Abstract
Fitness cost associated with pathogens carrying unnecessary virulence alleles is the fundamental assumption for preventing the emergence of complex races in plant pathogen populations but this hypothesis has rarely been tested empirically on a temporal and spatial scale which is sufficient to distinguish evolutionary signals from experimental error. We analyzed virulence characteristics of ∼1000 isolates of the barley pathogen Rhynchosporium secalis collected from different parts of the United Kingdom between 1984 and 2005. We found a gradual increase in race complexity over time with a significant correlation between sampling date and race complexity of the pathogen (r20 = 0.71, p = 0.0002) and an average loss of 0.1 avirulence alleles (corresponding to an average gain of 0.1 virulence alleles) each year. We also found a positive and significant correlation between barley cultivar diversity and R. secalis virulence variation. The conditions assumed to favour complex races were not present in the United Kingdom and we hypothesize that the increase in race complexity is attributable to the combination of natural selection and genetic drift. Host resistance selects for corresponding virulence alleles to fixation or dominant frequency. Because of the weak fitness penalty of carrying the unnecessary virulence alleles, genetic drift associated with other evolutionary forces such as hitch-hiking maintains the frequency of the dominant virulence alleles even after the corresponding resistance factors cease to be used.
Highlights
The evolution of race complexity, here defined as the number of differential cultivars a pathogen isolate infects, has been one of main concerns of plant pathologists, plant breeders and farmers in devising strategies of resistance gene deployment
The emergence of complex races in pathogen populations is thought unlikely to occur unless selective regimes favouring the complex races are present recurrently and the benefits from this positive host selection are large enough to compensate for the cost of carrying unnecessary virulence alleles
The genetic basis of the resistance phenotype is not known and matching virulence in the pathogen is known as Barley Rhynchosporium Virulence (BRV) factors
Summary
The evolution of race complexity, here defined as the number of differential cultivars a pathogen isolate infects, has been one of main concerns of plant pathologists, plant breeders and farmers in devising strategies of resistance gene deployment. The emergence of complex races in pathogen populations is thought unlikely to occur unless selective regimes favouring the complex races are present recurrently and the benefits from this positive host selection are large enough to compensate for the cost of carrying unnecessary virulence alleles. Experimental test and verification of evolutionary theory including the evolution of race complexity through long-term observation of population dynamics under large farm field conditions is limited. Analysis of pathogen data from these surveys can provide plant breeders/pathologists with information and material for resistance screening, and can be very useful for studying the evolution of plant pathogens because many of these surveys cover large geographic areas and continue for several decades [4], [5], [6]
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