Abstract
In haplodiploid species, Wolbachia-induced cytoplasmic incompatibility (CI) can be expressed in one of two ways: as a "conversion" of diploid fertilized eggs into haploid males or as embryonic mortality. Here we describe CI-type variation within the parasitic wasp genus Nasonia and genetically analyze the basis of this variation. We reach four main conclusions: (i) CI is expressed primarily as conversion in N. vitripennis, but as embryonic mortality in the sibling species N. giraulti and N. longicornis; (ii) the difference in CI type between N. giraulti (mortality) and N. vitripennis (conversion) is determined by host nuclear genotype rather than by Wolbachia differences; (iii) N. vitripennis "conversion genes" are recessive in hybrid females; and (iv) a difference in CI level between the sibling species N. giraulti and N. longicornis is due to the different Wolbachia infections in the species rather than to the host genotype. These results show that host nuclear genes can influence the type of CI present in a species. On the basis of these findings, we propose a model for how different CI types evolve in haplodiploids due to selection on nuclear genes modifying CI.
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- Bordenstein S. R., O'Hara F. P., Werren J. H. Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature. 2001 Feb 8;409(6821):707–710. doi: 10.1038/35055543. [DOI] [PubMed] [Google Scholar]
- Bordenstein S. R., Werren J. H. Effects of A and B Wolbachia and host genotype on interspecies cytoplasmic incompatibility in Nasonia. Genetics. 1998 Apr;148(4):1833–1844. doi: 10.1093/genetics/148.4.1833. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boyle L., O'Neill S. L., Robertson H. M., Karr T. L. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science. 1993 Jun 18;260(5115):1796–1799. doi: 10.1126/science.8511587. [DOI] [PubMed] [Google Scholar]
- Breeuwer J. A., Werren J. H. Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics. 1993 Oct;135(2):565–574. doi: 10.1093/genetics/135.2.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Breeuwer J. A., Werren J. H. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature. 1990 Aug 9;346(6284):558–560. doi: 10.1038/346558a0. [DOI] [PubMed] [Google Scholar]
- Campbell B. C., Steffen-Campbell J. D., Werren J. H. Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer (ITS2) and 28S rDNA sequences. Insect Mol Biol. 1993;2(4):225–237. doi: 10.1111/j.1365-2583.1994.tb00142.x. [DOI] [PubMed] [Google Scholar]
- Fujii Y., Kageyama D., Hoshizaki S., Ishikawa H., Sasaki T. Transfection of Wolbachia in Lepidoptera: the feminizer of the adzuki bean borer Ostrinia scapulalis causes male killing in the Mediterranean flour moth Ephestia kuehniella. Proc Biol Sci. 2001 Apr 22;268(1469):855–859. doi: 10.1098/rspb.2001.1593. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoffmann A. A., Turelli M. Unidirectional incompatibility in Drosophila simulans: inheritance, geographic variation and fitness effects. Genetics. 1988 Jun;119(2):435–444. doi: 10.1093/genetics/119.2.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hurst G. D., Jiggins F. M. Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Dis. 2000 Jul-Aug;6(4):329–336. doi: 10.3201/eid0604.000402. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karr T. L. Paternal investment and intracellular sperm-egg interactions during and following fertilization in Drosophila. Curr Top Dev Biol. 1996;34:89–115. doi: 10.1016/s0070-2153(08)60709-7. [DOI] [PubMed] [Google Scholar]
- LAVEN H. Speciation by cytoplasmic isolation in the Culex pipiens-complex. Cold Spring Harb Symp Quant Biol. 1959;24:166–173. doi: 10.1101/sqb.1959.024.01.017. [DOI] [PubMed] [Google Scholar]
- McGraw E. A., Merritt D. J., Droller J. N., O'Neill S. L. Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila. Proc Biol Sci. 2001 Dec 22;268(1485):2565–2570. doi: 10.1098/rspb.2001.1839. [DOI] [PMC free article] [PubMed] [Google Scholar]
- O'Neill S. L., Karr T. L. Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature. 1990 Nov 8;348(6297):178–180. doi: 10.1038/348178a0. [DOI] [PubMed] [Google Scholar]
- 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. 1996 Jun;143(2):961–972. doi: 10.1093/genetics/143.2.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Poccia D., Collas P. Transforming sperm nuclei into male pronuclei in vivo and in vitro. Curr Top Dev Biol. 1996;34:25–88. doi: 10.1016/s0070-2153(08)60708-5. [DOI] [PubMed] [Google Scholar]
- 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. 1995 Apr;40(4):408–418. doi: 10.1002/mrd.1080400404. [DOI] [PubMed] [Google Scholar]
- Ryan S. L., Saul G. B., 2nd, Conner G. W. Aberrant segregation of R-locus genes in male progeny from incompatible crosses in Mormoniella. J Hered. 1985 Jan-Feb;76(1):21–26. doi: 10.1093/oxfordjournals.jhered.a110011. [DOI] [PubMed] [Google Scholar]
- Ryan S. L., Saul G. B., 2nd Post-fertilization effect of incompatibility factors in Mormoniella. Mol Gen Genet. 1968;103(1):29–36. doi: 10.1007/BF00271154. [DOI] [PubMed] [Google Scholar]
- Stouthamer R., Breeuwer J. A., Hurst G. D. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol. 1999;53:71–102. doi: 10.1146/annurev.micro.53.1.71. [DOI] [PubMed] [Google Scholar]
- Stouthamer R., Breeuwert J. A., Luck R. F., Werren J. H. Molecular identification of microorganisms associated with parthenogenesis. Nature. 1993 Jan 7;361(6407):66–68. doi: 10.1038/361066a0. [DOI] [PubMed] [Google Scholar]
- Turelli M., Hoffmann A. A. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature. 1991 Oct 3;353(6343):440–442. doi: 10.1038/353440a0. [DOI] [PubMed] [Google Scholar]
- Vavre F., Fleury F., Varaldi J., Fouillet P., Boulétreau M. Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences. Evolution. 2000 Feb;54(1):191–200. doi: 10.1111/j.0014-3820.2000.tb00019.x. [DOI] [PubMed] [Google Scholar]
- Wade M. J., Stevens L. Microorganism mediated reproductive isolation in flour beetles (genus Tribolium). Science. 1985 Feb 1;227(4686):527–528. doi: 10.1126/science.3966160. [DOI] [PubMed] [Google Scholar]
- Weeks A. R., Breeuwer J. A. Wolbachia-induced parthenogenesis in a genus of phytophagous mites. Proc Biol Sci. 2001 Nov 7;268(1482):2245–2251. doi: 10.1098/rspb.2001.1797. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Werren J. H., Bartos J. D. Recombination in Wolbachia. Curr Biol. 2001 Mar 20;11(6):431–435. doi: 10.1016/s0960-9822(01)00101-4. [DOI] [PubMed] [Google Scholar]
- Werren J. H. Biology of Wolbachia. Annu Rev Entomol. 1997;42:587–609. doi: 10.1146/annurev.ento.42.1.587. [DOI] [PubMed] [Google Scholar]
- Yen J. H., Barr A. R. New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature. 1971 Aug 27;232(5313):657–658. doi: 10.1038/232657a0. [DOI] [PubMed] [Google Scholar]
- Zhou W., Rousset F., O'Neil S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci. 1998 Mar 22;265(1395):509–515. doi: 10.1098/rspb.1998.0324. [DOI] [PMC free article] [PubMed] [Google Scholar]