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Linkage Disequilibrium and Spatial Aggregation of Genotypes in Sexually Reproducing Populations of Erysiphe necator

Random mating and recombination in heterothallic ascomycetes should result in high genotypic diversity, 1:1 mating-type ratios, and random associations of alleles, or linkage equilibrium, at different loci. To test for random mating in populations of the grape powdery mildew fungus Erysiphe necator, we sampled isolates from vineyards of Vitis vinifera in Burdett, NY (NY09) and Winchester, VA (VA09) at the end of the epidemic in fall 2009. We also sampled isolates from the same Winchester, VA vineyard in spring 2010 at the onset of the next epidemic. Isolates were genotyped for mating type and 11 microsatellite markers. In the spring sample, which originated from ascospore infections, nearly every isolate had a unique genotype. In contrast, fall populations were less diverse. In all, 9 of 45 total genotypes in VA09 were represented by two or more isolates; 3 of 40 total genotypes in NY09 were represented by two or more isolates, with 1 genotype represented by 20 isolates. After clone correction, mating-type ratios in the three populations did not deviate from 1:1. However, even with clone correction, we detected significant linkage disequilibrium (LD) in all populations. Mantel tests detected positive correlations between genetic and physical distances within vineyards. Spatial autocorrelation showed aggregations up to 42 and 3 m in VA09 and NY09, respectively. Spatial autocorrelation most likely results from short dispersal distances. Overall, these results suggest that spatial genetic aggregation and clonal genotypes that arise during the asexual phase of the epidemic contribute to persistent LD even though populations undergo sexual reproduction annually.