Do vertically transmitted symbionts co-existing in a single host compete or cooperate? A modelling approach

Journal of Evolutionary Biology

Volumn 21, Issue 1, 2008, Pages 145-161

  Vautrin, E ^a,b   Genieys, S ^c   Charles, S ^b   Vavre, F ^b  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

Competition; Cooperation; Cytoplasmic incompatibility; Matrix based models; Multiple infections; Mutualism; Wolbachia

Indexed keywords

BACTERIUM; COEXISTENCE; COMPETITION (ECOLOGY); COOPERATIVE BEHAVIOR; CYTOPLASMIC INCOMPATIBILITY; FECUNDITY; FITNESS; MUTUALISM; POPULATION BOTTLENECK; POPULATION DYNAMICS; POPULATION MODELING;

WOLBACHIA;

EID: 37149027196     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2007.01460.x     Document Type: Article

References (69)

1. Aksoy, S. 1995. Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. Int. J. Syst. Bacteriol. 45 : 848 851.
2. Baumann, P., Baumann, L., Lai, C.Y., Rouhbakhsh, D., Moran, N.A. Clark, M.A. 1995. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu. Rev. Microbiol. 49 : 55 94.
3. Brown, S.P., Hochberg, M.E. Grenfell, B.T. 2002. Does multiple infection select for raised virulence Trends Microbiol. 10 : 401 405.
4. Buchner, P. 1965. Endosymbiosis of Animals with Plant Microorganisms. Wiley, New York.
5. Bull, J.J., Molineux, I.J. Rice, W.R. 1991. Selection of benevolence in a host-parasite system. Evolution 45 : 875 882.
6. Chao, L., Hanley, K.A., Burch, C.L., Dahlberg, C. Turner, P.E. 2000. Kin selection and parasite evolution: higher and lower virulence with hard and soft selection. Q. Rev. Biol. 75 : 261 275.
7. Chen, X., Li, S. Aksoy, S. (1999). Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J. Mol. Evol. 48 : 49 58.
8. Cheng, Q., Ruel, T.D., Zhou, W., Moloo, S.K., Majiwa, P., O'Neill, S.L. Aksoy, S. 2000. Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp. Med. Vet. Entomol. 14 : 44 50.
9. Clark, M.A., Moran, N.A. Baumann, P. 1999. Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol. Biol. Evol. 16 : 1586 1598.
10. Dale, C. Welburn, S.C. 2001. The endosymbionts of tsetse flies: manipulating host-parasite interactions. Int. J. Parasitol. 31 : 628 631.
11. Day, T. Proulx S.R. 2004. A general theory for the evolutionary dynamics of virulence. Am. Nat. 163 : E40 E63.
12. Diekmann, O. 2004. A beginners guide to adaptive dynamics. In : Mathematical Modelling of Population Dynamics, Vol. 63 (R. Rudnicki, ed.), pp. 47 86. Banach Center Publications, Institute of Mathematics, Polish Academy of Sciences, Warsaw.
13. Ebert, D. Herre, E.A. 1996. The evolution of parasitic diseases. Parasitol. Today 12 : 96 101.
14. Egas, M., Vala, F. Breeuwer, J.A. 2002. On the evolution of cytoplasmic incompatibility in haplodiploid species. Evolution 56 : 1101 1109.
15. Engelstadter, J., Telschow, A. Hammerstein, P. 2004. Infection dynamics of different Wolbachia-types within one host population. J. Theor. Biol. 231 : 345 355.
16. Engelstadter, J., Hammerstein, P. Hurst, G.D. 2007. The evolution of endosymbiont density in doubly infected host species. J. Evol. Biol. 20 : 685 695.
17. Frank, S.A. 1992. A kin selection model for the evolution of virulence. Proc. R. Soc. Lond. Ser. B 250 : 195 197.
18. Frank, S.A. 1996. Models of parasite virulence. Q. Rev. Biol. 71 : 37 78.
19. Frank, S.A. 1998. Dynamics of cytoplasmic incompatability with multiple Wolbachia infections. J. Theor. Biol. 192 : 213 218.
20. Gardner, A., West, S.A. Buckling, A. 2004. Bacteriocins, spite and virulence. Proc. R. Soc. Lond. Ser. B 271 : 1529 1535.
21. Goto, S., Anbutsu, H. Fukatsu, T. 2006. Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Appl. Environ. Microbiol. 72 : 4805 4810.
22. Gower, C.M. Webster, J.P. 2005. Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution 59 : 544 553.
23. Hardin, G. 1968. The tragedy of the commons. Science 162 : 1243 1248.
24. Hartl, D.L. Clark, A.G. 1997. Principles of Population Genetics, 3rd edn. Sinauer Associates, Inc., Sunderland, MA.
25. Haynes, S., Darby, A.C., Daniell, T.J., Webster, G., Van Veen, F.J., Godfray, H.C., Prosser, J.I. Douglas, A.E. 2003. Diversity of bacteria associated with natural aphid populations. Appl. Environ. Microbiol. 69 : 7216 7223.
26. Herre, E.A., Knowlton, N., Mueller, U.G. Rehner, S.A. 1999. The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol. Evol. 14 : 49 53.
27. Hiroki, M., Tagami, Y., Miura, K. Kato, Y. 2004. Multiple infection with Wolbachia inducing different reproductive manipulations in the butterfly Eurema hecabe. Proc. R. Soc. Lond. Ser. B 271 : 1751 1755.
28. Hodgson, D.J., Hitchman, R.B., Vanbergen, A.J., Hails, R.S., Possee, R.D. Cory, J.S. 2004. Host ecology determines the relative fitness of virus genotypes in mixed-genotype nucleopolyhedrovirus infections. J. Evol. Biol. 17 : 1018 1025.
29. 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. Lond. Ser. B 263 : 97 104.
30. Ikeda, T., Ishikawa, H. Sasaki, T. 2003. Regulation of Wolbachia density in the Mediterranean flour moth, Ephestia kuehniella, and the almond moth, Cadra cautella. Zool. Sci. 20 : 153 157.
31. Jamnongluk, W., Kittayapong, P., Baimai, V. O'Neill, S.L. 2002. Wolbachia infections of tephritid fruit flies: molecular evidence for five distinct strains in a single host species. Curr. Microbiol. 45 : 255 260.
32. Keller, L. Surette, M.G. 2006. Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4 : 249 258.
33. Koga, R., Tsuchida, T. Fukatsu, T. 2003. Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. R. Soc. Lond. Ser. B 270 : 2543 2550.
34. Lipsitch, M., Siller, S. Nowak, M.A. 1996. The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50 : 1729 1741.
35. Massey, R.C., Buckling, A. Ffrench-Constant, R. 2004. Interference competition and parasite virulence. Proc. R. Soc. Lond. Ser. B 271 : 785-788.
36. May, R.M. & Anderson, R.M. 1983. Parasite-host coevolution. In : Coevolution (D. J. Futuyama M. Slatkin, eds. pp. 186 206. Sinauer, Sunderland, MA.
37. McGraw, E.A., Merritt, D.J., Droller, J.N. O'Neill, S.L. 2002. Wolbachia density and virulence attenuation after transfer into a novel host. Proc. Natl. Acad. Sci. USA 99 : 2918 2923.
38. Mira, A. Moran, N.A. 2002. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb. Ecol. 44 : 137 143.
39. Montenegro, H., Solferini, V.N., Klaczko, L.B. Hurst, G.D.D. 2005. Male-killing Spiroplasma naturally infecting Drosophila melanogaster. Insect Mol. Biol. 14 : 281 287.
40. Montllor, C., Maxmen, A. Alexander, H. 2002. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27 : 189 195.
41. Moran, N.A. Wernegreen, J.J. 2000. Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol. Evol. 15 : 321 326.
42. Mouton, L., Henri, H., Bouletreau, M. Vavre, F. 2003. Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol. Ecol. 12 : 3459 3465.
43. Mouton, L., Dedeine, F., Henri, H., Bouletreau, M., Profizi, N. Vavre, F. 2004. Virulence, multiple infections and regulation of symbiotic population in the Wolbachia-Asobara tabida Symbiosis. Genetics 168 : 181 189.
44. 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.
45. Parsek, M.R. Greenberg, E.P. 2005. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol. 13 : 27 33.
46. Read, A.F. Taylor, L.H. 2001. The ecology of genetically diverse infections. Science 292 : 1099 1102.
47. Reuter, M. Keller, L. 2003. High levels of multiple Wolbachia infection and recombination in the ant Formica exsecta. Mol. Biol. Evol. 20 : 748 753.
48. Rousset, F., Braig, H.R. O'Neill, S.L. 1999. A stable triple Wolbachia infection in Drosophila with nearly additive incompatibility effects. Heredity 82 : 620 627.
49. Russell, J.A. Moran, N.A. 2006. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc. R. Soc. Lond. Ser. B 273 : 603 610.
50. Sachs, J.L. Bull, J.J. 2005. Experimental evolution of conflict mediation between genomes. Proc. Natl. Acad. Sci. USA 102 : 390 395.
51. Sachs, J.L., Mueller, U.G., Wilcox, T.P. Bull, J.J. 2004. The evolution of cooperation. Q. Rev. Biol. 79 : 135 160.
52. Sakurai, M., Koga, R., Tsuchida, T., Meng, X.Y. Fukatsu, T. 2005. Rickettsia symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropism, effect on host fitness, and interaction with the essential symbiont Buchnera. Appl. Environ. Microbiol. 71 : 4069 4075.
53. Scarborough, C.L., Ferrari, J. Godfray, H.C. 2005. Aphid protected from pathogen by endosymbiont. Science 310 : 1781.
54. Schjorring, S. Koella, J.C. 2003. Sub-lethal effects of pathogens can lead to the evolution of lower virulence in multiple infections. Proc. R. Soc. Lond. Ser. B 270 : 189 193.
55. Shapiro, J.A. 1998. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52 : 81 104.
56. Sinkins, S.P., Braig, H.R. O'Neill, S.L. 1995. Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proc. R. Soc. Lond. Ser. B 261 : 325 330.
57. Stewart, A.D., Logsdon, J.M. Jr. Kelley, S.E. 2005. An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59 : 730 739.
58. Stouthamer, R., Breeuwer, J.A. Hurst, G.D. 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53 : 71 102.
59. Thao, M.L., Clark, M.A., Baumann, L., Brennan, E.B., Moran, N.A. Baumann, P. 2000. Secondary endosymbionts of psyllids have been acquired multiple times. Curr. Microbiol. 41 : 300 304.
60. Tsuchida, T., Koga, R., Shibao, H., Matsumoto, T. Fukatsu, T. 2002. Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 11 : 2123 2135.
61. Tsuchida, T., Koga, R. Fukatsu, T. 2004. Host plant specialization governed by facultative symbiont. Science 303 : 1989.
62. Turelli, M. 1994. Evolution of incompatibility-inducing microbes and their hosts. Evolution 48 : 1500 1513.
63. van Baalen, M. Sabelis, M.W. 1995. The dynamics of multiple infection and the evolution of virulence. Am. Nat. 146 : 881 910.
64. Vautrin, E., Charles, S., Genieys, S. Vavre, F. 2007. Evolution and invasion dynamics of multiple infections with Wolbachia investigated using matrix based models. J. Theor. Biol. 245 : 197 209.
65. Vavre, F., Fleury, F., Lepetit, D., Fouillet, P. Bouletreau, M. 1999. Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol. Biol. Evol. 16 : 1711 1723.
66. Vavre, F., Fouillet, P. Fleury, F. 2003. Between- and within-host species selection on cytoplasmic incompatibility-inducing Wolbachia in haplodiploids. Evolution 57 : 421 427.
67. Werren, J.H. O'Neill, S.L. 1998. The evolution of heritable symbionts. In : Influential Passengers: Inherited Microorganisms and Arthropod Reproduction (S. L. O'Neill, A. A. Hoffmann J. H. Werren, eds.), pp. 1 47. Oxford University Press, New York.
68. West, S.A. Buckling, A. 2003. Cooperation, virulence and siderophore production in bacterial parasites. Proc. R. Soc. Lond. Ser. B 270 : 37 44.
69. Zchori-Fein, E. Brown, J.K. 2002. Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Ann. Entomol. Soc. Am. 95 : 711 718.