Multiregional origins of the domesticated tetraploid wheats

Abstract

We used genotyping-by-sequencing (GBS) to investigate the evolutionary history of domesticated tetraploid wheats. With a panel of 189 wild and domesticated wheats, we identified 1,172,469 single nucleotide polymorphisms (SNPs) with a read depth ≥3. Principal component analyses (PCAs) separated the Triticum turgidum and Triticum timopheevii accessions, as well as wild T. turgidum from the domesticated emmers and the naked wheats, showing that SNP typing by GBS is capable of providing robust information on the genetic relationships between wheat species and subspecies. The PCAs and a neighbour-joining analysis suggested that domesticated tetraploid wheats have closest affinity with wild emmers from the northern Fertile Crescent, consistent with the results of previous genetic studies on the origins of domesticated wheat. However, a more detailed examination of admixture and allele sharing between domesticates and different wild populations, along with genome-wide association studies (GWAS), showed that the domesticated tetraploid wheats have also received a substantial genetic input from wild emmers from the southern Levant. Taking account of archaeological evidence that tetraploid wheats were first cultivated in the southern Levant, we suggest that a pre-domesticated crop spread from this region to southeast Turkey and became mixed with a wild emmer population from the northern Fertile Crescent. Fixation of the domestication traits in this mixed population would account for the allele sharing and GWAS results that we report. We also propose that feralization of the component of the pre-domesticated population that did not acquire domestication traits has resulted in the modern wild population from southeast Turkey displaying features of both the domesticates and wild emmer from the southern Levant, and hence appearing to be the sole progenitor of domesticated tetraploids when the phylogenetic relationships are studied by methods that assume a treelike pattern of evolution.

Fig 1. PCAs based on a filtered subset of 51,365 SNPs (no indels, minor allele frequency ≥0.05, minimum depth coverage 5×, <20% missing data).

(A) 186 T. turgidum and T. timopheevii accessions, (B) 158 T. turgidum accessions, and (C) 49 naked wheat accessions. In panel A the three accessions occupying intermediate positions between the T. turgidum and T. timopheevii clusters are labelled, and in panel B the cluster of accessions including two identified as members of the judaicum race is circled. To avoid confusion, the symbols in panels A and B give the taxonomic identification of each accession after the reclassifications described in the text.

Fig 2. Neighbour joining tree for 158 T. turgidum accessions based on 1,172,469 SNPs.

The positions of the three T. turgidum subsp. carthlicum accessions and the two members of the judaicum race of T. turgidum subsp. dicoccoides are marked. Branches are labelled with code numbers as listed in S1 Table.

Fig 3. STRUCTURE analysis of 186 accessions based on 29,674 SNPs at K = 4.

Each accession is shown as a vertical line divided into coloured sections, with the length of each section proportional to the membership coefficient (Q) of the individual accession to each of the model populations. Abbreviations: arm, T. timopheevii subsp. armeniacum; car, T. turgidum subsp. carthlicum; dur, T. turgidum subsp. durum; pol, T. turgidum subsp. polonicum; tim, T. timopheevii subsp. timopheevii; tura, T. turgidum subsp. turanicum; turg, T. turgidum subsp. turgidum; E, eastern wild emmer; KD, Karaca Dağ wild emmer; N, northern wild emmer, S, south wild emmer. The three accessions from northern Syria (PI 487263, PI 487264 and K62358) that were subsequently reassigned from the north to south wild emmer groups are indicated by asterisks, and the two judaicum accessions are indicated by arrows.

Fig 4. Venn diagrams showing allele sharing between different groups of wild and domesticated T. turgidum accessions.

The domesticated set includes all emmer and naked wheat accessions from outside of southwest Asia (see S1 Table). (A) Analysis of all wild emmers based on 106,128 SNPs. (B) Re-analysis after transfer to accessions PI 487263, PI 487264 and K62358 from the ‘other’ to the south group. (C) Allele sharing between wild and domesticated emmers. (D) Allele sharing between wild emmers and naked wheats.

Fig 5. Manhattan plots displaying the results of GWAS.

The analyses compare the domesticated accessions against (A) all the wild emmer accessions, (B) the ‘other’ wild emmer accessions, and (C) the south wild emmer accessions. The horizontal blue lines represent the Bonferroni threshold [−log₁₀ (P) >6.58] and the red lines represents the 20 markers with the highest–log₁₀(P) values.