Evolution of incompatibility-inducing microbes in subdivided host populations

Evolution

Volumn 63, Issue 2, 2009, Pages 432-447

  Haygood, Ralph ^a,b   Turelli, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

Clade selection; Kin selection; Modifier evolution; Spite; Symbiont evolution; Wolbachia

Indexed keywords

BACTERIUM; DEMOGRAPHY; EGG; EVOLUTIONARY BIOLOGY; FECUNDITY; HOST; KIN SELECTION; POPULATION DENSITY; SYMBIOSIS;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CYTOLOGY; EVOLUTION; EXTRACHROMOSOMAL INHERITANCE; FEMALE; FERTILITY; INSECT; MALE; MICROBIOLOGY; PHYSIOLOGY; SEXUAL DEVELOPMENT; STATISTICAL MODEL; SYMBIOSIS;

ANIMALS; EVOLUTION; EXTRACHROMOSOMAL INHERITANCE; FEMALE; FERTILITY; INSECTS; MALE; MODELS, BIOLOGICAL; MODELS, STATISTICAL; SEX CHARACTERISTICS; SYMBIOSIS;

ARTHROPODA; BACTERIA (MICROORGANISMS); HEXAPODA; NEMATODA; WOLBACHIA;

EID: 58849163129     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00550.x     Document Type: Article

References (61)

1. Ballard, J. W. O. 2004. Sequential evolution of a symbiont inferred from the host: Wolbachia and Drosophila simulans. Mol. Biol. Evol. 21 : 428 442.
2. Bourtzis, K., S. L. Dobson, H. R. Braig, and S. L. O'Neill. 1998. Rescuing Wolbachia have been overlooked. Nature 391 : 852 853.
3. Boyle, L., S. L. O'Neill, H. Robertson, H., and T. L. Karr. 1993. Horizontal transfer of Wolbachia pipientis by microinjection of egg cytoplasm: infection levels and the expression of cytoplasmic incompatibility in Drosophila. Science 260 : 1796 1799.
4. Breeuwer, J. A. J., and J. H. Werren. 1993. Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics 135 : 565 574.
5. Burt, A., and R. Trivers. 2006. Genes in conflict. Belknap Press, Cambridge, MA.
6. Caspari, E., and G. S. Watson. 1959. On the evolutionary importance of cytoplasmic sterility in mosquitoes. Evolution 13 : 568 570.
7. Charlat, S., C. Calmet, and H. Merçot. 2001. On the mod resc model and the evolution of Wolbachia incompatibility types. Genetics 159 : 1415 1422.
8. Charlat, S., A. Nirgianaki, K. Bourtzis, and H. Merçot. 2002. Evolution of Wolbachia-induced cytoplasmic incompatibility in Drosophila simulans and D. sechellia. Evolution 59 : 1735 1742.
9. Champion de Crespigny, F. E., and N. Wedell. 2007. Mate preferences in Drosophila infected with Wolbachia. Behav. Ecol. Sociobiol. 61 : 1229 1235.
10. Christiansen, F. B. 1975. Hard and soft selection in a subdivided population. Am. Nat. 109 : 11 16.
11. Clancy, D. J., and A. A. Hoffmann. 1998. Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans. Ent. Exp. Appl. 86 : 13 24.
12. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer Associates, Sunderland, MA.
13. Coyne, J. A., N. H. Barton, and M. Turelli. 2000. Is Wright's shifting balance process important in evolution? Evolution 54 : 306 317.
14. Dedeine, F., F. Vavre, D. D. Shoemaker, and M. Boulétreau. 2004. Intra-individual coexistence of a Wolbachia strain required for host oogenesis with two strains inducing cytoplasmic incompatibility in the wasp Asobara tabida. Evolution 58 : 2167 2174.
15. Dobson, S. L., E. J. Marsland, and W. Rattanadechakul. 2002. Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160 : 1087 1094.
16. Engelstädter, J. and S. Charlat. 2006. Outbreeding selects for spiteful cytoplasmic elements. Proc. R. Soc. Lond. B 273 : 923 929.
17. Engelstädter, J., S. Charlat, A. Pomiankowski, and G. D. D. Hurst. 2006. The evolution of cytoplasmic incompatibility types: integrating segregation, inbreeding and outbreeding. Genetics 172 : 2601 2611.
18. Fine, P. E. M. 1978. On the dynamics of symbiote-dependent cytoplasmic incompatibility in Culicine mosquitoes. J. Invert. Pathol. 30 : 10 18.
19. Frank, S. A. 1997. Cytoplasmic incompatibility and population structure. J. Theor. Biol. 184 : 327 330.
20. Frank, S. A. 1998. Foundations of social evolution. Princeton Univ. Press, Princeton, NJ.
21. Gardner, A., and S. A. West. 2004. Spite and the scale of competition. J. Evol. Biol. 17 : 1195 1203.
22. Guillemaud, T., and F. Rousset. 1997. Consequences of Wolbachia transmission process on the infection dynamics. J. Evol. Biol. 10 : 601 612.
23. Hamilton, W. D. 1970. Selfish and spiteful behaviour in an evolutionary model. Nature 228 : 1218 1220.
24. Hoerauf, A., K. Nissen-Pahle, C. Schmetz, K. Henkle-Duhrsen, M. L. Blaxter, et al. 1999. Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J. Clin. Invest. 103 : 11 17.
25. Hoffmann, A. A., and K. M. Nielsen. 1985. The effect of resource subdivision on genetic variation in Drosophila. Am. Nat. 125 : 421 430.
26. Hoffmann, A. A., and M. Turelli. 1997. Cytoplasmic incompatibility in insects. Pp. 42 80 in S. L. O'Neill, A. A. Hoffmann and J. H. Werren, eds. Influential passengers. Oxford Univ. Press, Oxford, UK.
27. Hoffmann, A. A., M. Turelli, and L. G. Harshman. 1990. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126 : 933 948.
28. Hoffmann, A. A., D. J. Clancy, and E. Merton. 1994. Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics 136 : 993 999.
29. Hoffmann, A. A., M. Hercus, and H. Dagher. 1998. Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster. Genetics 148 : 221 231.
30. Hornett, E. A., S. Charlat, A. M. R. Duplouy, N. Davies, G. K. Roderick, N. Wedell, and G. D. D. Hurst. 2006. Evolution of male-killer suppression in a natural population. PLoS Biol. 4 : 1643 1648.
31. Hurst, L. D. 1991. The evolution of cytoplasmic incompatibility or when spite can be successful. J. Theor. Biol. 148 : 269 277.
32. Hurst, L. D., and G. T. McVean. 1996. Clade selection, reversible evolution and the persistence of selfish elements: the evolutionary dynamics of cytoplasmic incompatibility. Proc. R. Soc. Lond. B 263 : 97 104.
33. Hurst, G. D. D., L. D. Hurst, and M. E. N. Majerus. 1992. Selfish genes move sideways. Nature 356 : 659 660.
34. Jansen, V. A. A., M. Turelli, and H. C. J. Godfray. 2008. Stochastic spread of Wolbachia. Proc. R. Soc. Lond. B 275 : 2769 2776.
35. Laven, H. 1959. Speciation by cytoplasmic isolation in the Culex pipiens complex. Cold Spring Harb. Symp. Quant. Biol. 24 : 166 173.
36. Mateos, M., S. J. Castrezana, B. J. Nankivell, A. M. Estes, T. A. Markow, and N. A. Moran. 2006. Heritable endosymbionts of Drosophila. Genetics 174 : 363 376.
37. Merçot, H., and D. Poinsot. 1998. [Rescuing Wolbachia have been] discovered on Mount Kilimanjaro. Nature 391 : 853.
38. Montchamp-Moreau, C., J.-F. Ferveur, and M. Jacques. 1991. Geographic distribution and inheritance of three cytoplasmic incompatibility types in Drosophila simulans. Genetics 129 : 399 407.
39. Nigro, L., and T. Prout. 1990. Is there selection on RFLP differences in mitochondrial DNA? Genetics 125 : 551 556.
40. O'Neill, S. L., and T. L. Karr. 1990. Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348 : 178 180.
41. O'Neill, S. L., R. Giordano, A. M. E. Colbert, T. L. Karr, and H. M. Robertson. 1992. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl. Acad. Sci. USA 89 : 2699 2702.
42. Pannebakker, B. A., B. Loppin, C. P. H. Elemans, L. Humbolt, and F. Vavre. 2007. Parasitic inhibition of cell death facilitates symbiosis. Proc. Natl. Acad. Sci. USA 104 : 213 215.
43. Prout, T. 1994. Some evolutionary possibilities for a microbe that causes incompatibility in its host. Evolution 48 : 909 911.
44. Rasgon, J. L., and T. W. Scott. 2003. Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: parameter estimates and infection dynamics in natural populations. Genetics 165 : 2029 2038.
45. Rasgon, J. L., and T. W. Scott. 2004. Impact of population age structure on Wolbachia transgene driver efficacy: ecologically complex factors and release of genetically modified mosquitoes. Insect Biochem. Mol. Biol. 34 : 707 713.
46. Rasgon, J. L., L. M. Styer, and T. W. Scott. 2003. Wolbachia-induced mortality as a mechanism to modulate pathogen transmission by vector arthropods. J. Med. Entomol. 40 : 125 132.
47. Reuter, M., L. Lehmann, and F. Guillaume. 2008. The spread of incompatibility-inducing parasites in sub-divided host populations. BMC Evol. Biol. 8 : 134.
48. Rousset, F., and M. Raymond. 1991. Cytoplasmic incompatibility in insects: why sterilize females? Trends Ecol. Evol. 6 : 54 57.
49. Stevens, L., and D. T. Wicklow. 1992. Multi-species interactions affect cytoplasmic incompatibility in Tribolium flour beetles. Am. Nat. 140 : 642 653.
50. Turelli, M. 1994. Evolution of incompatibility-inducing microbes and their hosts. Evolution 48 : 1500 1513.
51. Turelli, M., and A. A. Hoffmann. 1991. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353 : 440 442.
52. Turelli, M., and A. A. Hoffmann. 1995. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140 : 1319 1338.
53. Turelli, M., A. A. Hoffmann, and S. W. McKechnie. 1992. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics 132 : 713 723.
54. Vavre, F., F. Fleury, D. Lepetit, P. Fouillet, and M. Boulétreau. 1999. Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol. Biol. Evol. 16 : 1711 1723.
55. Wade, M. J., and L. Stevens. 1994. The effect of population subdivision on the rate of spread of parasite-mediated cytoplasmic incompatibility. J. Theor. Biol. 167 : 81 87.
56. Weeks, A. R., K. T. Reynolds, and A. A. Hoffmann. 2002. Wolbachia dynamics and host effects: what has (and has not) been demonstrated? Trends. Ecol. Evol. 17 : 257 262.
57. Weeks, A. R., M. Turelli, W. R. Harcombe, K. T. Reynolds, and A. A. Hoffmann. 2007. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 5 : 997 1005.
58. Werren, J. H. 1983. Sex ratio evolution under local mate competition in a parasitic wasp. Evolution 37 : 116 124.
59. Werren, J. H. 1997. Biology of Wolbachia. Ann. Rev. Entomology 42 : 587 609.
60. Zabalou, S., A. Apostolaki, S. Pattas, Z. Veneti, C. Paraskevopoulos, I. Livadaras, G. Markakis, T. Brissac, H. Merçot, and K. Bourtzis. 2008. Multiple rescue factors within a Wolbachia strain. Genetics 178 : 2145 2160.
61. Zchori-Fein, E., and S. J. Perlman. 2004. Distribution of the bacterial symbiont Cardinium in arthropods. Mol. Ecol. 13 : 2009 2016.