Long-distance gene flow outweighs a century of local selection and prevents local adaptation in the Irish famine pathogen Phytophthora infestans

Evolutionary Applications

Volumn 7, Issue 4, 2014, Pages 442-452

  Glais, Isabelle ^a   Montarry, Josselin ^a   Corbière, Roselyne ^a   Pasco, Claudine ^a   Marquer, Bruno ^a   Magalon, Hélène ^a,b   Andrivon, Didier ^a  

^a Universite Rennes 1   (France)

^b UNIVERSITÉ DE LA RÉUNION   (France)

Author keywords

Clonal lineage; Evolution; Gene flow; Host resistance; Local adaptation; Microsatellites; Potato late blight; Selection

Indexed keywords

EID: 84940258752     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12142     Document Type: Article

References (52)

1. Andrivon, D. 1994. Race structure and dynamics in populations of Phytophthora infestans. Canadian Journal of Botany 72:1681-1687.
2. Andrivon, D. 2012. Dynamics of change in human-driven and natural systems: fast forward, slow motion, same movie? A case study from plant protection. Sustainability 4:384-393.
3. Andrivon, D., and E. Limpert 1992. Origin and proportions of the components of composite populations of Erysiphe graminis f. sp. hordei. Journal of Phytopathology 135:6-19.
4. Andrivon, D., J. M. Lucas, and D. Ellissèche 2003. Development of natural late blight epidemics in pure and mixed plots of potato cultivars with different levels of partial resistance. Plant Pathology 52:586-594.
5. Andrivon, D., F. Pilet, J. Montarry, M. Hafidi, R. Corbière, E. H. Achbani, R. Pellé etal. 2007. Adaptation of Phytophthora infestans to partial resistance in potato: evidence from French and Moroccan populations. Phytopathology 97:338-343.
6. Arnaud-Haond, S., and K. Belkhir 2007. GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Molecular Ecology Notes 7:15-17.
7. Bahri, B., O. Kaltz, M. Leconte, C. de Vallavieille-Pope, and J. Enjalbert 2009. Tracking costs of virulence in natural populations of the wheat pathogen, Puccinia striiformis f. sp. tritici. BMC Evolutionary Biology 9:26.
8. Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste, and F. Bonhomme 1996-2004. GENETIX 4.05, Logiciel Sous Windows TM Pour La Génétique Des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR5171, Université de Montpellier II, Montpellier (France).
9. Blanquart, F., S. Gandon, and S. L. Nuismer 2012. The effect of migration and drift on local adaptation to a heterogeneous environment. Journal of Evolutionary Biology 25:1351-1363.
10. Bouws, H., and M. R. Finckh 2008. Effects of strip intercropping of potatoes with non-hosts on late blight severity and tuber yield in organic production. Plant Pathology 57:916-927.
11. Brown, J. K. M., and A. Tellier 2011. Plant-parasite coevolution: bridging the gap between genetics and ecology. Annual Review of Phytopathology 49:345-367.
12. Clément, J. A. J., H. Magalon, R. Pellé, B. Marquer, and D. Andrivon 2010. Alteration of pathogenicity-linked life-history traits by resistance of its host Solanum tuberosum impacts sexual reproduction of the plant pathogenic oomycete Phytophthora infestans. Journal of Evolutionary Biology 23:2668-2676.
13. Cooke, D. E. L., L. M. Cano, S. Raffaele, R. A. Bain, L. R. Cooke, G. J. Etherington, K. L. Deahl etal. 2012. Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathogens 8:e1002940.
14. Deahl, K. L., F. M. Perez, J. M. Thompson, C. Fleming-Archibald, S. Thompson, R. Collier, S. Kildea etal. 2009. Characterization of Phytophthora infestans isolates from Jersey, Channel Islands. Potato Research 52:341-354.
15. Drenth, A., I. C. Q. Tas, and F. Govers 1994. DNA fingerprinting uncovers a new sexually reproducing population of Phytophthora infestans in the Netherlands. European Journal of Plant Pathology 100:97-107.
16. Evanno, G., S. Regnaut, and J Goudet 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14:2611-2620.
17. Excoffier, L., and P. E. Smouse 1994. Using allele frequencies and geographic subdivision to reconstruct gene trees within a species - molecular variance parsimony. Genetics 136:343-359.
18. Falush, D., M. Stephens, and J. K. Pritchard 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567-1587.
19. Gandon, S., and T. Day 2009. Evolutionary epidemiology and the dynamics of adaptation. Evolution 63:826-838.
20. Garrett, K. A., and C. C. Mundt 2000. Host diversity can reduce potato late blight severity for focal and general patterns of primary inoculum. Phytopathology 90:1307-1312.
21. Goyeau, H., F. Halkett, M. F. Zapater, J. Carlier, and C. Lannou 2007. Clonality and host selection in the wheat pathogenic fungus Puccinia triticina. Fungal Genetics and Biology 44:474-483.
22. Halkett, F., J. C. Simon, and F. Balloux 2005. Tackling the population genetics of clonal and partially clonal organisms. Trends in Ecology and Evolution 20:194-201.
23. Haverkort, A. J., P. M. Boonekamp, R. Hutten, E. Jacobsen, L. A. P. Lotz, G. J. T. Kessel, R. G. F. Visser etal. 2008. Societal costs of late blight in potato and prospects of durable resistance through cisgenic modification. Potato Research 51:47-57.
24. Kawecki, T. J., and D. Ebert 2004. Conceptual issues in local adaptation. Ecology Letters 7:1225-1241.
25. Kiyosawa, S., D. Purba, M. S. Ali, Y. Okinaka, T. Shimizu, and A. Saito 1995. Influence of frequencies of host genotypes and fitness of virulence genes on nonrandom association type and pattern between avirulence loci. Breeding Science 45:287-293.
26. Knapova, G., and U. Gisi 2002. Phenotypic and genotypic structure of Phytophthora infestans populations on potato and tomato in France and Switzerland. Plant Pathology 51:641-653.
27. Langella, O. 1999. Populations 1.2.32, Population Genetic Software. Laboratoire Evolution, Génomes et Spéciation, CNRS UPR9034, Gif-sur-Yvette (France).
28. Lannou, C. 2012. Variation and selection of quantitative traits in plant pathogens. Annual Review of Phytopathology 50:319-338.
29. Leach, J. E., C. M. Vera-Cruz, J. F. Bai, and H. Leung 2001. Pathogen fitness penalty as a predictor of durability of disease resistance genes. Annual Review of Phytopathology 39:187-224.
30. Lees, A. K., R. Wattier, D. S. Shaw, L. Sullivan, N. A. Williams, and D. E. L. Cooke 2006. Novel microsatellite markers for the analysis of Phytophthora infestans populations. Plant Pathology 55:311-319.
31. Leonard, K. J. 1994. Stability of equilibria in a gene-for-gene coevolution model of host-parasite interactions. Phytopathology 84:70-77.
32. Montarry, J., I. Glais, R. Corbière, and D. Andrivon 2008. Adaptation to the most abundant host genotype in an agricultural plant-pathogen system - potato late blight. Journal of Evolutionary Biology 21:1397-1407.
33. Montarry, J., F. M. Hamelin, I. Glais, R. Corbière, and D. Andrivon 2010a. Fitness costs associated with unnecessary virulence factors and life history traits: evolutionary insights from the potato late blight pathogen Phytophthora infestans. BMC Evolutionary Biology 10:283.
34. Montarry, J., D. Andrivon, I. Glais, R. Corbière, G. Mialdea, and F. Delmotte 2010b. Microsatellite markers reveal two admixed genetic groups and an ongoing displacement within the French population of the invasive plant pathogen Phytophthora infestans. Molecular Ecology 19:1965-1977.
35. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583-590.
36. Nesse, R. M. 2011. Ten questions for evolutionary studies of disease vulnerability. Evolutionary Applications 4:264-277.
37. Nesse, R. M., C. T. Bergstrom, P. T. Ellison, J. S. Flier, P. Gluckman, D. R. Govindaraju, D. Niethammer etal. 2010. Making evolutionary biology a basic science for medicine. Proceedings of the National Academy of Sciences of the United States of America 107(Suppl 1):1800-1807.
38. Pariaud, B., V. Ravigné, F. Halkett, J. Carlier, and C. Lannou 2009. Aggressiveness and its role in the adaptation of plant pathogens. Plant Pathology 58:409-424.
39. Philips, S. L., M. W. Shaw, and M. S. Wolfe 2005. The effect of potato variety mixtures on epidemics of late blight in relation to plot size and level of resistance. The Annals of Applied Biology 147:245-252.
40. Pilet, F., M. Chacón, G. A. Forbes, and D. Andrivon 2006. Protection of susceptible potato cultivars against late blight in mixtures increases with decreasing inoculum pressure. Phytopathology 96:777-783.
41. Pritchard, J. K., M. Stephens, and P. Donnelly 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
42. R Foundation for Statistical Computing 2012. R version 2.15.0 (2012-03-30) Copyright (C).
43. Raymond, M., and F. Rousset 1995. Genepop Version1.2: population genetics software for exact tests and ecumenicism. Journal of Heredity 86:248-249.
44. Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219-1228.
45. Skelsey, P., W. A. H. Rossing, G. J. T. Kessel, and W. van der Werf 2010. Invasion of Phytophthora infestans at the landscape level: how do spatial scale and weather modulate the consequences of spatial heterogeneity in host resistance? Phytopathology 100:1146-1161.
46. Slatkin, M. 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457-462.
47. Spielman, L. J., A. Drenth, L. C. Davidse, L. J. Sujkowski, W. Gu, P. W. Pooley, and W. E. Fry 1991. A second worldwide migration and population displacement of Phytophthora infestans? Plant Pathology 40:422-430.
48. Tellier, A., and J. K. M. Brown 2011. Spatial heterogeneity, frequency-dependent selection and polymorphism in host-parasite interactions. BMC Evolutionary Biology 11:319.
49. Thrall, P. H., J. J. Burdon, and J. D. Bever 2002. Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution 56:1340-1351.
50. Weir, B. S., and C. C. Cockerham 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358-1370.
51. Whitlock, M. C. 2008. Evolutionary inference from QST. Molecular Ecology 17:1885-1896.
52. Whitlock, M. C., and K. J. Gilbert 2012. QST in a hierarchically structured population. Molecular Ecology Resources 12:481-483.