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International audience; Crop-to-wild gene flow have important evolutionary and ecological consequences and require careful consideration in conservation programs for wild genetic resources of potential use in breeding programs and in assessments of the risk of transgene escape into natural ecosystems. Using 26 microsatellites and a set of 1181 trees, we investigated the extent of introgression from the cultivated apple, Malus domestica, to its three closest wild relatives, M.sylvestris in Europe, M.orientalis in the Caucasus, and M.sieversii in Central Asia. We found footprints of introgression from M.domestica to M.orientalis (3.2% of hybrids), M.sieversii (14.8%), and M.sylvestris (36.7%). Malus sieversii and M.orientalis presented weak, but significant genetic structures across their geographic range. Malus orientalis displayed genetic differentiation with three differentiated populations in Turkey, Armenia, and Russia. Malus sieversii consisted of a main population spread over Central Asia and a smaller population in the Tian Shan Mountains. The low Sp values suggest high dispersal capacities for the wild apple relatives. High potential for crop-to-wild gene flow in apples needs to be considered in the implementation of in situ and ex situ actions for the conservation of wild apple genetic resources potentially useful to plant breeding.

Understanding how pathogens emerge is essential to bring disease-causing agents under durable human control. Here, we used cross-pathogenicity tests to investigate the changes in life-history traits of the fungal pathogen Venturia inaequalis associated with host-tracking during the domestication of apple and subsequent host-range expansion on the wild European crabapple (Malus sylvestris). Pathogenicity of 40 isolates collected in wild and domesticated ecosystems was assessed on the domesticated apple, its Central Asian main progenitor (M. sieversii) and M. sylvestris. Isolates from wild habitats in the centre of origin of the crop were not pathogenic on the domesticated apple and less aggressive than other isolates on their host of origin. Isolates from the agro-ecosystem in Central Asia infected a higher proportion of plants with higher aggressiveness, on both the domesticated host and its progenitor. Isolates from the European crabapple were still able to cause disease on other species but were less aggressive and less frequently virulent on these hosts than their endemic populations. Our results suggest that the domestication of apple was associated with the acquisition of virulence in the pathogen following host-tracking. The spread of the disease in the agro-ecosystem would also have been accompanied by an increase in overall pathogenicity.

Gene flow is an essential component of population adaptation and species evolution. Understanding of the natural and anthropogenic factors affecting gene flow is also critical for the development of appropriate management, breeding, and conservation programs. Here, we explored the natural and anthropogenic factors impacting crop-to-wild and within wild gene flow in apples in Europe using an unprecedented dense sampling of 1889 wild apple (Malus sylvestris) from European forests and 339 apple cultivars (Malus domestica). We made use of genetic, environmental, and ecological data (microsatellite markers, apple production across landscapes and records of apple flower visitors, respectively). We provide the first evidence that both human activities, through apple production, and human disturbance, through modifications of apple flower visitor diversity, have had a significant impact on crop-to-wild interspecific introgression rates. Our analysis also revealed the impact of previous natural climate change on historical gene flow in the nonintrogressed wild apple M. sylvestris, by identifying five distinct genetic groups in Europe and a north–south gradient of genetic diversity. These findings identify human activities and climate as key drivers of gene flow in a wild temperate fruit tree and provide a practical basis for conservation, agroforestry, and breeding programs for apples in Europe.