Expression and modulation of embryonic male-killing in Drosophila innubila: Opportunities for multilevel selection

Evolution

Volumn 59, Issue 4, 2005, Pages 838-848

  Dyer, Kelly A ^a   Minhas, Miranda S ^a   Jaenike, John ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Antibiotic curing; Bacterial density; Quantitative polymerase chain reaction; Sex ratio distortion; Wolbachia

Indexed keywords

BACTERIAL DISEASE; HOST SELECTION; HOST-SYMBIONT INTERACTION; MALE-KILLING; POPULATION DENSITY; POPULATION SIZE; SEX RATIO;

BACTERIA (MICROORGANISMS); DROSOPHILA INNUBILA; WOLBACHIA;

EID: 17844367142     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2005.tb01757.x     Document Type: Article

References (53)

1. Anbutsu, H., and T. Fukatsu. 2003. Population dynamics of male-killing and non-male-killing spiroplasmas in Drosophila melanogaster. Appl. Environ. Micro. 69:1428-1434.
2. Bourtzis, K., A. Nirgianaki, G. Markakis, and C. Savakis. 1996. Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144:1063-1073.
3. Boyle, L., S. L. O'Neill, H. M. Robertson, and T. L. Karr. 1993. Interspecific and intraspecific horizontal transfer of Wolbachia 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. Budar, F., and G. Pelletier. 2001. Male sterility in plants: occurrence, determinism, significance and use. CR. Acad. Sci. Ser. III Sci. Vie 324:543-550.
6. Clancy, D. J., and A. A. Hoffmann. 1998. Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans. Entomol. Exp. Appl. 86:13-24.
7. Clark, M. E., and T. L. Karr. 2002. Distribution of Wolbachia within Drosophila reproductive tissue: implications for the expression of cytoplasmic incompatibility. Integr. Comp. Biol. 42:332-339.
8. Cole, J. R., B. Chai, T. L. Marsh, R. J. Farris, Q. Wang, S. A. Kulam, S. Chandra, D. M. McGarrell, T. M. Schmidt, G. M. Garrity, and J. M. Tiedje. 2003. The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res. 31:442-443.
9. Couvet, D., O. Ronce, and C. Gliddon. 1998. The maintenance of nucleocytoplasmic polymorphism in a metapopulation: the case of gynodioecy. Am. Nat. 152:59-70.
10. Dyer, K. A., and J. Jaenike. 2004. Evolutionarily stable infection by a male-killing endosymbiont in Drosophila innubila: molecular evidence from the host and parasite genomes. Genetics 168:1443-1455.
11. Fisher, R. A. 1930. The genetical theory of natural selection. Oxford Univ. Press, Oxford, U.K.
12. Hanski, I. 1998. Metapopulation dynamics. Nature 396:41-49.
13. Hartl, D. L., and A. G. Clark. 1989. Principles of population genetics. 2nd ed. Sinauer, Sunderland, MA.
14. Hatcher, M. J., D. E. Taneyhill, A. M. Dunn, and C. Tofts. 1999. Population dynamics under parasitic sex ratio distortion. Theor. Popul. Biol. 56:11-18.
15. Heed, W., J. Russell, and D. Harrington. 1962. Diversity and density of Drosophila in the immediate vicinity of Tucson with special reference to D. pseudoobscura. Dros. Inf. Serv. 36:73-74.
16. Hirasawa, M., N. Shouji, T. Neta, K. Fukushima, and K. Takada. 1999. Three kinds of antibacterial substances from Lentinus edodes (Berk.) Sing. (shiitake, an edible mushroom). International Journal of Antimicrobial Agents 11:151-157.
17. Hurst, L. D. 1991. The incidences and evolution of cytoplasmic male killers. Proc. R. Soc. Lond. B 244:91-99.
18. Hurst, G. D. D., and F. M. Jiggins. 2000. Male-killing bacteria in insects: mechanisms, incidence, and implications. Emer. Inf. Dis. 6:329-336.
19. Hurst, G. D. D., E. L. Purvis, J. J. Slogett, and M. E. N. Majerus. 1994. The effect of infection with male-killing Rickettsia on the demography of female Adalia bipunctata L. (two-spot ladybird). Heredity 73:309-316.
20. Hurst, G. D. D., A. P. Johnson, J. H. G. von der Schulenburg, and Y. Fuyama. 2000. Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 156:699-709.
21. Hurst, G. D. D., F. M. Jiggins, and S. J. W. Robinson. 2001. What causes inefficient transmission of male-killing Wolbachia in Drosophila? Heredity 87:220-226.
22. Ijichi, N., N. Kondo, R. Matsumoto, M. Shimada, H. Ishikawa, and T. Fukatsu. 2002. Internal spatiotemporal population dynamics of infection with three Wolbachia strains in the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). Appl. Env. Micro. 68:4074-4080.
23. Ikeda, H. 1970. The cytoplasmically-inherited 'sex-ratio' condition in natural and experimental populations of Drosophila bifasciata. Genetics 65:311-333.
24. Jaenike, J. 2001. Sex chromosome meiotic drive. Annu. Rev. Ecol. Syst. 32:25-49.
25. Jaenike, J., K. A. Dyer, and L. K. Reed. 2003. Within-population structure of competition and the dynamics of male-killing Wolbachia. Evol. Ecol. Res. 5:1023-1036.
26. Jiggins, F. M., J. K. Bentley, M. E. N. Majerus, and G. D. D. Hurst. 2002. Recent changes in phenotype and patterns of host specializaton in Wolbachia bacteria. Mol. Ecol. 11:1275-1283.
27. Lowe, C. H. 1964. Arizona's natural environment: landscapes and habitats. Univ. of Arizona Press, Tucson.
28. Majerus, M. E. N. 2003. Sex wars: genes, bacteria, and biased sex ratios. Princeton Univ. Press, Princeton, NJ.
29. Manicacci, D., D. Couvet, E. Belhassen, P. H. Gouyon, and A. Atlan. 1996. Founder effects and sex ratio in the gynodioecious Thymus vulgarisL. Mol. Ecol. 5:63-72.
30. McCauley, D. E., M. S. Olson, S. N. Emery, and D. R. Taylor. 2000. Population structure influences sex ratio evolution in a gynodioecious plant. Am. Nat. 155:814-819.
31. McGraw, E. A., D. J. Merritt, J. N. Droller, and S. L. O'Neill. 2002. Wolbachia density and virulence attenuation after transfer into a novel host. Proc. Natl. Acad. Sci. USA 99:2918-2923.
32. Miller, S. G., B. C. Campbell, J. Becnel, and L. Ehrman. 1995. Bacterial entomopathogens from the Drosophila paulistorum species complex. J. Invert. Pathol. 65:125-131.
33. Normark, B. B. 2004. Haplodiploidy as an outcome of coevolution between male-killing cytoplasmic elements and their hosts. Evolution 58:790-798.
34. Ohta, T. 1973. Slightly deleterious mutant substitutions in evolution. Nature 246:96-98.
35. O'Neill, S. L., and T. L. Karr. 1990. Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348:178-180.
36. Patterson, J. T., and R. R. Wagner. 1943. Geographical distribution of species of the genus Drosophila in the United States and Mexico. University of Texas Publications 4313:217-281.
37. Pidiyar, V. J., K. Jangid, M. S. Patole, and Y. S. Shouche. 2004. Studies on cultured and uncultured microbiota of wild Culex quinquefasciatus midgut based on 16S ribosomal gene analysis. Am. J. Trip. Med. Hyg. 70:597-603.
38. Rispe, C., and N. A. Moran. 2000. Accumulation of deleterious mutations in endosymbionts: Muller's rachet with two levels of selection. Am. Nat. 156:425-441.
39. Rosa, L. H., K. M. G. Machado, C. G. Jacob, M. Capelari, C. A. Rosa, and C. L. Zani. 2003. Screening of Brazilian basidiomycetes for antimicrobial activity. Mem. Inst. Oswaldo Cruz 98:967-974.
40. Roughgarden, J. 1971. Density-dependent natural selection. Ecology 52:453-468.
41. Schramm, A., S. K. Davidson, J. A. Dodsworth, H. L. Drake, D. A. Stahl, and N. Dubilier. 2003. Acidovorax-like symbionts in the nephridia of earthworms. Environ. Micro. 5:804-809.
42. Stevens, L., and D. T. Wicklow. 1992. Multispecies interactions affect cytoplasmic incompatibility in Tribolium flour beetles. Am Nat 140:642-653.
43. Stouthamer, R., J. A. J. Breeuwer, and G. D. D. Hurst. 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53:71-102.
44. Suay, I., F. Arenal, F. J. Asensio, A. Basilio, M. C. Cabello, M. T. Diez, J. B. Garcia, A. G. del Val, J. Gorrochategui, P. Hernandez, F. Pelaez, M. Francisca Vicente. 2000. Screening of basidiomycetes for antimicrobial activities. Antonie Leeuwenkoek Int. J. Gen. Mol. Microbiol. 78:129-139.
45. Taylor, D. R., M. S. Olson, and D. E. McCauley. 2001. A quantitative genetic analysis of nuclear-cytoplasmic male sterility in structured populations of Silene vulgaris. Genetics 158:833-841.
46. Tompkins, D. M., and M. Begon. 1999. Parasites can regulate wildlife populations. Parasitol. Today 15:311-313.
47. Wallace, B. 1968. Topics in population genetics. Norton, New York.
48. Weisburg, W. W., S. M. Barns, D. A. Pelletier, and D. J. Lane. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697-703.
49. Welkos, S., and A. O'Brien. 1994. Determination of median lethal and infectious doses in animal-model systems. Method Enzymol. 235:29-39.
50. Werren, J. H. 1987. The coevolution of autosomal and cytoplasmic sex ratio factors. J. Theor. Biol. 124:317-334.
51. Wernegreen, J. J. 2002. Genome evolution in bacterial endosymbionts of insects. Nat. Rev. Genet. 3:850-861.
52. Zchori-Fein, E., Y. Gottlieb, and M. Coll. 2000. Wolbachia density and host fitness components in Muscidifurax uniraptor (Hymenoptera: Pteromalidae). J. Invert. Pathol. 75:267-272.
53. Zhou, W., F. Rousset, and S. O'Neill. 1998. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc. R. Soc. Lond. B 265:509-515.