EVOLUTIONARY DIVERSIFICATION THROUGH HYBRIDIZATION IN A WILD HOST–PATHOGEN INTERACTION

Abstract Coevolutionary outcomes between interacting species are predicted to vary across landscapes, as environmental conditions, gene flow, and the strength of selection vary among populations. Using a combination of molecular, experimental, and field approaches, we describe how broad-scale patterns of environmental heterogeneity, genetic divergence, and regional adaptation have the potential to influence coevolutionary processes in the Linum marginale–Melampsora lini plant–pathogen interaction. We show that two genetically and geographically divergent pathogen lineages dominate interactions with the host across Australia, and demonstrate a hybrid origin for one of the lineages. We further demonstrate that the geographic divergence of the two lineages of M. lini in Australia is related to variation among lineages in virulence, life-history characteristics, and response to environmental conditions. When correlated with data describing regional patterns of variation in host resistance diversity and mating system these observations highlight the potential for gene flow and geographic selection mosaics to generate and maintain coevolutionary diversification in long-standing host–pathogen interactions.

[1]  C. Brubaker,et al.  Frequency and fidelity of alien chromosome transmission in Gossypium hexaploid bridging populations. , 2007, Genome.

[2]  Michael E Hochberg,et al.  Coevolution of symbiotic mutualists and parasites in a community context. , 2007, Trends in ecology & evolution.

[3]  S. Laffan,et al.  Multi‐extent analysis of the relationship between pteridophyte species richness and climate , 2006 .

[4]  C. Brubaker,et al.  Isolation and characterization of microsatellite loci from the rust pathogen, Melampsora lini , 2006 .

[5]  B. Kobe,et al.  Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Anna‐Liisa Laine Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales , 2006, Proceedings of the Royal Society B: Biological Sciences.

[7]  B. Howlett,et al.  Major Gene Resistance to Blackleg in Brassica napus Overcome Within Three Years of Commercial Production in Southeastern Australia. , 2006, Plant disease.

[8]  P. Dodds,et al.  Haustorially Expressed Secreted Proteins from Flax Rust Are Highly Enriched for Avirulence Elicitors[W] , 2005, The Plant Cell Online.

[9]  J. Enjalbert,et al.  Genetic evidence of local adaptation of wheat yellow rust (Puccinia striiformis f. sp. tritici) within France , 2005, Molecular ecology.

[10]  J. Bever,et al.  Arbuscular mycorrhizal fungi: Hyphal fusion and multigenomic structure , 2005, Nature.

[11]  D. Nelson,et al.  Genetic Variation in Ustilago bullata: Molecular Genetic Markers and Virulence on Bromus tectorum Host Lines , 2005, International Journal of Plant Sciences.

[12]  Anna‐Liisa Laine Resistance variation within and among host populations in a plant–pathogen metapopulation: implications for regional pathogen dynamics , 2004 .

[13]  S. Otto,et al.  Host-parasite interactions and the evolution of ploidy. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[14]  A. Lebeda,et al.  Variation and distribution of virulence phenotypes of Bremia lactucae in natural populations of Lactuca serriola , 2004 .

[15]  P. Dodds,et al.  The Melampsora lini AvrL567 Avirulence Genes Are Expressed in Haustoria and Their Products Are Recognized inside Plant Cells , 2004, The Plant Cell Online.

[16]  M. Milgroom,et al.  Stepwise Evolution of Races in Fusarium oxysporum f. sp. ciceris Inferred from Fingerprinting with Repetitive DNA Sequences. , 2004, Phytopathology.

[17]  T. Pawlowska,et al.  Organization of genetic variation in individuals of arbuscular mycorrhizal fungi , 2004, Nature.

[18]  A. D. Peters,et al.  Liberating genetic variance through sex. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[19]  M. Berenbaum,et al.  PHENOTYPE MATCHING IN WILD PARSNIP AND PARSNIP WEBWORMS: CAUSES AND CONSEQUENCES , 2003, Evolution; international journal of organic evolution.

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

[21]  N. Gudmestad,et al.  Variability in Virulence Among Asexual Progenies of Phytophthora infestans. , 2003, Phytopathology.

[22]  E D Brodie,et al.  THE EVOLUTIONARY RESPONSE OF PREDATORS TO DANGEROUS PREY: HOTSPOTS AND COLDSPOTS IN THE GEOGRAPHIC MOSAIC OF COEVOLUTION BETWEEN GARTER SNAKES AND NEWTS , 2002, Evolution; international journal of organic evolution.

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

[24]  J. Burdon,et al.  Coevolutionary patterns in the Linum marginale: Melampsora lini association at a continental scale , 2002 .

[25]  S. Somerville,et al.  Quantitative trait loci analysis of powdery mildew disease resistance in the Arabidopsis thaliana accession kashmir-1. , 2001, Genetics.

[26]  M. Dickinson,et al.  Support for a stepwise mutation model for pathogen evolution in Australasian Puccinia striiformis f.sp. tritici by use of molecular markers , 2001 .

[27]  C. Brasier Rapid Evolution of Introduced Plant Pathogens via Interspecific Hybridization , 2001 .

[28]  C. Brasier Plant pathology: The rise of the hybrid fungi , 2000, Nature.

[29]  G. Newcombe,et al.  Melampsora ‹columbiana, a natural hybrid of M. medusae and M. occidentalis , 2000 .

[30]  J. N. Thompson,et al.  The evolution of species interactions. , 1999, Science.

[31]  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.

[32]  J. Duncan,et al.  Origin of a new Phytophthora pathogen through interspecific hybridization. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Thompson,et al.  Specific Hypotheses on the Geographic Mosaic of Coevolution , 1999, The American Naturalist.

[34]  C. Benkman The Selection Mosaic and Diversifying Coevolution between Crossbills and Lodgepole Pine , 1999, The American Naturalist.

[35]  C. Lively,et al.  HOST‐PARASITE COEVOLUTION: EVIDENCE FOR RARE ADVANTAGE AND TIME‐LAGGED SELECTION IN A NATURAL POPULATION , 1998, Evolution; international journal of organic evolution.

[36]  J. Burdon,et al.  Sources and patterns of diversity in plant-pathogenic fungi. , 1997, Phytopathology.

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

[38]  J. Burdon,et al.  Changed patterns of resistance in a population of Linum marginale attacked by the rust pathogen Melampsora lini. , 1995 .

[39]  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.

[40]  S. Frank,et al.  EVOLUTION OF HOST‐PARASITE DIVERSITY , 1993, Evolution; international journal of organic evolution.

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

[42]  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.

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

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

[45]  J. Burdon,et al.  Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini , 2004, Oecologia.

[46]  B. McDonald,et al.  Pathogen population genetics, evolutionary potential, and durable resistance. , 2002, Annual review of phytopathology.

[47]  C. Lively,et al.  Temporal and spatial distributions of parasites and sex in a freshwater snail , 2002 .

[48]  E. Humphreysa,et al.  Support for a stepwise mutation model for pathogen evolution in Australasian Puccinia striiformis f.sp. tritici by use of molecular markers , 2001 .

[49]  F. Rohlf,et al.  NTSYS-pc Numerical Taxonomy and Multivariate Analysis System, version 2.1: Owner manual , 1992 .

[50]  H. Geiger,et al.  Genetics of quantitative resistance to fungal diseases , 1989 .

[51]  H. H. Flor The Complementary Genic Systems in Flax and Flax Rust , 1956 .

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