Ecological and evolutionary drivers of phenotypic and genetic variation in the European crabapple (Malus sylvestris (L.) Mill.), a wild relative of the cultivated apple

Abstract Characterizing the phenotypic and genetic variation among populations of crop wild relatives help understanding the ecological and evolutionary processes involved in population divergence, and better harness their diversity to mitigate the impact of climate change on crops. We assessed genetic and phenotypic diversity of the European crabapple, Malus sylvestris , a main contributor to the cultivated apple genome ( Malus domestica ), and investigated for ecological divergence. We assessed variation in growth rate and traits related to carbon uptake between seedlings measured in a common garden, and related it to the genetic ancestry of the seedlings, assessed using 13 microsatellite loci and Bayesian clustering method. The occurrence of patterns of isolation-by-distance, -by-climate and -by-adaptation that might have caused genetic and phenotypic differentiation among M. sylvestris populations was also tested. Seedlings belonged to seven M. sylvestris populations in Europe, with 11.6% of seedlings introgressed by M. domestica . Significant trait variation among M. sylvestris populations was observed, which for some was of moderate to high heritability. Lack of association between trait and genetic divergence suggests that this significant phenotypic variation is not adaptive, but strong association between genetic variation and the climate during the last glacial maximum suggests local adaptation of M. sylvestris to past climates. This study provides an insight into the ecological and evolutionary drivers of phenotypic and genetic differentiation among populations of a wild apple species and relative of cultivated apples, which is a starting point for future breeding programs. Societal impact Statement Apple is a major fruit crop worldwide and a model species for understanding the evolutionary processes underlying perennial crop domestication. Several wild species have contributed to the genetic make-up of the cultivated apple, yet phenotypic and genetic diversity data across their natural distribution is lacking. This study revealed phenotypic variation between populations of the European crabapple, and showed that both geography, and surprisingly, past but not current climate, shaped its genetic structure. We provide a starting point for harnessing wild apple diversity for apple breeding programs to mitigate the impact of climate change on this perennial crop.