Wolbachia plays no role in the one-way reproductive incompatibility between the hybridizing field crickets Gryllus firmus and G. pennsylvanicus

Heredity

Volumn 101, Issue 5, 2008, Pages 435-444

  Maroja, L S ^a   Clark, M E ^b   Harrison, R G ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Antibiotic treatment; Cytoplasmic incompatibility; Real time PCR; Reproductive isolation

Indexed keywords

ANTIBIOTICS; BACTERIUM; CRICKET; CYTOPLASM; HYBRIDIZATION; INCOMPATIBILITY; MATING BEHAVIOR; POLYMERASE CHAIN REACTION; REPRODUCTION; REPRODUCTIVE ISOLATION;

ANIMAL; ARTICLE; CROSS BREEDING; CYTOLOGY; FEMALE; GENETICS; GRYLLIDAE; HYBRIDIZATION; MALE; MICROBIOLOGY; OOCYTE; PHYSIOLOGY; REPRODUCTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SEXUAL BEHAVIOR; SPECIES DIFFERENCE; SPERMATOZOON; WOLBACHIA;

ANIMALS; CROSSES, GENETIC; FEMALE; GRYLLIDAE; HYBRIDIZATION, GENETIC; MALE; OVUM; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; SPECIES SPECIFICITY; SPERMATOZOA; WOLBACHIA;

ALPHAPROTEOBACTERIA; GRYLLINAE; GRYLLUS FIRMUS; HEXAPODA; WOLBACHIA;

EID: 54349116711     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2008.75     Document Type: Article

References (73)

1. Barr AR (1980). Cytoplasmic incompatibility in natural populations of a mosquito, Culex pipiens. Nature 283: 71-72.
2. Bordenstein SR (2003). Symbiosis and the origin of species. In: Miller T, Bourtzis K (eds). Insect Symbiosis. CRC Press: New York.
3. Bordenstein SR, O'Hara FP, Werren JH (2001). Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Science 409: 675-677.
4. Bourtzis K, Nirgianaki A, Markakis G, Savakis C (1996). Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144: 1063-1073.
5. Boyle L, O'Neill SL, Robertson HM, Karr TL (1993). Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260: 1796-1799.
6. Breeuwer JAJ, Stouthamer R, Barns SM, Pelletier DA, Weisburg WG, Werren JH (1992). Phylogeny of cytoplasmic incompatibility microorganisms in the parasitoid wasp genus Nasonia based on 16S ribosomal DNA sequences. Insect Mol Biol 1: 25-36.
7. Breeuwer JAJ, Werren JH (1990). Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346: 558-560.
8. Breeuwer JAJ, Werren JH (1993). Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics 135: 565-574.
9. Breeuwer JAJ, Werren JH (1995). Hybrid breakdown between two haploid species: the role of nuclear and cytoplasmic genes. Evolution 49: 705-717.
10. Bressac C, Rousset F (1993). The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J Invert Pathol 61: 226-230.
11. Burpee DM, Sakaluk SK (1993). Repeated matings offset the costs of reproduction in female field crickets. Evol Ecol 7: 240-250.
12. Callaini G, Dallai R, Riparbelli MG (1997). Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila simulans. J Cell Sci 110: 271-280.
13. Callaini GM, Riparbelli G, Giordano R, Dallai R (1996). Mitotic defects associated with cytoplasmic incompatibility in Drosophila simulans. J Invert Pathol 67: 55-64.
14. Clark ME, Bailey-Jourdain C, Ferree PM, England S, Sullivan W, Windsor D et al. (2008). Wolbachia modification of sperm does not always require residence within developing sperm. Heredity (in press).
15. Clark ME, Veneti Z, Bourtzis K, Karr TL (2002). The distribution and proliferation of the intracellular bacteria Wolbachia during spermatogenesis in Drosophila. Mech Dev 111: 3-15.
16. Clark ME, Veneti Z, Bourtzis K, Karr TL (2003). Wolbachia distribution and cytoplasmic incompatibility during sperm development: the cyst as the basic cellular unit of CI expression. Mech Dev 120: 185-198.
17. Coyne JA (1992). Genetics and speciation. Nature 355: 511-515.
18. Coyne JA, Orr HA (2004). Speciation. Sinauer Associates: Sunderland, MA.
19. Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Boulétreau M (2001). Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98: 6247-6252.
20. Duron O, Weill M (2006). Wolbachia infection influences the development of Culex pipiens embryos in incompatible crosses. Heredity 96: 493-500.
21. Giordano R, Jackson JJ, Robertson HM (1997). The role of Wolbachia bacteria in reproductive incompatibilities and hybrid zones of Diabrotica beetles and Gryllus crickets. Proc Natl Acad Sci USA 94: 11439-11444.
22. Giordano R, O'Neil SL, Robertson HM (1995). Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophila sechellia and D. mauritiana. Genetics 140: 1307-1317.
23. Harrison RG (1983). Barriers to gene exchange between closely related cricket species. I. Laboratory hybridization studies. Evolution 37: 245-251.
24. Harrison RG (1985). Barriers to gene exchange between closely related cricket species. II. Life cycle variation and temporal isolation. Evolution 39: 244-259.
25. Harrison RG, Bogdanowicz SM (1997). Patterns of variation and linkage disequilibrium in a field cricket hybrid zone. Evolution 51: 493-505.
26. Harrison RG, Rand DM (1989). Mosaic hybrid zones and the nature of species boundaries. In: Otte D, Endler JA (eds). Speciation and its Consequences. Sinauer: Sunderland, MA. pp 111-133.
27. Harrison RG, Rand DM, Wheeler WC (1987). Mitochondrial DNA variation in field crickets across a narrow hybrid zone. Mol Biol Evol 4: 144-158.
28. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008). How many species are infected with Wolbachia? - a statistical analysis of current data. FEMS Microbiol Lett 281: 215-220.
29. Hoerauf A, Nissen-Pahle K, Schmetz C, Henkle-Duhrsen K, Blaxter ML, Büttner DW 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.
30. Hoerauf A, Volkmann L, Hamelmann C, Adjei O, Autenrieth IB, Fleischer B et al. (2000). Endosymbiotic bacteria in worms as targets for a novel chemotherapy in filariasis. Lancet 355: 1242-1243.
31. Hoffmann AA, Clancy D, Duncan J (1996). Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity 76: 1-8.
32. Hurst GD, Jiggins FM, Robinson SJW (2001). What causes inefficient transmission of male-killing Wolbachia in Drosophila? Heredity 87: 220-226.
33. Hurst GD, Johnson AP, Schulenburg JH, Fuyama Y (2000). Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 156: 699-709.
34. Hurst GDD, Jiggins FM, Schulenburg JHG, Bertrand D, West SA, Goriacheva II et al. (1999). Male-killing Wolbachia in two species of insect. Proc R Soc Lond B Biol Sci 266: 735-740.
35. Ikeda H (1970). The cytoplasmically-inherited 'sex-ratio' condition in natural and experimental populations of Drosophila bifasciata. Genetics 65: 311-333.
36. Ivy TM, Sakaluk SK (2005). Polyandry promotes enhanced offspring survival in decorated crickets. Evolution 59: 152-159.
37. Jaenike J, Dyer KA, Cornish C, Minhas MS (2006). Asymmetrical reinforcement and Wolbachia infection in Drosophila. PLoS Biol 4: e325.
38. Jeyaprakash A, Hoy MA (2000). Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 9: 393-405.
39. Lassy CW, Karr TL (1996). Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans. Mech Dev 57: 47-58.
40. Mandel MJ, Ross C, Harrison RG (2001). Do Wolbachia infections play a role in unidirectional incompatibilities in a field cricket hybrid zone? Mol Ecol 10: 703-709.
41. Maroja LS (2008). Barriers to gene exchange in a field cricket hybrid zone. PhD dissertation, Cornell University, Ithaca, NY.
42. Marshall JL (2004). The Allonemobius-Wolbachia host-endosymbiont system: evidence for rapid speciation and against reproductive isolation driven by cytoplasmic incompatibility. Evolution 58: 2409-2425.
43. McGraw EA, Merritt DJ, Droller NJ, O'Neill SL (2002). Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci USA 99: 2918-2923.
44. Navajas M, Tsagkarakov A, Lagnel J, Perrot-Minnot M-J (2000). Genetic differentiation in Tetranychus urticae (Acari: Tetranychidae): polymorphism, host races or sibling species? Exp Appl Acarol 24: 365-376.
45. O'Neill SL, Giordano R, Colbert AME, Karr TL, Robertson HM (1992). 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 89: 2699-2702.
46. O'Neill SO, Karr TL (1990). Bidirectional cytoplasmic incompatibility between conspecific populations of Drosophila simulans. Nature 348: 178-180.
47. Poinsot D, Bourtzis K, Markakis G, Savakis C, Merlot H (1998). Wolbachia transfer from Drosophila melanogaster into D. simulans: host effect and cytoplasmic incompatibility relationships. Genetics 150: 227-237.
48. R Development Core Team (2006). R: a language and environment for statistical computing. Vienna, Austria (http://www.R-project.org).
49. Riparbelli MG, Giordano R, Callaini G (2007). Effects of Wolbachia on sperm maturation and architecture in Drosophila simulans Riverside. Mech Dev 124: 699-714.
50. Ross CL, Harrison RG (2002). A fine-scale spatial analysis og the mosaic hybrid zone between Gryllus firmus and Gryllus pennsylvanicus. Evolution 56: 2296-2312.
51. Ross CL, Harrison RG (2006). Viability selection on over-wintering eggs in a field cricket mosaic hybrid zone. Oikos 115: 53-68.
52. Rousset F, Bouchon D, Pintureau B, Juchault P, Solignac M (1992). Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc R Soc Lond B Biol Sci 250: 91-98.
53. Sakaluk SK, Schaus JM, Eggert AK, Snedden WA, Brady PL (2002). Polyandry and fitness of offspring reared under varying nutritional stress in decorated crickets. Evolution 56: 1999-2007.
54. Shoemaker DD, Katju V, Jaenike J (1999). Wolbachia and the evolution of reproductive isolation between Drosophila recens and Drosophila subquinaria. Evolution 53: 1157-1164.
55. Simmons LW (1988). The calling song of the field cricket Gryllus bimaculatus (De Geer): constraints on transmission and its role in intermale competition and female choice. Anim Behav 36: 380-394.
56. Stouthamer R, Breeuwer JAJ, Hurst DD (1999). Wolbachia Pipientis: microbial manipulator of arthropod reproduction. Ann Rev Microbiol 53: 71-102.
57. Stouthamer R, Breeuwer JAJ, Luck RF, Werren JH (1993). Molecular identification of microorganisms associated with parthenogenesis. Nature 361: 66-68.
58. Telschow A, Hammerstein P, Werren JH (2005a). The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation. Evolution 59: 1607-1619.
59. Telschow A, Yamamura N, Werren JH (2005b). Bidirectional cytoplasmic incompatibility and the stable coexistence of two Wolbachia strains in parapatric host populations. J Theor Biol 235: 265-274.
60. Tram U, Sullivan W (2002). Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296: 1124-1126.
61. Vala F, Breeuwer JA, Sabelis MW (2000). Wolbachia induced 'hybrid breakdown' in the two-spotted spider mite Tetranychus urticae Koch. Proc R Soc Lond B Biol Sci 267: 1931-1937.
62. Veneti Z, Clark ME, Zabalou S, Karr TL, Savakis C, Bourtzis K (2003). Cytoplasmic incompatibility and sperm cyst infection in different Drosophila-Wolbachia associations. Genetics 164: 545-552.
63. Wagner WE, Kelley RJ, Tucker KR, Harper CJ (2001). Females receive a life-span benefit from male ejaculates in a field cricket. Evolution 55: 994-1001.
64. Weeks AR, Reynolds KT, Hoffmann AA (2002). Wolbachia dynamics and host effects: what has (and has not) been demonstrated? Trends Ecol Evol 17: 257-262.
65. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA (2007). From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5: e114.
66. Werren JH (1997a). Biology of Wolbachia. Annu Rev Entomol 42: 587-609.
67. Werren JH (1997b). Wolbachia and speciation. In: Howard D, Berlocher S (eds). Endless Species and Speciation. Oxford University Press: New York.
68. Werren JH, Windsor D, Guo RL (1995). Distribution of Wolbachia among neotropical arthropods. Proc Royal Soc Lond B 262: 197-204.
69. Werren JH, Windsor DM (2000). Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc R Soc Lond B Biol Sci 267: 1277-1285.
70. West SA, Cook JM, Werren JH, Godfray HC (1998). Wolbachia in two insect host-parasitoid communities. Mol Ecol 7: 1457-1465.
71. Willett C, Ford MJ, Harrison RG (1997). Inferences about the origin of a field cricket hybrid zone from a mitochondrial DNA phylogeny. Heredity 79: 484-494.
72. Yen JH, Barr AR (1971). New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens. Nature 232: 657-658.
73. Zchori-Fein E, Gottlieb Y, Coll M (2000). Wolbachia density and host fitness components in Muscidifurax uniraptor (Hymenoptera: pteromalidae). J Invertebr Pathol 75: 267-272.