Reticulated Origin of Domesticated Emmer Wheat Supports a Dynamic Model for the Emergence of Agriculture in the Fertile Crescent

Abstract

We used supernetworks with datasets of nuclear gene sequences and novel markers detecting retrotransposon insertions in ribosomal DNA loci to reassess the evolutionary relationships among tetraploid wheats. We show that domesticated emmer has a reticulated genetic ancestry, sharing phylogenetic signals with wild populations from all parts of the wild range. The extent of the genetic reticulation cannot be explained by post-domestication gene flow between cultivated emmer and wild plants, and the phylogenetic relationships among tetraploid wheats are incompatible with simple linear descent of the domesticates from a single wild population. A more parsimonious explanation of the data is that domesticated emmer originates from a hybridized population of different wild lineages. The observed diversity and reticulation patterns indicate that wild emmer evolved in the southern Levant, and that the wild emmer populations in south-eastern Turkey and the Zagros Mountains are relatively recent reticulate descendants of a subset of the Levantine wild populations. Based on our results we propose a new model for the emergence of domesticated emmer. During a pre-domestication period, diverse wild populations were collected from a large area west of the Euphrates and cultivated in mixed stands. Within these cultivated stands, hybridization gave rise to lineages displaying reticulated genealogical relationships with their ancestral populations. Gradual movement of early farmers out of the Levant introduced the pre-domesticated reticulated lineages to the northern and eastern parts of the Fertile Crescent, giving rise to the local wild populations but also facilitating fixation of domestication traits. Our model is consistent with the protracted and dispersed transition to agriculture indicated by the archaeobotanical evidence, and also with previous genetic data affiliating domesticated emmer with the wild populations in southeast Turkey. Unlike other protracted models, we assume that humans played an intuitive role throughout the process.

Gourds and squashes ( Cucurbita spp.) adapted to megafaunal extinction and ecological anachronism through domestication

“…The fixation of domesticated phenotypes requires a level of reproductive isolation between cultivated and wild forms to prevent the constant back-crossing of unfavorable traits into populations under human selection (37,38). For example, emmer wheat required removal from its source region to express the phenotypic effects of domestication robustly (39), and it has been suggested that maize flourished into its dramatic, familiar, hyperdomesticated forms only after being transported out of southern Mesoamerica (40). This requirement may vary by species, with the level of isolation being linked to the genetic configuration and cultural importance of domestication traits.…”

Regional diversity on the timing for the initial appearance of cereal cultivation and domestication in southwest Asia

“…at different stages (i.e., wild, wild-cultivated, domesticated, or a mixture) and hybridized with local wild genetic lineages (24)(25)(26)(27), as well as the continued exploitation of wild cereal stands, should be considered as possible explanations for the protracted establishment of domesticated cereals in southwest Asia.…”

“…The new evidence indicates that predomestication cultivation occurred broadly at the same time in different regions (22,23). Genetic evidence indicates that cultivation practices involved multiple wild progenitor populations located across different regions, and therefore it is not possible to pinpoint the exact origins of domesticated plants (24)(25)(26)(27)(28)(29). Domesticated cereals first emerged during the EPPNB (c. 10.5 ka Cal BP), but they did not become dominant until 1,000 y later (11,12), indicating that domesticated species evolved slowly (21) and that the rates of evolution during domestication were similar to those observed in wild species subject to natural selection (30,31).…”

The Impact of Genetic Changes during Crop Domestication

“…Recently there has been considerable debate on domestication as a centric/punctuated process in the cradle of agriculture [20][21][22] versus multiple origins over protracted time periods [23][24][25]. Indeed, domesticated crops could have single or multiple origins, linear or reticulate descent from an ancestral population(s), with gene flow within and between wild and domesticated populations throughout the evolution of the crop.…”

“…Chickpea is thought to have a monophyletic origin, given the narrow distribution of its wild progenitor [26] and the limited genetic diversity of the cultigen [7,27]. Domesticated barley (Hordeum vulgare) [28,29] and emmer wheat (Triticum turgidum L.) [23] have more polyphyletic tendencies. Both show traces of mosaic eastern and western ancestral origins from opposite ends of the Near Eastern Fertile Crescent.…”