Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies

Evolution

Volumn 63, Issue 3, 2009, Pages 624-640

  Russell, Jacob A ^a,d   Goldman Huertas, Benjamin ^a   Moreau, Corrie S ^a,e   Baldo, Laura ^b   Stahlhut, Julie K ^c   Werren, John H ^c   Pierce, Naomi E ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ROCHESTER   (United States)

^d DREXEL UNIVERSITY   (United States)

^e FIELD MUSEUM OF NATURAL HISTORY   (United States)

Author keywords

Bacteria; Coevolution; Insects; Phylogenetics; Specialization; Symbiont

Indexed keywords

ANT; BACTERIUM; BUTTERFLY; COEVOLUTION; DIVERGENCE; EVOLUTIONARY BIOLOGY; GEOGRAPHICAL VARIATION; HOST-SYMBIONT INTERACTION; ISOLATED POPULATION; PHYLOGENETICS; SPECIALIZATION; SYMBIONT;

ANIMAL; ANT; ARTICLE; BACTERIUM IDENTIFICATION; BUTTERFLY; EVOLUTION; GENETICS; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY; SYMBIOSIS; WOLBACHIA;

ANIMALS; ANTS; BACTERIAL TYPING TECHNIQUES; BUTTERFLIES; EVOLUTION; PHYLOGENY; SYMBIOSIS; WOLBACHIA;

BACTERIA (MICROORGANISMS); FORMICIDAE; HEXAPODA; LYCAENIDAE; PAPILIONOIDEA; WOLBACHIA;

EID: 60849134825     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00579.x     Document Type: Article

References (95)

1. Baldo, L., N. Lo, and J. H. Werren. 2005. The mosaic nature of the Wolbachia surface protein (wsp). J. Bacteriol. 187 : 5406 5418.
2. Baldo, L., S. Bordenstein, J. J. Wernegreen, and J. H. Werren. 2006a. Widespread recombination throughout Wolbachia genomes. Mol. Biol. Evol. 23 : 437 449.
3. Baldo, L., J. C. Dunning Hotopp, K. A. Jolley, S. R. Bordenstein, S. A. Biber, R. R. Choudhury, C. Hayashi, M. C. J. Maiden, H. Tettelin, and J. H. Werren. 2006b. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl. Environ. Microbiol. 72 : 7098 7110.
4. Baldo, L, L. Prendini, A. Corthals, and J. H. Werren. 2007. Wolbachia are present in Southern African scorpions and cluster with supergroup F. Curr. Microbiol. 55 : 367 373.
5. Baldo, L., A. Nadia, N. A. Ayoub, C. Y. Hayashi, J. A. Russell, J. K. Stahlhut, and J. H. Werren. 2008. Insight into the routes of Wolbachia invasion: high levels of horizontal transfer in the spider genus Agelenopsis revealed by Wolbachia strain and mitochondrial DNA diversity. Mol. Ecol. 17 : 557 569.
6. Ballard, J. W. O. 2000. Comparative genomics of mitochondrial DNA in Drosophila simulans. J. Mol. Evol. 51 : 64 75.
7. Ballard, J. W. O., J. Hatzidakis, T. L. Karr, and M. Kreitman. 1996. Reduced variation in Drosophila simulans mitochondrial DNA. Genetics 144 : 1519 1528.
8. Bordenstein, S. R., F. P. O'Hara, and J. H. Werren. 2001. Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409 : 707 710.
9. Bouchon, D., T. Rigaud, and P. Juchault. 1998. Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc. R. Soc. Lond. B. 265 : 1081 1090.
10. Charlat, S., G. D. D. Hurst, and H. Merçot. 2003. Evolutionary consequences of Wolbachia infections. Trends Genet. 19 : 217 223.
11. Darby, A. C., and A. E. Douglas. 2003. Elucidation of the transmission patterns of an insect-borne bacterium. Appl. Environ. Microbiol. 69 : 4403 4407.
12. Davidson, D. W., S. C. Cook, R. R. Snelling, and T. H. Chua. 2003. Explaining the abundance of ants in lowland tropical rainforest canopies. Science 300 : 969 972.
13. Dedeine, F., M. Ahrens, L. Calcaterra, and D. D. Shoemaker. 2005. Social parasitism in fire ants (Solenopsis spp.): a potential mechanism for interspecies transfer of Wolbachia. Mol. Ecol. 14 : 1543 1548.
14. Didelot, X., and D. Falush. 2007. Inference of bacterial microevolution using multilocus sequence data. Genetics 175 : 1251 1266.
15. Dittmar, K., and M. F. Whiting. 2004. New Wolbachia endosymbionts from Nearctic and Neotropical fleas. J. Parasitol. 90 : 953 957.
16. Dobson, S. L., K. Bourtzis, H. R. Braig, B. F. Jones, W. G. Zhou, F. Rousset, and S. L. O'Neill. 1999. Wolbachia infections are distributed throughout insect somatic and germ line tissues. Ins. Biochem. Mol. Biol. 29 : 153 160.
17. 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.
18. Dyson, E. A., and G. D. D. Hurst. 2004. Persistence of an extreme sex-ratio bias in a natural population. Proc. Natl. Acad. Sci. USA 101 : 6520 6523.
19. Enright, M. C., and B. G. Spratt. 1998. A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiol. UK 144 : 3049 3060.
20. Excoffier, L., P. E. Smouse, and J. M. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131 : 479 491.
21. Excoffier, L., G. Laval, and S. Schneider. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinformatics Online 1 : 47 50.
22. Feil, E. J., B. C. Li, D. M. Aanensen, W. P. Hanage, and B. G. Spratt. 2004. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 186 : 1518 1530.
23. Felsenstein, J. 1989. PHYLIP - Phylogeny Inference Package (Version 3.2). Cladistics 5 : 164 166.
24. Fenn, K., and M. Blaxter. 2004. Are filarial nematode Wolbachia obligate mutualist symbionts? Trends Ecol. Evol. 19 : 163 166.
25. Fujii, Y., D. Kageyama, S. Hoshizaki, H. Ishikawa, and T. Sasaki. 2001. 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. R. Soc. Lond. B. 268 : 855 859.
26. Genecodes. 2003. Sequencher (Version 3.1.1). Ann Arbor, Genecodes Co.
27. Gottlieb, Y., and E. Zchori-Fein. 2001. Irreversible thelytokous reproduction in Muscidifurax uniraptor. Entomol. Exp. Appl. 100 : 271 278.
28. Grenier, S., B. Pintureau, A. Heddi, F. Lassabliere, C. Jager, C. Louis, and C. Khatchadourian. 1998. Successful horizontal transfer of Wolbachia symbionts between Trichogramma wasps. Proc. R. Soc. Lond. B. 265 : 1441 1445.
29. Hammer, M. H., T. M. Karafet, A. J. Redd, H. Jarjanazi, S. Santachiara-Benerecetti, H. Soodyall, and S. L. Zegura. 2001. Hierarchical patterns of global human Y-chromosome diversity. Mol. Biol. Evol. 18 : 1189 1203.
30. Hilgenböecker, K., A. Telschow, P. Hammerstein, P. Schlattmann, A. Telschow, and J. H. Werren. 2008. How many species are infected with Wolbachia? - a statistical analysis of current data. FEMS Microbiol. Lett. 281 : 215 220.
31. Hiroki, M., Y. Kato, T. Kamito, and K. Miura. 2002. Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera : Pieridae). Naturwissenschaften 89 : 167 170.
32. Hölldobler, B., and E. O. Wilson. 1990. The ants. Cambridge: The Belknap Press of Harvard Univ. Press, Cambridge, MA.
33. Huigens, M. E., and R. Stouthamer. 2003. Parthenogenesis associated with Wolbachia. Pp 247 266. in K. Bourtzis, and T. A. Miller, eds. Insect symbiosis. CRC Press, Boca Raton, FL.
34. Huigens, M. E., R. P. de Almeida, P. A. H. Boons, R. F. Luck, and R. Stouthamer. 2004. Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc. R. Soc. Lond. B. 271 : 509 515.
35. Hurst, G. D. D., and F. M. Jiggins. 2005. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc. R. Soc. Lond. B. 272 : 1525 1534.
36. Jaenike, J., K. A. Dyer, C. Cornish, and M. S. Minhas. 2006. Asymmetrical reinforcement and Wolbachia infection in Drosophila. PLOS Biol. 4 : 1852 1862.
37. Jaenike, J., M. Polak, A. Fiskin, M. Helou, and M. Minhas. 2007. Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol. Lett. 3 : 23 25.
38. Jeong, S. C., N. J. Ritchie, and D. D. Myrold. 1999. Molecular phylogenies of plants and Frankia support multiple origins of actinorhizal symbioses. Mol. Phylogenet. Evol. 13 : 493 503.
39. Jeyaprakash, A., and M. A. Hoy. 2000. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol. Biol. 9 : 393 405.
40. Jiggins, F. M., G. D. D. Hurst, C. E. Dolman, and M. E. N. Majerus. 2000a. High-prevalence male-killing Wolbachia in the butterfly Acraea encedana. J. Evol. Biol. 13 : 495 501.
41. Jiggins, F. M., G. D. D. Hurst, and M. E. N. Majerus. 2000b. Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc. R. Soc. Lond. B. 267 : 69 73.
42. Jiggins, F. M., J. H. G. von der Schulenburg, G. D. D. Hurst, and M. E. N. Majerus. 2001. Recombination confounds interpretation of Wolbachia evolution. Proc. R. Soc. Lond. B. 268 : 1423 1427.
43. Jiggins, F. M., J. K. Bentley, M. E. N. Majerus, and G. D. D. Hurst. 2002. Recent changes in phenotype and patterns of host specialization in Wolbachia bacteria. Mol. Ecol. 11 : 1275 1283.
44. Kaeding, A. J., J. C. Ast, M. M. Pearce, H. Urbanczyk, S. Kimura, H. Endo, M. Nakamura, and P. V. Dunlap. 2007. Phylogenetic diversity and cosymbiosis in the bioluminescent symbioses of "Photobacterium mandapamensis," Appl. Env. Microbiol. 73 : 3173 3182.
45. Kang, L., X. Ma, L. Cai, S. Liao, L. Sun, H. Zhu, X. Chen, D. Shen, S. Zhao, and C. Li. 2003. Superinfection of Laodelphax striatellus with Wolbachia from Drosophila simulans. Heredity 90 : 71 76.
46. Kittayapong, P., W. Jamnongluk, A. Thipaksorn, J. R. Milne, and C. Sindhusake. 2003. Wolbachia infection complexity among insects in the tropical rice-field community. Mol. Ecol. 12 : 1049 1060.
47. Kyei-Poku, G. K., D. D. Colwell, P. Coghlin, B. Benkel, and K. D. Floate. 2005. On the ubiquity and phylogeny of Wolbachia in lice. Mol. Ecol. 14 : 285 294.
48. Maddison, W. P., and D. R. Maddison. 2003. MacClade: analysis of phylogeny and character evolution (ver. 4.06). Sinauer Associates, Sunderland, MA.
49. Maiden, M. C. J., J. A. Bygraves, E. Feil, G. Morelli, J. E. Russell, R. Urwin, Q. Zhang, J. J. Zhou, K. Zurth, D. A. Caugant, et al. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95 : 3140 3145.
50. Margulis, L., and R. Fester. 1991. Symbiosis as a source of evolutionary innovation. The MIT Press. Cambridge, MA.
51. McGlynn. 1999. The worldwide transfer of ants: geographical distribution and ecological invasions. J. Biogeogr. 26 : 535 548.
52. 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.
53. Moran, N. A., and P. Baumann. 1994. Phylogenetics of cytoplasmically inherited microorganisms of arthropods. Trends Ecol. Evol. 9 : 15 20.
54. Moran, N. A., and J. J. Wernegreen. 2000. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15 : 321 326.
55. Moreau, C. S., C. D. Bell, R. Vila, S. B. Archibald, and N. E. Pierce. 2006. Phylogeny of the ants: diversification in the age of angiosperms. Science 312 : 101 104.
56. Moreau, C. S. 2008. Unraveling the evolutionary history of the hyperdiverse ant genus Pheidole (Hymenoptera: Formicidae). Mol. Phylogenet. Evol. 48 : 224 239.
57. Noda, H., T. Miyoshi, Q. Zhang, K. Watanabe, K. Deng, and S. Hoshikazi. 2001. Wolbachia infection shared among planthoppers (Homoptera: Delphacidae) and their endoparasite (Strepsiptera: Elenchidae): a probable case of interspecies transmission. Mol. Ecol. 10 : 2101 2106.
58. O'Neill, S. L., A. A. Hoffmann, and J. H. Werren. 1997. Influential passengers. Oxford Univ. Press, New York, NY.
59. Peek, A. S., R. A. Feldman, R. A. Lutz, and R. C. Vrijenhoek. 1998. Cospeciation of chemoautotrophic bacteria and deep sea clams. Proc. Natl. Acad. Sci. USA 95 : 9962 9966.
60. Pérez-Lezaun, A., F. Calafell, D. Comas, E. Mateu, E. Bosch, R. Martínez-Arias, J. Clarimón, G. Fiori, D. Luiselli, F. Facchini, et al. 1999. Sex-specific migration patterns in Central Asian populations, revealed by analysis of Y-chromosome short tandem repeats and mtDNA. Am. J. Hum. Genet. 65 : 208 219.
61. Pierce, N. E., M. F. Braby, A. Heath, D. J. Lohman, J. Mathew, D. B. Rand, and M. A. Travassos. 2002. The ecology and evolution of ant associations in the Lycaenidae. Annu. Rev. Entomol. 47 : 733 771.
62. Poinsot, D., and H. Merçot. 2001. Wolbachia injection from usual to naive host in Drosophila simulans (Diptera: Drosophilidae). Eur. J. Entomol. 98 : 25 30.
63. Purcell, A. H., K. G. Suslow, and M. Klein. 1994. Transmission via plants of an insect pathogenic bacterium that does not multiply or move in plants. Microb. Ecol. 27 : 19 26.
64. Rasgon, J. L., A. J. Cornel, and T. W. Scott. 2006. Evolutionary history of a mosquito endosymbiont revealed through mitochondrial hitchhiking. Proc. R. Soc. Lond. B. 273 : 1603 1611.
65. Raymond, M., and F. Rousset. 1995. An exact test for population differentiation. Evolution 49 : 1280 1283.
66. Riegler, M., S. Charlat, C. Stauffer, and H. Merçot. 2004. Wolbachia transfer from Rhagoletis cerasi to Drosophila simulans: investigating the outcomes of host-symbiont coevolution. Appl. Environ. Microbiol. 70 : 273 279.
67. Rigaud, T., P. S. Pennings, and P. Juchault. 2001. Wolbachia bacteria effects after experimental interspecific transfers in terrestrial isopods. J. Invertebr. Pathol. 77 : 251 257.
68. Roussett, F., D. Bouchon, B. Pintureau, P. Juchault, and M. Solignac. 1992. Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc. R. Soc. Lond. B. 250 : 91 98.
69. Sasaki, T., and H. Ishikawa. 2000. Transinfection of Wolbachia in the Mediterranean flour moth, Ephestia kuehniella, by embryonic microinjection. Heredity 85 : 130 135.
70. Sheppard, S. K., N. D. McCarthy, D. Falush, M. C. J. Maiden. 2008. Convergence of Campylobacter species: implications for bacterial evolution. Science 320 : 237 239.
71. Shoemaker, D. D., V. Katju, and J. Jaenike. 1999. Wolbachia and the evolution of reproductive isolation between Drosophila recens and Drosophila subquinaria. Evolution 53 : 1157 1164.
72. Shoemaker, D. D., C. A. Machado, D. Molbo, J. H. Werren, D. M. Windsor, and E. A. Herre. 2002. The distribution of Wolbachia in fig wasps: correlations with host phylogeny, ecology and population structure. Proc. R. Soc. Lond. B. 269 : 2257 2267.
73. Shoemaker, D. D., K. A. Dyer, M. Ahrens, K. McAbee, and J. Jaenike. 2004. Decreased diversity but increased substitution rate in host mtDNA as a consequence of Wolbachia endosymbiont infection. Genetics 168 : 2049 2058.
74. Simon, C., F. Frati, A. Bechenbach, B. Crespi, H. Liu, and P. Flook. 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequence and compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 87 : 651 701.
75. Sintupachee, S., J. R. Milne, S. Poonchaisri, V. Baimai, and P. Kittayapong. 2006. Closely related Wolbachia strains within the pumpkin arthropod community and the potential for horizontal transmission via the plant. Mol. Ecol. 51 : 294 301.
76. Stanley, H. F., S. Casey, J. M. Carnahan, S. Goodman, J. Harwood, and R. K. Wayne. 1996. Worldwide patterns of mitochondrial DNA differentiation in the Harbor Seal (Phoca vitulina). Mol. Biol. Evol. 13 : 368 382.
77. Tagami, Y., and K. Miura. 2004. Distribution and prevalence of Wolbachia in Japanese populations of Lepidoptera. Ins. Mol. Biol. 13 : 359 364.
78. Tsutsui, N. D., S. N. Kauppinen, A. F. Oyafuso, and R. K. Grosberg. 2003. The distribution and evolutionary history of Wolbachia in native and introduced populations of the invasive argentine ant (Linepithema humile). Mol. Ecol. 12 : 3057 3068.
79. Urquhart, F. A. 1976. Found at last: the Monarch's winter home. Natl. Geogr. Mag. 150 : 160 173.
80. van Borm, S., T. Wenseleers, J. Billen, and J. J. Boomsma. 2001. Wolbachia in leafcutter ants: a widespread symbiont that may induce male killing or incompatible matings. J. Evol. Biol. 14 : 805 814.
81. van Meer, M. M. M., and R. Stouthamer. 1999. Cross-order transfer of Wolbachia from Muscidifurax uniraptor (Hymenoptera : Pteromalidae) to Drosophila simulans (Diptera : Drosophilidae). Heredity 82 : 163 169.
82. van Meer, M. M. M., J. Witteveldt, and R. Stouthamer. 1999. Phylogeny of the arthropod endosymbiont Wolbachia based on the wsp gene. Ins. Mol. Biol. 8 : 399 408.
83. 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.
84. Webb, C. O., D. D. Ackerly, and S. W. Kembel. 2006. Phylocom: software for the analysis of community phylogenetic structure and trait evolution. Version 3.40. http://www.phylodiversity.net/phylocom/.
85. Wenseleers, T., F. Ito, S. van Borm, R. Huybrechts, F. Volckaert, and J. Billen. 1998. Widespread occurrence of the micro-organism Wolbachia in ants. Proc. R. Soc. Lond. B. 265 : 1447 1452.
86. Wenseleers, T., L. Sundstrom, and J. Billen. 2002. Deleterious Wolbachia in the ant Formica truncorum. Proc. R. Soc. Lond. B. 269 : 623 629.
87. Werren, J. H. 1997. Biology of Wolbachia. Ann. Rev. Entomol. 42 : 587 609.
88. Werren, J. H. 1998. Wolbachia and speciation. Pp. 245 260 in D. Howard, and S. Berlocher, eds. Endless forms: species and speciation. Oxford Univ. Press, Oxford.
89. Werren, J. H., and J. D. Bartos. 2001. Recombination in Wolbachia. Curr. Biol. 11 : 431 435.
90. Werren, J. H., and D. M. Windsor. 2000. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc. R. Soc. Lond. B. 267 : 1277 1285.
91. Werren, J. H., D. Windsor, and L. R. Guo. 1995a. Distribution of Wolbachia among neotropical arthropods. Proc. R. Soc. Lond. B. 262 : 197 204.
92. Werren, J. H., W. Zhang, and L. R. Guo. 1995b. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc. R. Soc. Lond. B. 261 : 55 63.
93. West, S. A., J. M. Cook, J. H. Werren, and H. C. J. Godfray. 1998. Wolbachia in two insect host-parasitoid communities. Mol. Ecol. 7 : 1457 1465.
94. Zchori-Fein, E., and S. J. Perlman. 2004. Distribution of the bacterial symbiont Cardinium in arthropods. Mol. Ecol. 13 : 2009 2016.
95. 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.