PARTIAL RESISTANCE IN THE LINUM‐MELAMPSORA HOST–PATHOGEN SYSTEM: DOES PARTIAL RESISTANCE MAKE THE RED QUEEN RUN SLOWER?

Five levels of disease expression were scored in a cross‐inoculation study of 120 host and 60 pathogen lines of wild flax Linum marginale and its rust fungus Melampsora lini sampled from six natural populations. Patterns of partial resistance showed clear evidence of gene‐for‐gene interactions, with particular levels of partial resistance occurring in specific host–pathogen combinations. Sympatric and putatively more highly coevolved host–pathogen combinations had a lower frequency of partial resistance types relative to allopatric combinations. Sympatric host–pathogen combinations also showed a lower diversity of resistance responses, but there was a trend toward a greater fraction of this variance being determined by pathogen‐genotype × host‐genotype interactions. In this system, there was no evidence that partial resistances slow host–pathogen coevolution. The analyses show that if variation is generated by among population host or pathogen dispersal, then coevolution occurs largely by pathogens overcoming the partial resistances that are generated.

[1]  E Kisdi,et al.  The Evolution of Host‐Parasite Range , 2010, The American Naturalist.

[2]  C. Lively.  A review of Red Queen models for the persistence of obligate sexual reproduction. , 2010, The Journal of heredity.

[3]  Mike Boots,et al.  The Implications of Coevolutionary Dynamics to Host‐Parasite Interactions , 2009, The American Naturalist.

[4]  E. Decaestecker,et al.  Host–parasite ‘Red Queen’ dynamics archived in pond sediment , 2007, Nature.

[5]  F. Jiggins,et al.  The age and evolution of an antiviral resistance mutation in Drosophila melanogaster , 2007, Proceedings of the Royal Society B: Biological Sciences.

[6]  D. Danial,et al.  Variation in virulence and resistance in the bean-bean rust pathosystem in Ecuador , 2007, Euphytica.

[7]  T. Loughin.  SAS® for Mixed Models, 2nd edition Edited by Littell, R. C., Milliken, G. A., Stroup, W. W., Wolfinger, R. D., and Schabenberger, O. , 2006 .

[8]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[9]  B. Bohannan,et al.  Adaptation varies through space and time in a coevolving host–parasitoid interaction , 2004, Nature.

[10]  J. Burdon,et al.  Evolution of Virulence in a Plant Host-Pathogen Metapopulation , 2003, Science.

[11]  J. Bever,et al.  LOCAL ADAPTATION IN THE LINUM MARGINALE—MELAMPSORA LINI HOST‐PATHOGEN INTERACTION , 2002, Evolution; international journal of organic evolution.

[12]  Paul B Rainey,et al.  Antagonistic coevolution between a bacterium and a bacteriophage , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[13]  D. Ebert,et al.  GENETIC VARIATION IN A HOST‐PARASITE ASSOCIATION: POTENTIAL FOR COEVOLUTION AND FREQUENCY‐DEPENDENT SELECTION , 2001, Evolution; international journal of organic evolution.

[14]  A. Sasaki.  Host-parasite coevolution in a multilocus gene-for-gene system , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  C. Lively,et al.  Parasite adaptation to locally common host genotypes , 2000, Nature.

[16]  J. Burdon,et al.  RESISTANCE AND VIRULENCE STRUCTURE IN TWO LINUM MARGINALE‐MELAMPSORA LINI HOST‐PATHOGEN METAPOPULATIONS WITH DIFFERENT MATING SYSTEMS , 1999, Evolution; international journal of organic evolution.

[17]  M. Sorrells,et al.  Mapping genes conferring and suppressing leaf rust resistance in wheat , 1997 .

[18]  G. Ash.  Wheat Rusts: An Atlas of Resistance Genes. , 1996, Australasian Plant Pathology.

[19]  Gary G. Koch,et al.  Categorical Data Analysis Using The SAS1 System , 1995 .

[20]  J. Burdon,et al.  The population genetic structure of the rust fungus Melampsora lini as revealed by pathogenicity, isozyme and RFLP markers , 1995 .

[21]  J. Burdon,et al.  THE DISTRIBUTION AND ORIGIN OF GENES FOR RACE‐SPECIFIC RESISTANCE TO MELAMPSORA LINI IN LINUM MARGINALE , 1994, Evolution; international journal of organic evolution.

[22]  T. Hsiang,et al.  Variation in Melampsora occidentalis rust on poplars in the Pacific Northwest , 1993 .

[23]  I. Crute,et al.  Diversity and variation in expression of resistance to Erysiphe fischeri in Senecio vulgaris , 1993 .

[24]  H. M. Alexander,et al.  Genotypic variation in plant disease resistance―physiological resistance in relation to field disease transmission , 1993 .

[25]  Jeremy J. Burdon,et al.  Gene-for-gene coevolution between plants and parasites , 1992, Nature.

[26]  Ali S. Hadi,et al.  Finding Groups in Data: An Introduction to Chster Analysis , 1991 .

[27]  J. Burdon,et al.  HOST‐PATHOGEN INTERACTIONS IN NATURAL POPULATIONS OF LINUM MARGINALE AND MELAMPSORA LINI: I. PATTERNS OF RESISTANCE AND RACIAL VARIATION IN A LARGE HOST POPULATION , 1991, Evolution; international journal of organic evolution.

[28]  J. Burdon,et al.  Flax rust from Linum marginale: variation in a natural host−pathogen interaction , 1989 .

[29]  J. Seger.  Dynamics of some simple host-parasite models with more than two genotypes in each species. , 1988, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[30]  J. Burdon.  Phenotypic and genetic patterns of resistance to the pathogen Phakopsora pachyrhizi in populations of Glycine canescens , 1987, Oecologia.

[31]  B. Weir,et al.  Multiline varieties and disease control , 1985, Theoretical and Applied Genetics.

[32]  R M May,et al.  Epidemiology and genetics in the coevolution of parasites and hosts , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[33]  G. Bell,et al.  A Big Book on Sex@@@The Masterpiece of Nature: The Evolution and Genetics of Sexuality. , 1983 .

[34]  W. Hamilton.  Sex versus non-sex versus parasite , 1980 .

[35]  K. Leonard,et al.  SELECTION PRESSURES AND PLANT PATHOGENS , 1977 .

[36]  J. Hatchett,et al.  Genetics of the Ability of the Hessian Fly, Mayetiola destructor, to Survive on Wheats Having Different Genes for Resistance , 1970 .

[37]  E. Varney.  Plant diseases: Epidemics and control , 1964, American Potato Journal.

[38]  Å. Granberg.  Microbotryum violaceum on Silene dioica : understanding traits that influence plant-pathogen interactions , 2007 .

[39]  Mark J. van der Laan,et al.  Cluster Analysis of Genomic Data with Applications in R , 2005 .

[40]  Curtis M. Lively,et al.  Infection genetics: gene-for-gene versus matching-alleles models and all points in between , 2002 .

[41]  B. Weir,et al.  5. The "dirty crop" approach with complex mixtures of genotypes based on overlapping gene sets * , 1985 .

[42]  L. V. Valen,et al.  A new evolutionary law , 1973 .

[43]  Hh Flor,et al.  Host-parasite interaction in flax rust–its genetics and other implications , 1955 .