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, 8 (5), e1002703

New Insight Into the History of Domesticated Apple: Secondary Contribution of the European Wild Apple to the Genome of Cultivated Varieties

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New Insight Into the History of Domesticated Apple: Secondary Contribution of the European Wild Apple to the Genome of Cultivated Varieties

Amandine Cornille et al. PLoS Genet.

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.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Geographic origins of the samples of the four wild Malus species used: M. sylvestris (blue), M. orientalis (yellow), M. baccata (purple), and M. sieversii (red).
Samples of unknown origin (N = 28) were not projected onto the map.
Figure 2
Figure 2. Proportions of ancestry of Malus genotypes from five species (N = 770) from K = 2 to K = 8 ancestral genepools (“clusters”) inferred with the STRUCTURE program.
Each individual is represented by a vertical bar, partitioned into K segments representing the amount of ancestry of its genome in K clusters. When several clustering solutions (“modes”) were represented within replicate runs, the proportion of simulations represented by each mode is given.
Figure 3
Figure 3. Proportions of ancestry in two ancestral genepools inferred with the STRUCTURE program, based on datasets including M. domestica (green, N = 299) and each of the four wild Malus species (red).
The x-axis is not to scale (details in Table S2).
Figure 4
Figure 4. Admixture models compared in approximate Bayesian computations.
Model a assumes that M. domestica is derived from M. sieversii and that the ancestral M. domestica population was involved in reciprocal introgression events with M. orientalis and M. sylvestris, and subsequently introgressed back into M. sieversii. Model b assumes no introgression from M. domestica into wild species, model c assumes the only admixture event is from M. sylvestris into M. domestica, and model d assumes no admixture. Admixture times between M. domestica and the three wild species were fixed (see text). Abbreviations: Nk, effective population sizes; Tk, divergence times; r1, r3, r4 introgression from M. domestica into M. sieversii, M. sylvestris, and M. orientalis respectively; r2, r5 introgression from M. sylvestris and M. orientalis, respectively, into M. domestica.
Figure 5
Figure 5. Proportions of ancestry of M. domestica genotypes (cider and dessert apples) in two ancestral genepools inferred with the STRUCTURE program.

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