Exploring the effect of the Cardinium endosymbiont on spiders

Journal of Evolutionary Biology

Volumn 25, Issue 8, 2012, Pages 1521-1530

  Stefanini, A ^a   Duron, O ^a  

^a INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

Cardinium; Endosymbiosis; Reproductive parasite; Spider

Indexed keywords

MITOCHONDRIAL DNA;

BACTERIUM; CYTOPLASM; ENDOSYMBIONT; EVOLUTIONARY BIOLOGY; GENETIC MARKER; GEOGRAPHICAL VARIATION; LIFE HISTORY TRAIT; MATERNAL EFFECT; MITOCHONDRIAL DNA; REPRODUCTIVE BIOLOGY; SEX RATIO; SPIDER;

ANIMAL; ARTICLE; BACTEROIDETES; CYTOPLASM; EVOLUTION; FEMALE; GENETIC VARIABILITY; GENETICS; MALE; MICROBIOLOGY; OOCYTE; PHYSIOLOGY; REPRODUCTION; SPIDER; SYMBIOSIS;

ANIMALS; BACTEROIDETES; BIOLOGICAL EVOLUTION; CYTOPLASM; DNA, MITOCHONDRIAL; FEMALE; GENETIC VARIATION; MALE; OVUM; REPRODUCTION; SPIDERS; SYMBIOSIS;

ARANEAE; ARTHROPODA; BACTERIA (MICROORGANISMS); CANDIDATUS CARDINIUM; CANDIDATUS CARDINIUM HERTIGII; HOLOCNEMUS PLUCHEI;

EID: 84864012574     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2012.02535.x     Document Type: Article

References (55)

1. Duron, O., Bouchon, D., Boutin, S., Bellamy, L., Zhou, L., Engelstadter, J. et al. 2008a. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol. 6: 27.
2. Duron, O., Hurst, G.D., Hornett, E.A., Josling, J.A. & Engelstadter, J. 2008b. High incidence of the maternally inherited bacterium Cardinium in spiders. Mol. Ecol. 17: 1427-1437.
3. Dyer, K.A. & Jaenike, J.J. 2004. Evolutionary stable infection by a male-killing endosymbiont in Drosophila innubila: molecular evidence from the host and parasite genomes. Genetics 168: 1443-1455.
4. Engelstadter, J. & Hurst, G.D.D. 2009. The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol. Evol. Syst. 40: 127-149.
5. Fellous, S., Duron, O. & Rousset, F. 2011. Adaptation due to symbionts and conflicts between heritable agents of biological information. Nat. Rev. Genet. 12: 663.
6. Goodacre, S.L., Martin, O.Y., Thomas, C.F. & Hewitt, G.M. 2006. Wolbachia and other endosymbiont infections in spiders. Mol. Ecol. 15: 517-527.
7. Goodacre, S.L., Martin, O.Y., Bonte, D., Hutchings, L., Woolley, C., Ibrahim, K. et al. 2009. Microbial modification of host long-distance dispersal capacity. BMC Biol. 7: 32.
8. Gotoh, T., Noda, H. & Ito, S. 2007. Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98: 13-20.
9. Gueguen, G., Vavre, F., Gnankine, O., Peterschmitt, M., Charif, D., Chiel, E. et al. 2010. Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol. Ecol. 19: 4365-4378.
10. Gunnarsson, B., Goodacre, S.L. & Hewitt, G.M. 2009. Sex ratio, mating behaviour and Wolbachia infections in a sheetweb spider. Biol. J. Linn. Soc. 98: 181-186.
11. Haine, E.R. 2008. Symbiont-mediated protection. Proc. R. Soc. B: Biol. Sci. 275: 353-361.
12. Hedges, L.M., Brownlie, J.C., O'Neill, S.L. & Johnson, K.N. 2008. Wolbachia and virus protection in insects. Science 322: 702.
13. Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A. & Werren, J.H. 2008. How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiol. Lett. 281: 215-220.
14. Hunter, M.S., Perlman, S.J. & Kelly, S.E. 2003. A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc. R. Soc. B: Biol. Sci. 270: 2185-2190.
15. Hurst, G.D. & Jiggins, F.M. 2005. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc. R. Soc. B: Biol. Sci. 272: 1525-1534.
16. Hurst, L.D. & McVean, G.T. 1996. Clade selection, reversible evolution and the persistence of selfish elements: the evolutionary dynamics of cytoplasmic incompatibility. Proc. R. Soc. B: Biol. Sci. 263: 97-104.
17. Jaenike, J. & Brekke, T.D. 2010. Defensive endosymbionts: a cryptic trophic level in community ecology. Ecol. Lett. 14: 150-155.
18. Jaenike, J., Unckless, R., Cockburn, S.N., Boelio, L.M. & Perlman, S.J. 2010. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329: 212-215.
19. James, A.C. & Ballard, J.W.O. 2000. Expression of cytoplasmic incompatibility in Drosophila simulans and its impact on infection frequencies and distribution of Wolbachia pipientis. Evolution 54: 1661-1672.
20. Jiggins, F.M. 2003. Male-killing Wolbachia and mitochondrial DNA: selective sweeps, hybrid introgression and parasite population dynamics. Genetics 164: 5-12.
21. Jiggins, F.M. & Hurst, G.D. 2011. Rapid insect evolution by symbiont transfer. Science 332: 185-186.
22. Kenyon, S.G. & Hunter, M.S. 2007. Manipulation of oviposition choice of the parasitoid wasp, Encarsia pergandiella, by the endosymbiotic bacterium Cardinium. J. Evol. Biol. 20: 707-716.
23. Kumar, S., Tamura, K. & Nei, M. 2004. mega3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5: 150-163.
24. Kurtti, T.J., Munderloh, U.G., Andreadis, T.G., Magnarelli, L.A. & Mather, T.N. 1996. Tick cell culture isolation of an intracellular prokaryote from the tick Ixodes scapularis. J. Invertebr. Pathol. 67: 318-321.
25. Martin, O.Y. & Goodacre, S.L. 2009. Widespread infections by the bacterial endosymbiont Cardinium in arachnids. J. Arachnol. 37: 106-108.
26. Marzorati, M., Alma, A., Sacchi, L., Pajoro, M., Palermo, S., Brusetti, L. et al. 2006. A novel Bacteroidetes symbiont is localized in Scaphoideus titanus, the insect vector of Flavescence doree in Vitis vinifera. Appl. Environ. Microbiol. 72: 1467-1475.
27. Moran, N.A., McCutcheon, J.P. & Nakabachi, A. 2008. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42: 165-190.
28. Nakamura, Y., Kawai, S., Yukuhiro, F., Ito, S., Gotoh, T., Kisimoto, R. et al. 2009. Prevalence of Cardinium bacteria in planthoppers and spider mites and taxonomic revision of "Candidatus Cardinium hertigii" based on detection of a new Cardinium group from biting midges. Appl. Environ. Microbiol. 75: 6757-6763.
29. Noel, G.R. & Atibalentja, N. 2006. 'Candidatus Paenicardinium endonii', an endosymbiont of the plant-parasitic nematode Heterodera glycines (Nemata: Tylenchida), affiliated to the phylum Bacteroidetes. Int. J. Syst. Evol. Microbiol. 56: 1697-1702.
30. Oliver, K.M., Russell, J.A., Moran, N.A. & Hunter, M.S. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl Acad. Sci. USA 100: 1803-1807.
31. Oliver, K.M., Campos, J., Moran, N.A. & Hunter, M.S. 2008. Population dynamics of defensive symbionts in aphids. Proc. R. Soc. Lond. B: Biol. Sci. 275: 293-299.
32. Perlman, S.J., Magnus, S.A. & Copley, C.R. 2009. Pervasive associations between Cybaeus spiders and the bacterial symbiont Cardinium. J. Invertebr. Pathol. 103: 150-155.
33. Posada, D. & Crandall, K.A. 1998. modeltest: testing the model of DNA substitution. Bioinformatics 14: 817-818.
34. Provencher, L.M., Morse, G.E., Weeks, A.R. & Normark, B.B. 2005. Parthenogenesis in the Aspidiotus nerii complex (Hemiptera: Diaspididae): a single origin of a worldwide, polyphagous lineage associated with Cardinium bacteria. Ann. Entomol. Soc. Am. 98: 629-635.
35. Rogers, S.O. & Bendich, A.J. 1988. Extraction of DNA from plant tissues. In Plant Molecular Biology Manuel, vol. A6 (S.B. Gelvin & R.A. Schilperoort, eds), pp. 1-10. Kluwer Academic Publishers, Boston, MA.
36. Ros, V.I. & Breeuwer, J.A. 2009. The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni. Heredity 102: 413-422.
37. Russell, J.A. & Moran, N.A. 2006. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc. Biol. Sci. 273: 603-610.
38. Saridaki, A. & Bourtzis, K. 2010. Wolbachia: more than just a bug in insect genitals. Curr. Opin. Microbiol. 13: 67-72.
39. Scarborough, C.L., Ferrari, J. & Godfray, H.C. 2005. Aphid protected from pathogen by endosymbiont. Science 310: 1781.
40. Schulenburg, J.H.G.v.d., Hurst, G.D.D., Tetzlaff, D., Booth, G.E., Zakharov, I.A. & Majerus, M.E.N. 2002. History of infection with different male-killing bacteria in the two-spot ladybird beetle Adalia bipunctata revealed through mitochondrial DNA analysis. Genetics 160: 1075-1086.
41. Shoemaker, D.D., Keller, G. & Ross, K.G. 2003. Effects of Wolbachia on mtDNA variation in two fire ant species. Mol. Ecol. 12: 1757-1771.
42. Skow, C. & Jakob, E. 2003. Effects of maternal body size on clutch size and egg weight in a Pholcid spider (Holocnemus Pluchei). J. Arachnol. 31: 305-308.
43. Swofford, D.L. 2002. paup*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. (ed. S. Associates), Sunderland, MA.
44. Teixeira, L., Ferreira, A. & Ashburner, M. 2008. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 6: e2.
45. Vanthournout, B., Swaegers, J. & Hendrickx, F. 2011. Spiders do not escape reproductive manipulations by Wolbachia. BMC Evol. Biol. 11: 15.
46. Verne, S., Johnson, M., Bouchon, D. & Grandjean, F. 2012. Effects of parasitic sex-ratio distorters on host genetic structure in the Armadillidium vulgare-Wolbachia association. J. Evol. Biol. 25: 264-276.
47. Weeks, A.R. & Stouthamer, R. 2004. Increased fecundity associated with infection by a cytophaga-like intracellular bacterium in the predatory mite, Metaseiulus occidentalis. Proc. Biol. Sci. 271(Suppl 4): S193-S195.
48. Weeks, A., Marec, F. & Breeuwer, J.A. 2001. A mite species that consists entirely of haploid females. Science 29: 2479-2482.
49. Weeks, A.R., Velten, R. & Stouthamer, R. 2003. Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc. Biol. Sci. 270: 1857-1865.
50. Werren, J.H., Baldo, L. & Clark, M.E. 2008. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6: 741-751.
51. White, J.A., Kelly, S.E., Perlman, S.J. & Hunter, M.S. 2009. Cytoplasmic incompatibility in the parasitic wasp Encarsia inaron: disentangling the roles of Cardinium and Wolbachia symbionts. Heredity 102: 483-489.
52. White, J.A., Kelly, S.E., Cockburn, S.N., Perlman, S.J. & Hunter, M.S. 2010. Endosymbiont costs and benefits in a parasitoid infected with both Wolbachia and Cardinium. Heredity 106: 585-591.
53. Zchori-Fein, E. & Perlman, S.J. 2004. Distribution of the bacterial symbiont Cardinium in arthropods. Mol. Ecol. 13: 2009-2016.
54. Zchori-Fein, E., Gottlieb, Y., Kelly, S.E., Brown, J.K., Wilson, J.M., Karr, T.L. et al. 2001. A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proc. Natl Acad. Sci. USA 98: 12555-12560.
55. Zchori-Fein, E., Perlman, S.J., Kelly, S.E., Katzir, N. & Hunter, M.S. 2004. Characterization of a 'Bacteroidetes' symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of 'Candidatus Cardinium hertigii'. Int. J. Syst. Evol. Microbiol. 54: 961-968.