Cytoplasmic feminizing elements in a two-population model: Infection dynamics, gene flow modification, and the spread of autosomal suppressors

Journal of Evolutionary Biology

Volumn 23, Issue 12, 2010, Pages 2558-2568

  Kobayashi, Y ^a   Telschow, A ^b  

^a KYOTO UNIVERSITY   (Japan)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Effective migration rate; Feminization; Isopoda; Microsporidia; Neo female; Parasite; Sex ratio distorter; Wolbachia

Indexed keywords

BACTERIUM; CHROMOSOME; CYTOPLASM; FEMINIZATION; GENE FLOW; HOST-PARASITE INTERACTION; ISOPOD; MIGRATION; PARASITE TRANSMISSION; PARASITIC DISEASE; POPULATION MODELING; SEX DETERMINATION; SEX RATIO; VIABILITY;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; EVOLUTION; FEMALE; GENDER AND SEX; GENE FLOW; GENETICS; HOST PARASITE INTERACTION; MALE; PHYSIOLOGY; POPULATION DYNAMICS; SEX CHROMOSOME; SEX RATIO; WOLBACHIA;

ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; GENE FLOW; HOST-PARASITE INTERACTIONS; MALE; MODELS, GENETIC; POPULATION DYNAMICS; SEX CHROMOSOMES; SEX DETERMINATION PROCESSES; SEX RATIO; WOLBACHIA;

ISOPODA; MICROSPORIDIA; WOLBACHIA;

EID: 78449239581     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2010.02116.x     Document Type: Article

References (47)

1. Andreadis, T.G. & Hall, D.W. 1979. Development, ultrastructure, and mode of transmission of Amblyospora sp. (Microspora) in the mosquito. J. Protozool. 26: 444-452.
2. Bandi, C., Dunn, A.M., Hurst, G.D.D. & Rigaud, T. 2001. Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends Ecol. Evol. 17: 88-94.
3. Barton, N.H., & Bengtsson, B.O. 1986. The barrier to genetic exchange between hybridizing populations. Heredity 56: 357-376.
4. Bengtsson, B.O. 1985. The flow of genes through a genetic barrier. In: Evolution Essays in Honour of John Maynard Smith (J.J. Greenwood, P.H. Harvey, & M. Slatkin, eds), pp. 31-42. Cambridge University Press, Cambridge.
5. Broquet, T. & Petit, E.J. 2009. Molecular estimation of dispersal for ecology and population genetics. Annu. Rev. Ecol. Syst. 40: 193-216.
6. Budar, F., Touzet, P. & De Paepe, R. 2003. The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited. Genetica 117: 3-16.
7. Bull, J.J. 1983. Evolution of Sex Determining Mechanisms. Benjamin Cummings, CA.
8. Caubet, Y., Hatcher, M.J., Mocquard, J.P. & Rigaud, T. 2000. Genetic conflict and changes in heterogametic mechanisms of sex determination. J. Evol. Biol. 13: 766-777.
9. Engelstädter, J. & Hurst, G.D.D. 2007. The impact of male-killing bacteria on host evolutionary processes. Genetics 175: 245-254.
10. Engelstädter, J. & Telschow, A. 2009. Cytoplasmic incompatibility and host population structure. Heredity 103: 196-207.
11. Ewing, G., Nicholls, G. & Rodrigo, A. 2004. Using temporally spaced sequences to simultaneously estimated migration rates, mutation rate and population sizes in measurably evolving populations. Genetics 168: 2407-2420.
12. Haine, E.R., Motreuil, S. & Rigaud, T. 2007. Infection by a vertically-transmitted microsporidian parasite is associated with a female-biased sex ratio and survival advantage in the amphipod Gammarus roeseli. Parasitology 134: 1363-1367.
13. Hatcher, M.J. 2000. Persistence of selfish genetic elements: population structure and conflict. Trends Ecol. Evol. 15: 271-277.
14. 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.
15. Hurst, L.D. 1991. The incidence and evolution of cytoplasmic male killers. Proc. R. Soc. Lond. B 244: 91-99.
16. Hurst, G.D.D., Hurst, L.D. & Majerus, M.E.N. 1997. Cytoplasmic sex-ratios distorters. In: Influential Passengers: Inherited Microorganisms and Arthropod Reproduction (S.L. O'Neill, A.A. Hoffmann & J.H. Werren, eds), pp. 125-154. Oxford University Press, New York.
17. Hurst, G.D.D. & Werren, J.H. 2001. The role of selfish genetic elements in eukaryotic evolution. Nat. Rev. Genet. 2: 597-606.
18. Juchault, P. & Mocquard, J.P. 1993. Transfer of a parasitic sex factor to the nuclear genome of the host: a hypothesis on the evolution of sex-determining mechanisms in the terrestrial Isopod Armadillidium vulgare Latr. J. Evol. Biol. 6: 511-528.
19. Juchault, P., Rigaud, T. & Mocquard, J.P. 1992. Evolution of sex-determining mechanisms in a wild population of Armadillidium 'vulgare Latr. (Crustacea, Isopoda): competition between two feminizing parasitic sex factors. Heredity 69: 382-390.
20. Juchault, P., Rigaud, T. & Mocquard, J.P. 1993. Evolution of sex determination and sex ratio variability in wild populations of Armadillidium vulgare (Latr.) (Crustacea, Isopoda): a case study in conflict resolution. Acta Dcol. 14: 547-562.
21. Kobayashi, Y., Hammerstein, P. & Telschow, A. 2008. The neutral effective migration rate in a mainland-island context. Theor. Popul. Biol. 74: 84-92.
22. Mautner, S.I., Cook, K.A., Forbes, M.R., McCurdy, D.G. & Dunn, A.M. 2007. Evidence for sex ratio distortion by a new microsporidian parasite of a Corophiid amphipod. Parasitology 134: 1567-1573.
23. Moreau, J., Bertin, A., Caubet, Y. & Rigaud, T. 2001. Sexual selection in an isopod with Wolbachia-induced sex reversal: males prefer real females. J. Evol. Biol. 14: 388-394.
24. Rigaud, T. & Juchault, P. 1992. Genetic control of the vertical transmission of a cytoplasmic sex factor in Armadillidium vulgare Latr. (Crustacea, Oniscidea). Heredity 68: 47-52.
25. Rigaud, T. & Juchault, P. 1993. Conflict between feminizing sex ratio distorters and an autosomal masculinizing gene in the terrestrial isopod Armadillidium vulgare Latr. Genetics 133: 247-252.
26. Rigaud, T. & Juchault, P. 1998. Sterile intersexuality in an isopod induced by the interaction between a bacterium (Wolbachia) and the environment. Can. J. Zool. 76: 493-499.
27. Rigaud, T., Juchault, P. & Mocquard, J.P. 1991. Experimental study of temperature effects on the sex ratio of broods in terrestrial Crustacea Armadillidium vulgare Latr. Possible implications in natural populations. J. Evol. Biol. 4: 603-617.
28. Rigaud, T., Juchault, P. & Mocquard, J.P. 1997. The evolution of sex determination in isopod crustaceans. Bioessays 19: 409-416.
29. Rigaud, T. & Moreau, J. 2004. A cost of Wolbachia-induced sex reversal and female-biased sex ratios: decrease in female fetility after sperm depletion in a terrestrial isopod. Proc. Biol. Sci. 271: 1941-1946.
30. Rousset, F. 1999. Genetic differentiation in populations with different classes of individuals. Theor. Popul. Biol. 55: 297-308.
31. Rousset, F. 2004. Genetic Structure and Selection in Subdivided Populations. Princeton University Press, Princeton.
32. Saumitou-Laprade, P., Cuguen, J. & Vernet, P. 1994. Cytoplasmic male sterility in plants: molecular evidence and the nucleocytoplasmic conflict. Trends Ecol. Evol. 9: 431-435.
33. Taylor, D.R. 1990. Evolutionary consequences of cytoplasmic sex ratio distorters. Evol. Ecol. 4: 235-248.
34. Telschow, A., Hammerstein, P. & Werren, J.H. 2002. The effect of Wolbachia on genetic divergence between populations: models with two-way migration. Am. Nat. 160: S54-S66.
35. Telschow, A., Engelstädter, J., Yamamura, N. & Hammerstein, P. 2006. Asymmetric gene flow and constraints on adaptation caused by sex ratio distorters. J. Evol. Biol. 19: 869-878.
36. Telschow, A., Flor, M., Kobayashi, Y., Hammerstein, P. & Werren, J.H. 2007. Wolbachia-induced unidirectional cytoplasmic incompatibility and speciation: mainland-island model. PLoS ONE 2: e701.
37. Terry, R.S., Smith, J.E., Bouchon, D., Rigaud, T., Duncanson, P., Sharpe, R.G. & Dunn, A.M. 1999. Ultrastructural characterisation and molecular taxonomic identification of Nosema granulosis n. sp., a transovarially transmitted feminising (TTF) microsporidium. J. Eukaryot. Microbiol. 46: 492-499.
38. Terry, R.S., Smith, J.E., Sharpe, R.G., Rigaud, T., Littlewood, D.T.J., Ironside, J.E., Rollinson, D., Bouchon, D., MacNeil, C., Dick, J.T.A. & Dunn, A.M. 2004. Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proc. Biol. Sci. 271: 1783-1789.
39. Vitalis, R. & Couvet, D. 2001. Estimation of effective population size and migration rate from one- and two-locus identity measures. Genetics 157: 911-925.
40. Wang, J. & Whitlock, M.C. 2003. Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163: 429-446.
41. Werren, J.H. 1987. The coevolution of autosomal and cytoplasmic sex ratio factors. J. Theor. Biol. 124: 317-334.
42. Werren, J.H., Baldo, L. & Clark, M.E. 2008. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6: 741-751.
43. Werren, J.H. & Beukeboom, L.W. 1998. Sex determination, sex ratios, and genetic conflict. Annu. Rev. Ecol. Syst. 29: 233-261.
44. Werren, J.H., Nur, U. & Eickbush, D. 1987. An extrachromosomal factor causing loss of paternal chromosomes. Nature 327: 75-76.
45. Werren, J.H., Nur, U. & Wu, C.-I. 1988. Selfish genetic elements. Trends Ecol. Evol. 3: 297-302.
46. Werren, J.H. & Stouthamer, R. 2003. PSR (paternal sex ratio) chromosomes: the ultimate selfish genetic elements. Genetica 117: 85-101.
47. Werren, J.H. & Van Den Assem, J. 1986. Experimental analysis of a paternally inherited extrachromosomal factor. Genetics 114: 217-233.