Effects of parasitic sex-ratio distorters on host genetic structure in the Armadillidium vulgare-Wolbachia association

Journal of Evolutionary Biology

Volumn 25, Issue 2, 2012, Pages 264-276

  Verne, S ^a,b   Johnson, M ^a   Bouchon, D ^a   Grandjean, F ^a  

^a UNIVERSITÉ DE POITIERS   (France)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Armadillidium vulgare; Feminization; Microsatellite loci; Mitochondrial DNA; Wolbachia

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

BACTERIAL DISEASE; DISEASE PREVALENCE; EGG; FEMINIZATION; GENETIC MARKER; GENETIC STRUCTURE; HOST-PARASITE INTERACTION; ISOPOD; MITOCHONDRIAL DNA; POLYMORPHISM; SEX RATIO; VERTICAL TRANSMISSION;

ANIMAL; ARTICLE; CHEMISTRY; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENETIC POLYMORPHISM; GENETICS; HUMAN; ISOPODA; MALE; MICROBIOLOGY; PHYSIOLOGY; SEX DETERMINATION PROCESS; SEX RATIO; WOLBACHIA;

ANIMALS; DNA, MITOCHONDRIAL; FEMALE; HUMANS; ISOPODA; LINKAGE DISEQUILIBRIUM; MALE; MICROSATELLITE REPEATS; POLYMORPHISM, GENETIC; SEX DETERMINATION PROCESSES; SEX RATIO; WOLBACHIA;

ARMADILLIDIUM VULGARE; CRUSTACEA; ONISCIDEA; WOLBACHIA;

EID: 84855843666     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02413.x     Document Type: Article

References (73)

1. Ballard, J.W. 2000. Comparative genomics of mitochondrial DNA in Drosophila simulans. J. Mol. Evol. 51: 64-75.
2. Bazin, E., Glémin, S. & Galtier, N. 2006. Population size does not influence mitochondrial genetic diversity in animals. Science 312: 570-572.
3. Behura, S., Sahu, S., Mohan, M. & Nair, S. 2001. Wolbachia in the Asian rice gall midge, Orseolia oryzae (Wood-Mason): correlation between host mitotypes and infection status. Insect Mol. Biol. 10: 163-171.
4. Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N. & Bonhomme, F. 2004. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations.
5. Bouchon, D., Rigaud, T. & Juchault, P. 1998. Evidence for wide-spread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc. R. Soc. London B 265: 1081-1090.
6. Bouchon, D., Cordaux, R. & Grève, P. 2008. Feminizing Wolbachia and the evolution of sex determination in isopods. In: Insect Symbiosis, Volume 3 (K. Bourtzis & T.A. Miller, eds), pp. 273-294. CRC Press, Boca Raton.
7. Clement, M., Posada, D. & Crandall, K.A. 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9: 1657-1659.
8. Cordaux, R., Michel-Salzat, A. & Bouchon, D. 2001. Wolbachia infection in crustaceans: novel hosts and potential routes for horizontal transmission. J. Evol. Biol. 14: 237-243.
9. Cordaux, R., Michel-Salzat, A., Frelon-Raimond, M., Rigaud, T. & Bouchon, D. 2004. Evidence for a new feminizing Wolbachia strain in the isopod Armadillidium vulgare: evolutionary implications. Heredity 93: 78-84.
10. Cordaux, R., Bouchon, D. & Grève, P. 2011. The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends Genet 27: 332-341.
11. Cornuet, J.M. & Luikart, G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014.
12. Dannowski, J., Flor, M., Telschow, A. & Hammerstein, P. 2009. The effect of sibmating on the infection dynamics of male-killing bacteria. Evolution 63: 2525-2534.
13. Dean, M.D., Ballard, K.J., Glass, A. & Ballard, J.W. 2003. Influence of two Wolbachia strains on population structure of East African Drosophila simulans. Genetics 165: 1959-1969.
14. Dewayne Shoemaker, D., Keller, G. & Ross, K.G. 2003. Effects of Wolbachia on mtDNA variation in two fire ant species. Mol. Ecol. 12: 1757-1771.
15. Engelstädter, J., Telschow, A. & Yamamura, N. 2008. Coexistence of cytoplasmic incompatibility and male-killing-inducing endosymbionts, and their impact on host gene flow. Theor. Popul. Biol. 73: 125-133.
16. Excoffier, L., Laval, G. & Schneider, S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1: 47-50.
17. Fu, Y.-X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.
18. Gaggiotti, O.E., Lange, O., Rassmann, K. & Gliddon, C. 1999. A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol. Ecol. 8: 1513-1520.
19. Girman, D.J., Vilà, C., Geffen, E., Creel, S., Mills, M.G.L., McNutt, J.W. et al. 2001. Patterns of population subdivision, gene flow and genetic variability in the African wild dog (Lycaon pictus). Mol. Ecol. 10: 1703-1723.
20. Goudet, J. 1995. FSTAT (Version 1.2): a computer program to calculate F-statistics. J. Hered. 86: 485-486.
21. Goudet, J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from Updated from Goudet (1995).
22. Grandjean, F., Rigaud, T., Raimond, R., Juchault, P. & Souty-Grosset, C. 1993. Mitochondrial DNA polymorphism and feminizing sex factors dynamics in a natural population of Armadillidium vulgare (Crustacea, Isopoda). Genetica 92: 55-60.
23. Guo, S.W. & Thompson, E.A. 1992. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48: 361-372.
24. Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41: 95-98.
25. Hatcher, M.J. 2000. Persistence of selfish genetic elements: population structure and conflict. Trends Ecol. Evol. 15: 271-277.
26. Hatcher, M.J., Taneyhill, D.E., Dunn, A.M. & Tofts, C. 1999. Population dynamics under parasitic sex ratio distortion. Theor. Popul. Biol. 56: 11-28.
27. Hatcher, M.J., Dunn, A.M. & Tofts, C. 2000. The coexistence of hosts and sex ratio distorters in structured populations. Evol. Ecol. Res. 2: 185-205.
28. 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. Biol. Sci. 272: 1525-1534.
29. Ironside, J.E., Smith, J.E., Hatcher, M.J., Sharpe, R.G., Rollinson, D. & Dunn, A.M. 2003. Two species of feminizing microsporidian parasite coexist in populations of Gammarus duebeni. J. Evol. Biol. 16: 467-473.
30. Jeyaprakash, A. & Hoy, M.A. 2000. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol. Biol. 9: 393-405.
31. Juchault, P. & Mocquart, 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.
32. 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 Oecol. 14: 547-562.
33. Kalinowski, S.T. 2004. Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv. Genet. 5: 539-543.
34. Kalinowski, S.T. 2005. HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol. Ecol. Notes 5: 187-189.
35. Kobayashi, Y. & Telschow, A. 2010. Cytoplasmic feminizing elements in a two-population model: infection dynamics, gene flow modification, and the spread of autosomal suppressors. J. Evol. Biol. 23: 2558-2568.
36. Kobayashi, Y., Achaz, G. & Telschow, A. 2011. Effect of parasitic sex-ratio distorters on host gene frequencies in a mainland-island context. J. Evol. Biol. 24: 1695-1705.
37. Legrand, J.J. & Juchault, P. 1969. Le déterminisme de l'intersexualité chez les crustacés isopodes terrestres: corrélations entre intersexualité et monogénie. CR. Acad. Sci., Ser. III. Sci. Vie/Life Sci. 268: 1647-1649.
38. Legrand, J.-J., Juchault, P., Heily, G. & Le Bote, C. 1984. Nouvelles données sur le déterminisme génétique et épigénétique de la monogénie chez le crustacé isopode terrestre Armadillidium vulgare Latr. Genet. Sel. Evol. 16: 57.
39. Lewontin, R.C. 1964. The interaction of selection and linkage. I. General considerations; heterotic models. Genetics 49: 49-67.
40. Luikart, G. & Cornuet, J.M. 1998. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol. 12: 228-237.
41. Marcadé, I.I., Souty-Grosset, C., Bouchon, D., Rigaud, T. & Raimond, R. 1999. Mitochondrial DNA variability and Wolbachia infection in two sibling woodlice species. Heredity 83(Pt 1): 71-78.
42. Marcadé, I., Cordaux, R., Doublet, V., Debenest, C., Bouchon, D. & Raimond, R. 2007. Structure and evolution of the atypical mitochondrial genome of Armadillidium vulgare (Isopoda, Crustacea). J. Mol. Evol. 65: 651-659.
43. Meiklejohn, C.D., Montooth, K.L. & Rand, D.M. 2007. Positive and negative selection on the mitochondrial genome. Trends Genet. 23: 259-263.
44. Meirmans, P.G. & Van Tienderen, P.H. 2004. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 4: 792-794.
45. Michel-Salzat, A., Cordaux, R. & Bouchon, D. 2001. Wolbachia diversity in the Porcellionides pruinosus complex of species (Crustacea: Oniscidea): evidence for host-dependent patterns of infection. Heredity 87: 428-434.
46. Moreau, J. & Rigaud, T. 2003. Variable male potential rate of reproduction: high male mating capacity as an adaptation to parasite-induced excess of females? Proc. R. Soc. London B 270: 1535.
47. 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.
48. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590.
49. Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.
50. Nei, M. & Li, W.H. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. U S A 76: 5269-5273.
51. Piry, S., Luikart, G. & Cornuet, J.-M. 1999. Bottleneck: a computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 90: 502-503.
52. Raymond, M. & Rousset, F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249.
53. Rigaud, T. 1999. Further Wolbachia endosymbiont diversity: a tree hiding in the forest? Trends Ecol. Evol. 14: 212-213.
54. 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. Retrieved April 16, 2011.
55. 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.
56. Rigaud, T. & Juchault, P. 1995. Success and failure of horizontal transfers of feminizing Wolbachia endosymbionts in woodlice. J. Evol. Biol. 8: 249-255.
57. Rigaud, T., Antoine, D., Marcadé, I. & Juchault, P. 1997. The effect of temperature on sex ratio in the isopod Porcellionides pruinosus: environmental sex determination or a by-product of cytoplasmic sex determination? Evol. Ecol. 11: 205-215.
58. Rigaud, T., Bouchon, D., Souty-Grosset, C. & Raimond, R. 1999. Mitochondrial DNA polymorphism, sex ratio distorters and population genetics in the isopod Armadillidium vulgare. Genetics 152: 1669-1677.
59. Rossiter, S.J., Jones, G., Ransome, R.D. & Barratt, E.M. 2000. Genetic variation and population structure in the endangered greater horseshoe bat Rhinolophus ferrumequinum. Mol. Ecol. 9: 1131-1135.
60. Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219-1228.
61. Rozas, J. & Rozas, R. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174-175.
62. Scribner, K.T., Petersen, M.R., Fields, R.L., Talbot, S.L., Pearce, J.M. & Chesser, R.K. 2001. Sex-biased gene flow in spectacled eiders (Anatidae): inferences from molecular markers with contrasting modes of inheritance. Evolution 55: 2105-2115.
63. Seielstad, M.T., Minch, E. & Cavalli-Sforza, L.L. 1998. Genetic evidence for a higher female migration rate in humans. Nat. Genet. 20: 278-280.
64. Sokal, R.R. & Rohlf, F.J. 1995. Biometry: The Principles and Practice of Statistics in Biological Research. W. H. Freeman and Co, New York.
65. Taylor, D.R. 1990. Evolutionary consequences of cytoplasmic sex-ratio distorters. Evol. Ecol. 4: 235-248.
66. 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.
67. Telschow, A., Engelstädter, J., Yamamura, N., Hammerstein, P. & Hurst, G. 2006. Asymmetric gene flow and constraints on adaptation caused by sex ratio distorters. J. Evol. Biol. 19: 869-878.
68. Templeton, A.R., Crandall, K.A. & Sing, C.F. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132: 619.
69. Verne, S., Puillandre, N., Brunet, G., Gouin, N., Samollow, P.B., Anderson, J.D. et al. 2006. Characterization of polymorphic microsatellite loci in the terrestrial isopod Armadillidium vulgare. Mol. Ecol. Notes 6: 328-330.
70. Verne, S., Johnson, M., Bouchon, D. & Grandjean, F. 2007. Evidence for recombination between feminizing Wolbachia in the isopod genus Armadillidium. Gene 397: 58-66.
71. Weir, B.S. & Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
72. Werren, J.H. & Windsor, D.M. 2000. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc. R. Soc. Lond. B Biol. Sci. 267: 1277-1285.
73. Wright, S. 1943. Isolation by distance. Genetics 28: 114-138.