Cytoplasmic incompatability in Drosophila melanogaster due to different Wolbachia genotypes



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Abstract

Wolbachia is an endosymbiont prevalent among different arthropoda and in some Nematoda species. The bacteria ads across the populations of host species via induction of reproductive abnormalities: cytoplasmic incompatability, parthenogenesis, feminization, and male killing. we estimated the level of cytoplasmic incompatability in Drosophila melanogaster caused by three most prevalent Wolbachia genotypes, namely wmel, wmelCS и wmelCS2. wmel and wmelCS genotypes were shown to cause mild cytoplasmic incompatibility (< 10 %), while wmelCS Wolbachia were unable to do so. Possible mechanisms of sustainability of Wolbachia in the populations of Drosophila melanogaster are discussed.

About the authors

Yury Y Ilinsky

Institute of Cytology and Genetics SB RAS, Novosibirsk, Novosibirsk Oblast, RF

Email: paulee@bionet.nsc.ru 630090, Novosibirsk, Lavrentyeva pr., 10. Russia

Ilya K Zakharov

Institute of Cytology and Genetics SB RAS, Novosibirsk, Novosibirsk Oblast, RF

Email: zakharov@bionet.nsc.ru 630090, Novosibirsk, Lavrentyeva pr., 10. Russia

References

  1. Горячева И. И., 2004. Бактерии рода Wolbachia -репродуктивные паразиты членистоногих//Успехи современной биологии. Т. 124. № 3. С. 246-259.
  2. Илинский Ю. Ю., 2008. Эндосимбионт Wolbachia в природных популяциях Drosophila melanogaster: Автореф. канд. дис. Новосибирск 16 с.
  3. Илинский Ю. Ю., Захаров И. К., 2007-a. Характеристика инфицированности цитоплазматическим эндосимбионтом Wolbachia популяции Drosophila melanogaster Умани//Доклады Академии наук. Т. 413. № 4. С. 561-563.
  4. Илинский Ю. Ю., Захаров И. К., 2007-б. Эндосимбионт Wolbachia в евразийских популяцих Drosophila melanogaster//Генетика. Т. 43. № 7. С. 905-915.
  5. Литвинова Е. М., 1977. Биология размножения дрозофилы//Проблемы генетики в исследованиях на дрозофиле/под. ред. Хвостова В. В. и др. Новосибирск: Наука. С. 19-61.
  6. Arakaki N., Miyoshi T., Noda H., 2001. Wolbachia-mediated parthenogenesis in the predatory thrips Franklinothrips vespiformis (Thysanoptera: Insecta)//Proc. Biol. Sci. Vol. 268. P. 1011-1016.
  7. Bourtzis K., Nirgianaki A., Onyango P., Savakis C., 1994. A prokaryotic dnaA sequence in Drosophila melanogaster: Wolbachia infection and cytoplasmic incompatibility among laboratory strains//Insect Mol. Biol. Vol. 3. P. 131-142.
  8. Braig H. R., Zhou W., Dobson S. L., O'Neill S. L., 1998. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis//J. Bacteriol. Vol. 180. P. 2373-2378.
  9. Breeuwer J. A., 1997 Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani//Nature.. Vol. 79. P. 41-47.
  10. Breeuwer J. A., Werren J. H., 1990. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species//Nature. Vol. 346. P. 558-560.
  11. Breeuwer J. A., Werren J. H., 1993. Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis//Genetics. Vol. 135. P. 565-574.
  12. Brower J., 1975. Cytoplasmic incompatibility: Occurrence in a stored-product PST Ephestia cautella//Ann. Entomol. Soc. Am. Vol. 69. P. 1011-1015.
  13. Charlat S., Hurst G. D., Mercot H., 2003a. Evolutionary consequences of Wolbachia infections//Trends Genet. Vol. 19. P. 217-223.
  14. Fry A. J., Palmer M. R., Rand D. M., 2004. Variable fitness effects of Wolbachia infection in Drosophila melanogaster//Heredity. Vol. 93. P. 379-389.
  15. Fujii Y., Kageyama D., Hoshizaki S., et. al., 2001. Transfection of Wolbachia in Lepidoptera: The femi-nizer of the adzuki bean borer Ostrinia scapulalis causes male killing in the mediterranean flour moth Ephestia kuehniella//Proc. Biol. Sci. Vol. 268. P. 855-859.
  16. Ghelelovitch S., 1952. Sur le determinisme genet-ique de la sterilite dans le croisement entre differenres souches de culex autogenicus roubaud.//C. R. Acad. Sci. Paris. Vol. 24. P. 2386-2388.
  17. Harcombe W., Hoffmann A. A., 2004. Wolbachia effects in Drosophila melanogaster: In search of fitness benefits//J. Invertebr. Pathol. Vol. 87. P. 45-50.
  18. Hilgenboecker K., Hammerstein P., Schlattmann P., et. al., 2008. How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol. Lett. Vol. 281. P. 215-220.
  19. Hoffmann A. A., Clancy D. J., Merton E., 1994. Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster//Genetics. Vol. 136. P. 993-999.
  20. Hsiao P., Hsiao C., 1985. Rickettsia as the cause of cytoplasmic incompatibility in the alfalfa weevil, Hypera postica//J. Invertebr. Pathol. Vol. 45. P. 244-246.
  21. Hurst G. D., Jiggins F. M., 2000. Male-killing bacteria in insects: Mechanisms, incidence, and implications//Emerg. Infect. Dis. Vol. 6. P. 329-336.
  22. Hurst G. D., Jiggins F. M., Robinson S. J., 2001. What causes inefficient transmission of male-kill-8. 8. ТОМ VII № 2 2009 ISSN 1811-0932 16 СИМБИОГеНетИКА ing Wolbachia in Drosophila?//Heredity. Vol. 87. P. 220-226.
  23. Hurst G. D., Johnson A. P., Schulenburg J. H., Fuyama Y., 2000. Male-killing Wolbachia in Drosophila: A temperature-sensitive trait with a threshold bacterial density//Genetics. Vol. 156. P. 699-709.
  24. Ikeda T., Ishikawa H., Sasaki T., 2003-a. Infection density of Wolbachia and level of cytoplasmic incompatibility in the Mediterranean flour moth, Ephestia kuehniella//J. Invertebr. Pathol. Vol. 84. P. 1-5.
  25. Ilinsky Y. Y., Zakharov I. K., 2006-a. Genetic correlation between types of mtdna of Drosophila melanogaster and genotypes of its primary endosymbiont, Wolbachia.//Drosophila Inform. SerV. Vol. P. 89-91.
  26. Ilinsky Y. Y., Zakharov I. K., 2006-b. Wolbachia in populations of Drosophila melanogaster//Drosophila Inform. SerV. Vol. P. 91-92.
  27. Iturbe-Ormaetxe I., Burke G. R., Riegler M., O'Neill S. L., 2005. Distribution, expression, and motif variability of ankyrin domain genes in Wolbachia pipientis//J. Bacteriol. Vol. 187. P. 5136-5145.
  28. Jiggins F. M., Hurst G. D. D., Majerus M. E. N., 1998. Sex ratio distortion in Acraea encedon (Lepidoptera: Nymphalidae) is caused by a male killing bacterium//Heredity. Vol. 81. P. 87-91.
  29. Jiggins F. M., Hurst G. D., Majerus M. E., 2000-a. Sexratio-distorting Wolbachia causes sex-role reversal in its butterfly host//Proc. Biol. Sci. Vol. 267. P. 69-73.
  30. Jiggins F. M., Hurst G. D. D., Dolman C. E., Majerus M. E. N., 2000-b. High-prevalence male-killing Wolbachia in the buttery, Acraea encedana//J. Evol. Biol. Vol. 13. P. 495-501.
  31. Jiggins F. M., Bentley J. K., Majerus M. E., Hurst G. D., 2001-a. How many species are infected with Wolbachia? Cryptic sex ratio distorters revealed to be common by intensive sampling//Proc. Biol. Sci. Vol. 268. P. 1123-1126.
  32. Jiggins F. M., Hurst G. D., Schulenburg J. H., Majerus M. E., 2001-b. Two male-killing Wolbachia strains coexist within a population of the butterfly Acraea encedon//Heredity. Vol. 86. P. 161-166.
  33. Jiggins F. M., von Der Schulenburg J. H., Hurst G. D., Majerus M. E., 2001-c. Recombination confounds interpretations of Wolbachia evolution//Proc. Biol. Sci. Vol. 268. P. 1423-1427.
  34. Jiggins F. M., Bentley J. K., Majerus M. E., Hurst G. D., 2002-a. Recent changes in phenotype and patterns of host specialization in Wolbachia bacteria//Mol. Ecol. Vol. 11. P. 1275-1283.
  35. Jiggins F. M., Hurst G. D., Yang Z., 2002-b. Host-symbiont conflicts: Positive selection on an outer membrane protein of parasitic but not mutualistic rickettsiaceae//Mol. Biol. Evol. Vol. 19. P. 1341-1349.
  36. Jiggins F. M., Randerson J. P., Hurst G. D., Majerus M. E., 2002-c. How can sex ratio distorters reach extreme prevalences? Male-killing Wolbachia are not suppressed and have near-perfect vertical transmission efficiency in Acraea encedon//Evolution Internat. J. Org. Evolution. Vol. 56. P. 2290-2295.
  37. Jiggins F. M., Hurst G. D., 2003. The evolution of parasite recognition genes in the innate immune system: Purifying selection on Drosophila melanogaster peptidoglycan recognition proteins//J. Mol. Evol. Vol. 57. P. 598-605.
  38. Kageyama D., Nishimura G., Hoshizaki S., Ishikawa Y., 2002. Feminizing Wolbachia in an insect, Ostrinia furnacalis (Lepidoptera: Crambidae)//Heredity. Vol. 88. P. 444-449.
  39. Kageyama D., Nishimura G., Hoshizaki S., Ishikawa Y., 2003-a. Two kinds of sex ratio distorters in a moth, Ostrinia scapulalis//Genome. Vol. 46. P. 974-982.
  40. Kageyama D., Ohno S., Hoshizaki S., Ishikawa Y., 2003-b. Sexual mosaics induced by tetra-cycline treatment in the Wolbachia-infected adzuki bean borer, Ostrinia scapulalis//Genome. Vol. 46. P. 983-989.
  41. Kang L., Zhu H., Cheng Q., et. al., 2002. Cloning and characterization of a gene encoding glutathione-regulated potassium-efflux system protein kefkl from the endosymbiont Wolbachia//DNA Seq. Vol. 13. P. 375-381.
  42. Kittayapong P., Baisley K. J., Baimai V., O'Neill S. L., 2000. Distribution and diversity of Wolbachia infections in southeast asian mosquitoes (Diptera: Culicidae)//J. Med. Entomol. Vol. 37. P. 340-345.
  43. Laven H., 1951. Crossing experiments with Culex strains//Evolution. Vol. 5. P. 370-375.
  44. Laven H., 1959-b. Speciation by citoplasmic isolation in the Culex pipiens complex//Cold Spring Harbor SymP. Quant. Biol. Vol. 24. P. 166-173.
  45. Laven H., 1959-a. Speciation and evolution in Culex pipiens./In Genetics of Insect Vectors of Disease. North Holland Elsevier.
  46. Leu S., Li J., Hciao T., 1989. Characterisation of Wolbachia postica the cause of reproductive incompatibility among alfalfa weevil strains//J. Invertebr. Pathol. Vol. 54. P. 248-259.
  47. McGraw E. A., Merritt D. J., Droller J. N., O'Neill S. L., 2001. Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila//Proc. Biol. Sci. Vol. 268. P. 2565-2570.
  48. Mercot H., Charlat S., 2004. Wolbachia infections in Drosophila melanogaster and D. simulans: Polymorphism and levels of cytoplasmic incompatibility//Genetica. Vol. 120. P. 51-59. 36. 36. ТОМ VII № 2 2009 ISSN 1811-0932 СИМБИОГеНетИКА 17
  49. Min K. T., Benzer S., 1997. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death//Proc. Natl. Acad. Sci. USA. Vol. 94. P. 10792-10796.
  50. Minamori S., Morihira K., 1969. Multiple mating in females of Drosophila melanogaster//J. Sci. Hiroshima UniVol. Ser. B. Vol. 1. P. 22.
  51. Noda H., 1984. Cytoplasmic incompatibility in allopatric field populations of the small brown planthopper of Laodelphax striatellus, in Japan//Entamol. ExP. Appl. Vol. 35. P. 263-267.
  52. Noda H., 1987. Further studies on cytoplasmic incompatibility in local populations of Laodelphax striatellus in Japan (Homoptera: Delphacidae)//Appl. Entomol. Zool. Vol. 22. P. 443-448.
  53. Noda H., Koizumi Y., Zhang Q., Deng K., 2001. Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera//Insect. Biochem. Mol. Biol. Vol. 31. P. 727-737.
  54. Noda H., Koizumi Y., Zhang Q., Deng K., 2001. Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera//Insect. Biochem. Mol. Biol. Vol. 31. P. 727-737.
  55. O`Neill S., 1989. Cytoplasmic symbionts in Tribolim confusum//J. Invertebr. Pathol. Vol. 53. P. 132-113.
  56. O'Neill S. L., Karr T. L., 1990. Bidirectional incompatibility between conspecific populations of Drosophila simulans//Nature. Vol. 348. P. 178-180.
  57. Pidiyar V. J., Jangid K., Dayananda K. M., et. al., 2003. Phylogenetic affiliation of Aeromonas culicicola MTCC 3249 (t) based on gyrB gene sequence and pcr-amplicon sequence analysis of cytolytic enterotoxin gene//Syst. Appl. Microbiol. Vol. 26. P. 197-202.
  58. Poinsot D., Bourtzis K., Markakis G., et. al., 1998. Wolbachia transfer from Drosophila melanogaster into D. simulans: Host effect and cytoplasmic incompatibility relationships//Genetics. Vol. 150. P. 227-237.
  59. Randerson J. P., Jiggins F. M., Hurst L. D., 2000. Male killing can select for male mate choice: A novel solution to the paradox of the lek//Proc. Biol. Sci. Vol. 267. P. 867-874.
  60. Rasgon J. L., Scott T. W., 2003. Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: Parameter estimates and infection dynamics in natural populations//Genetics. Vol. 165. P. 2029-2038.
  61. Reynolds K. T., Hoffmann A. A., 2002. Male age, host effects and the weak expression or non-expression of cytoplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia//Genet. Res. Vol. 80. P. 79-87.
  62. Reynolds K. T., Thomson L. J., Hoffmann A. A., 2003. The effects of host age, host nuclear background and temperature on phenotypic effects of the virulent Wolbachia strain popcorn in Drosophila melanogaster//Genetics. Vol. 164. P. 1027-1034.
  63. Riegler M., Sidhu M., Miller W. J., O'Neill S. L., 2005. Evidence for a global Wolbachia replacement in Drosophila melanogaster//Curr. Biol. Vol. 15. P. 1428-1433.
  64. Rigaud T., Antoine D., Marcade I., Juchault P., 1997. The effect of temperature on sex ratio in the Isopod Porcellionides pruinosus: Environmental sex determination or by-product of cytoplasmic sex determination//Evol. Ecol. Vol. 11. P. 205-215.
  65. Stromnaess O., Kvelland J.,1962. Sexual activity of Drosophila melanogaster males//Hereditas. Vol. 48. P. 342-470.
  66. Sun L. V., Foster J. M., Tzertzinis G., et. al., 2001. Determination of Wolbachia genome size by pulsed-field gel electrophoresis//J. Bacteriol. Vol. 183. P. 2219-2225.
  67. Sun L. V., Riegler M., O'Neill S. L., 2003. Development of a physical and genetic map of the virulent Wolbachia strain wMelPop//J. Bacteriol. Vol. 185. P. 7077-7084.
  68. Turelli M., Hoffmann A. A., 1991. Rapid spread of an inherited incompatibility factor in California Drosophila//Nature. Vol. 353. P. 440-442.
  69. Turelli M., Hoffmann A. A., McKechnie S. W., 1992. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations//Genetics. Vol. 132. P. 713-723.
  70. Van Borm S., Wenseleers T., Billen J., Boomsms J., 2001. Wolbachia in leafcutter ants: A widespread symbiont that may induce male killing or incompatible matings//J. Evolutionary Biology. Vol. 14. P. 805-814.
  71. Vavre F., Fleury F., Varaldi J., et. al., 2000. Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects, epidemiologic and evolutionary consequences//Evolution. Vol. 54. P. 191.
  72. Wade M. J., Stevens L., 1985. Microorganism mediated reproductive isolation in flour beetles (genus Tribolium)//Science. Vol. 227. P. 527-528.
  73. Wu M., Sun L. V., Vamathevan J., et. al., 2004. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: A streamlined genome overrun by mobile genetic elements//PLoS Biol. Vol. 2. P. E69.
  74. Yamada R., Floate K. D., Riegler M., O'Neill S. L., 2007. Male development time influences the strength of Wolbachia-induced cytoplasmic incompatibility expression in Drosophila melanogaster//Genetics. Vol. 177. P 801-808. 62. 62. ТОМ VII № 2 2009 ISSN 1811-0932 18 СИМБИОГеНетИКА
  75. Zhou W., Rousset F., O'Neil S., 1998. Phylogeny and pcr-based classification of Wolbachia strains using wsp gene sequences//Proc. Biol. Sci. Vol. 265. P. 509-515.

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