Population processes at multiple spatial scales maintain diversity and adaptation in the linum marginale - Melampsora lini association

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Nemri, Adnane ^a   Barrett, Luke G ^a   Laine, Anna Liisa ^a,b   Burdon, Jeremy J ^a   Thrall, Peter H ^a  

^a CSIRO   (Australia)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ASEXUAL REPRODUCTION; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; FUNGAL VIRULENCE; FUNGUS; GENETIC VARIABILITY; HOST PATHOGEN INTERACTION; INFECTION RESISTANCE; LIFE HISTORY; LINUM; LINUM MARGINALE; MATING; MELAMPSORA LINI; NONHUMAN; PHENOTYPE; PLANT FUNGUS INTERACTION; REPRODUCTION;

ADAPTATION, BIOLOGICAL; ANALYSIS OF VARIANCE; AUSTRALIA; BASIDIOMYCOTA; DISEASE RESISTANCE; ECOSYSTEM; EVOLUTION, MOLECULAR; FLAX; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; MODELS, GENETIC; PHENOTYPE; PHYLOGENY; PHYLOGEOGRAPHY; PLANT DISEASES; SYMPATRY;

LINUM MARGINALE; LINUM USITATISSIMUM; MELAMPSORA LINI; UREDINALES;

EID: 84864441926     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041366     Document Type: Article

References (75)

1. Thrall PH, Burdon JJ, Young A, ((2001)) Variation in resistance and virulence among demes of a plant host-pathogen metapopulation. Journal of Ecology 89: 736-748.
2. Burdon JJ, Jarosz AM, Kirby GC, ((1989)) Pattern and patchiness in plant-pathogen interactions- causes and consequences. Annual Review of Ecology and Systematics 20: 119-136.
3. Laine A-L, ((2009)) Role of coevolution in generating biological diversity: spatially divergent selection trajectories. Journal of Experimental Botany 60: 2957-2970.
4. Salvaudon L, Giraud T, Shykoff JA, ((2008)) Genetic diversity in natural populations: a fundamental component of plant-microbe interactions. Current Opinion in Plant Biology 11: 135-143.
5. Laine A-L, Burdon JJ, Dodds PN, Thrall PH, ((2011)) Spatial variation in disease resistance: from molecules to metapopulations. Journal of Ecology 99: 96-112.
6. Thompson JN (2005) The geographic mosaic of coevolution. Chicago: University of Chicago Press. 370 p.
7. Laine A-L, Tellier A, ((2008)) Heterogeneous selection promotes maintenance of polymorphism in host-parasite interactions. Oikos 117: 1281-1288.
8. Wolinska J, King KC, ((2009)) Environment can alter selection in host-parasite interactions. Trends in Parasitology 25: 236-244.
9. Barrett LG, Thrall PH, Burdon JJ, Linde CC, ((2008)) Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends in Ecology & Evolution 23: 678-685.
10. Lively CM, ((2010)) The effect of host genetic diversity on disease spread. American Naturalist 175: E149-E152.
11. Lively CM, Craddock C, Vrijenhoek RC, ((1990)) Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature 344: 864-866.
12. Schmid-Hempel P, Crozier RH, ((1999)) Ployandry versus polygyny versus parasites. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 354: 507-515.
13. Whiteman NK, Matson KD, Bollmer JL, Parker PG, ((2006)) Disease ecology in the Galapagos Hawk (Buteo galapagoensis): host genetic diversity, parasite load and natural antibodies. Proceedings of the Royal Society B: Biological Sciences 273: 797-804.
14. Altermatt F, Ebert D, ((2008)) Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecology Letters 11: 918-928.
15. Whitehorn PR, Tinsley MC, Brown MJF, Darvill B, Goulson D, ((2011)) Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proceedings of the Royal Society B: Biological Sciences 278: 1195-1202.
16. Chin KM, Wolfe MS, ((1984)) The spread of Erisyphe graminis f. sp. hordei in mixtures of barley varieties. Plant Pathology 33: 89-100.
17. Mundt CC, ((2002)) Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology 40: 381-410.
18. Mundt C, Brunet J, Sackett K, ((2008)) Impact of density and disease on frequency-dependent selection and genetic polymorphism: experiments with stripe rust and wheat. Evolutionary Ecology 22: 637-657.
19. Ganz HH, Ebert D, ((2010)) Benefits of host genetic diversity for resistance to infection depend on parasite diversity. Ecology 91: 1263-1268.
20. Thrall PH, Burdon JJ, ((2000)) Effect of resistance variation in a natural plant host-pathogen metapopulation on disease dynamics. Plant Pathology 49: 767-773.
21. Laine A-L, ((2006)) Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proceedings of the Royal Society B: Biological Sciences 273: 267-273.
22. King KC, Delph LF, Jokela J, Lively CM, ((2009)) The geographic mosaic of sex and the Red Queen. Current Biology 19: 1438-1441.
23. Berenos C, Wegner KM, Schmid-Hempel P, ((2011)) Antagonistic coevolution with parasites maintains host genetic diversity: an experimental test. Proceedings of the Royal Society B: Biological Sciences 278: 218-224.
24. Doligez A, Baril C, Joly HI, ((1998)) Fine-scale spatial genetic structure with nonuniform distribution of individuals. Genetics 148: 905-920.
25. Vekemans X, Hardy OJ, ((2004)) New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology 13: 921-935.
26. Howard RS, Lively CM, ((2002)) The Ratchet and the Red Queen: the maintenance of sex in parasites. Journal of Evolutionary Biology 15: 648-656.
27. Galvani AP, Coleman RM, Ferguson NM, ((2003)) The maintenance of sex in parasites. Proceedings of the Royal Society of London Series B: Biological Sciences 270: 19-28.
28. Roelfs AP, Groth JV, ((1980)) A comparison of virulence phenotypes in wheat-stem rust populations reproducing sexually and asexually. Phytopathology 70: 855-862.
29. Groth JV, McCain JW, Roelfs AP, ((1995)) Virulence and isozyme diversity of sexual versus asexual collections of Uromyces appendiculatus (bean rust fungus). Heredity 75: 234-242.
30. Gandon S, Nuismer SL, ((2009)) Interactions between genetic drift, gene flow, and selection mosaics drive parasite local adaptation. American Naturalist 173: 212-224.
31. Garant D, Forde SE, Hendry AP, ((2007)) The multifarious effects of dispersal and gene flow on contemporary adaptation. Functional Ecology 21: 434-443.
32. Parker MA, ((1991)) Nonadaptive evolution and disease resistance in an annual legume. Evolution 45: 1209-1217.
33. Lande R, Arnold SJ, ((1983)) The measurement of selection on correlated characters. Evolution 37: 1210-1226.
34. Thrall PH, Burdon JJ, ((1999)) The spatial scale of pathogen dispersal: Consequences for disease dynamics and persistence. Evolutionary Ecology Research 1: 681-701.
35. Lively CM, Delph LF, Dybdahl MF, Jokela J, ((2008)) Experimental test for a co-evolutionary hotspot in a host-parasite interaction. Evolutionary Ecology Research 10: 95-103.
36. Burdon JJ, Thrall PH, Brown AHD, ((1999)) Resistance and virulence structure in two Linum marginale-Melampsora lini host-pathogen metapopulations with different mating systems. Evolution 53: 704-716.
37. Barrett LG, Thrall PH, Burdon JJ, Nicotra AB, Linde CC, ((2008)) Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini. Molecular Ecology 17: 3401-3415.
38. Burdon JJ, Roberts JK, ((1995)) The population genetic structure of the rust fungus Melampsora lini as revealed by pathogenicity, isozyme and RFLP markers. Plant Pathology 44: 270-278.
39. Barrett LG, Thrall PH, Burdon JJ, ((2007)) Evolutionary diversification through hybridization in a wild host-pathogen interaction. Evolution 61: 1613-1621.
40. Lawrence GJ, Burdon JJ, ((1989)) Flax rust from Linum marginale- variation in a natural host pathogen interaction. Canadian Journal of Botany/Revue Canadienne de Botanique 67: 3192-3198.
41. Jarosz AM, Burdon JJ, ((1991)) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. II. Local and regional variation in patterns of resistance and racial structure. Evolution 45: 1618-1627.
42. Burdon JJ, Jarosz AM, ((1991)) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. I. patterns of resistance and racial variation in a large host population. Evolution 45: 205-217.
43. Burdon JJ, ((1994)) The distribution and origin of genes for race-specific resistance to Melampsora lini in Linum marginale. Evolution 48: 1564-1575.
44. Jarosz AM, Burdon JJ, ((1992)) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. III. Influence of pathogen epidemics on host survivorship and flower production. Oecologia 89: 53-61.
45. Ravensdale M, Nemri A, Thrall PH, Ellis JG, Dodds PN, ((2010)) Co-evolutionary interactions between host resistance and pathogen effector genes in flax rust disease. Molecular Plant Pathology 12: 93-102.
46. Antonovics J, Thrall PH, Burdon JJ, Laine A-L, ((2011)) Partial resistance in the Linum-Melampsora host-pathogen system: does partial resistance make the Red Queen run slower? Evolution 65: 512-522.
47. Cloutier S, Niu Z, Datla R, Duguid S, ((2009)) Development and analysis of EST-SSRs for flax (Linum usitatissimum L.). Theoretical and Applied Genetics 119: 53-63.
48. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes. pp. 288-295.
49. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS® for Mixed Models. Cary, USA.: SAS Institute Inc.
50. Lloyd M, ((1967)) Mean crowding. Journal of Animal Ecology 36: 1-30.
51. Degen B, Petit R, Kremer A, ((2001)) SGS- Spatial Genetic Software: a computer program for analysis of spatial genetic and phenotypic structures of individuals and populations. Journal of Heredity 92: 447-448.
52. Deichsel G, Trampisch H (1985) Clusteranalyse und Diskriminanzanalyse. Gustav Fischer Verlag. Stuttgart.
53. Thompson JN, Thompson JN (1994) The coevolutionary process. The coevolutionary process: xi+376p.
54. Lawrence GJ, Dodds PN, Ellis JG, ((2007)) Rust of flax and linseed caused by Melampsora lini. Molecular Plant Pathology 8: 349-364.
55. Kawecki TJ, Ebert D, ((2004)) Conceptual issues in local adaptation. Ecology Letters 7: 1225-1241.
56. Thrall PH, Burdon JJ, Bever JD, ((2002)) Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution 56: 1340-1351.
57. Flor HH, ((1942)) Inheritance of pathogenicity in Melampsora lini. Phytopathology 32: 653-669.
58. Clay K, Kover PX, ((1996)) The Red Queen hypothesis and plant/pathogen interactions. Annual Review of Phytopathology 34: 29-50.
59. Ooi K, Yahara T, ((1999)) Genetic variation of geminiviruses: comparison between sexual and asexual host plant populations. Molecular Ecology 8: 89-97.
60. Thrall PH, Laine A-L, Ravensdale M, Nemri A, Dodds PN, et al. ((2012)) Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecology Letters 15: 425-435.
61. Hoebe PN, Stift M, Holub EB, Mable BK, ((2011)) The effect of mating system on growth of Arabidopsis lyrata in response to inoculation with the biotrophic parasite Albugo candida. Journal of Evolutionary Biology 24: 391-401.
62. Koslow JM, DeAngelis DL, ((2006)) Host mating system and the prevalence of disease in a plant population. Proceedings of the Royal Society B: Biological Sciences 273: 1825-1831.
63. Jokela J, Dybdahl MF, Lively CM, ((2009)) The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. American Naturalist 174: S43-S53.
64. Neiman M, Koskella B (2009) Sex and the Red Queen. Lost Sex: Springer Netherlands. pp. 133-159.
65. Koskella B, Lively CM, ((2009)) Evidence for negative frequency-dependent selection during experimental coevolution of a freshwater snail and a sterilizing trematode. Evolution 63: 2213-2221.
66. Lively CM, ((2010)) A review of Red Queen models for the persistence of obligate sexual reproduction. Journal of Heredity 101: S13-20.
67. Dodds PN, Lawrence GJ, Ellis JG, ((2001)) Contrasting modes of evolution acting on the complex N locus for rust resistance in flax. Plant Journal 27: 439-453.
68. Ellis JG, Lawrence GJ, Dodds PN, ((2007)) Further analysis of gene-for-gene disease resistance specificity in flax. Molecular Plant Pathology 8: 103-109.
69. Lawrence GJ, Anderson PA, Dodds PN, Ellis JG, ((2010)) Relationships between rust resistance genes at the M locus in flax. Molecular Plant Pathology 11: 19-32.
70. Hamilton WD, ((1980)) Sex versus non-sex versus parasite. Oikos 35: 282-290.
71. Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. Berkeley, CA: University of California Press.
72. Lively CM, Howard RS, ((1994)) Selection by parasites for clonal diversity and mixed mating. Philosophical Transactions of the Royal Society B: Biological Sciences 346: 271-280.
73. Agrawal AF, Lively CM, ((2001)) Parasites and the evolution of self-fertilization. Evolution 55: 869-879.
74. Steets JA, Wolf DE, Auld JR, Ashman T-L, ((2007)) The role of natural enemies in the expression and evolution of mixed mating in hermaphroditic plants and animals. Evolution 61: 2043-2055.
75. Garcia-Guzman G, Morales E, ((2007)) Life-history strategies of plant pathogens: distribution patterns and phylogenetic analysis. Ecology 88: 589-596.