Abstract

The apple is the most common and culturally important fruit crop of temperate areas. The elucidation of its origin and domestication history is therefore of great interest. The wild Central Asian species Malus sieversii has previously been identified as the main contributor to the genome of the cultivated apple (Malus domestica), on the basis of morphological, molecular, and historical evidence. The possible contribution of other wild species present along the Silk Route running from Asia to Western Europe remains a matter of debate, particularly with respect to the contribution of the European wild apple. We used microsatellite markers and an unprecedented large sampling of five Malus species throughout Eurasia (839 accessions from China to Spain) to show that multiple species have contributed to the genetic makeup of domesticated apples. The wild European crabapple M. sylvestris, in particular, was a major secondary contributor. Bidirectional gene flow between the domesticated apple and the European crabapple resulted in the current M. domestica being genetically more closely related to this species than to its Central Asian progenitor, M. sieversii. We found no evidence of a domestication bottleneck or clonal population structure in apples, despite the use of vegetative propagation by grafting. We show that the evolution of domesticated apples occurred over a long time period and involved more than one wild species. Our results support the view that self-incompatibility, a long lifespan, and cultural practices such as selection from open-pollinated seeds have facilitated introgression from wild relatives and the maintenance of genetic variation during domestication. This combination of processes may account for the diversification of several long-lived perennial crops, yielding domestication patterns different from those observed for annual species.

Highlights

  • Domestication is a process of increasing codependence between plants and animals on the one hand, and human societies on the other [1,2]

  • We found no pair of samples assigned to the same clonal lineage unless using a threshold of 22 pairwise differences between multilocus genotypes, indicating that our samples did not include any clonal genotypes

  • Many apple cultivars, including modern cultivars in particular, share recent common ancestors, and siblings or clones of wild species can be collected unintentionally in the field. Because these features could result in a spurious genetic structure due to the presence of closely related individuals in the dataset, we checked for the presence of groups of related individuals in our dataset between M. domestica cultivars and between the individuals of each wild species

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Summary

Introduction

Domestication is a process of increasing codependence between plants and animals on the one hand, and human societies on the other [1,2]. Genetic data have suggested that domestication or the spread of domesticated traits has been fairly rapid in some annual species (e.g, maize or sunflower), with limited numbers of populations or species contributing to current diversity [10,18,19,20,21,22]. A combination of genetics and archaeology suggested a protracted model of domestication for other annual crops, and in particular for the origin of wheat or barley in the Fertile Crescent [11,23]. Trees have several biological features that make them fascinating and original models for investigating domestication: they are outcrossers with a long lifespan and a long juvenile phase, Author Summary

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