Rescue
Nature Communications (2022)
-
Environmental Temperature, but Not Male Age, Affects Wolbachia and Prophage WO Thereby Modulating Cytoplasmic Incompatibility in the Parasitoid Wasp, Habrobracon Hebetor
Microbial Ecology (2022)
-
A Margulian View of Symbiosis and Speciation: the Nasonia Wasp System
Symbiosis (2022)
-
The high Wolbachia infection does not drive Tetrapedia diversipes (Hymenoptera: Apidae) sex bias and population genetic structure
Apidologie (2022)
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.
