Evolution of fruit and seed traits during almond naturalization

Cultivated plant species often naturalize and enter wild communities in a process known as feralization. To successfully feralize, crops must overcome ecological barriers and may undergo selection on certain traits, diverging phenotypically and genetically from their crop ancestors. In spite of the agronomic and ecological relevance of crop feralization, the eco-evolutionary dynamics driving it remain understudied. In this paper, we evaluated phenotypic and genotypic differentiation in fruit and seed traits during the naturalization of the almond tree (Prunus dulcis (Mill.) D.A. Webb) in SE Iberia and evaluated the potential role of natural selection in this process. To do so, we investigated the patterns of genetic divergence between cultivated and feral populations using functional (the cyanogenesis Sk gene) and neutral (17 SSR loci) markers and analysed morphological and biochemical traits in kernels of 342 individuals from 15 cultivated and 24 feral populations. We detected very little genetic differentiation in neutral markers between cultivated and feral populations. The majority of the observed genetic variation was due to differences within each type. Conversely, the recessive allele sk responsible for seed toxicity was significantly more frequent in feral populations. Phenotypic differentiation between cultivated and naturalized almond populations was also significant. Feral almond kernels were smaller and lighter, had denser and more resistant shells (endocarps) and more toxic seeds. Selection analyses indicated that these genetic and phenotypic patterns might be driven by directional selection on fruit and seed traits, potentially linked to defence against predation. Synthesis. Our findings indicate that almond naturalization is consistent with strong directional selection on fruits and seeds, leading to smaller and more toxic seeds encased in harder endocarps. Accordingly, we propose that feralization of this crop is, at least to some degree, driven by adaptive evolution of dispersal and recruitment traits.This study was funded by the Spanish Ministry of Economy and Finance (grant CGL2016-79950-R) and the Junta de Andalucia I+D+i program (grant P18-RTJ-4704)