Natural selection: how to get from population genetics to population biology

J.K.M. Brown, L.S. Arraiano, J.C. Makepeace, R.A. Wyand and H.N. Slatter
Department of Disease and Stress Biology, John Innes Centre, Colney, NORWICH, NR4 7UH, England

Over the last two decades, the use of molecular markers has become central to research on the population genetics of plant pathogens. In appropriately designed surveys and experiments, DNA markers provide valuable information about the structure of pathogen populations, particularly rates and directions of migration but also recombination, genetic drift and mutation. However, while these processes alter the structure of a pathogen population and reassort genes between places (migration) or between genomes (recombination), they do not change frequencies of genes or genotypes in the population as a whole. They are therefore merely the background to the principal driving force of evolution, natural selection.
Yet while studies of DNA marker variation have flourished, research on natural selection in pathogen populations has been comparatively neglected. This has limited our understanding of populations of plant pathogens because, to estimate the rate of evolution of a trait, it is necessary to understand its costs as well as its benefits. Although it is obvious that the use of a resistant crop variety will select for the corresponding pathogen virulence, or that the use of a pesticide will select for resistance to that chemical, an understanding of the dynamics of these pathogen traits, especially their long-term persistence, requires knowledge of their costs. Equally, while plant disease resistance is obviously desirable in order to control disease, its value for plant breeders and farmers may be limited if it is costly.
We will present recent research in our lab in which we have investigated costs of pathogen traits (virulence and fungicide resistance) and of plant disease resistance. Examples will be drawn from fungal diseases of cereals: yellow rust (Puccinia striiformis), powdery mildew (Blumeria graminis) and septoria tritici blotch (Mycosphaerella graminicola). Three general themes emerge from this research: a full understanding of pathogen population biology requires knowledge of processes that determine pathogen population structure to be integrated with knowledge of natural selection; knowledge about natural selection of host and pathogen traits can be applied to improve methods of crop protection; and rates and the direction of natural selection are strongly dependent on the environment. We suggest that the last point is one reason why recent research on pathogen population biology has largely neglected natural selection, because it is often difficult to design laboratory experiments that produce results which have a simple interpretation in field conditions.

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