Reticulated origin of domesticated emmer wheat supports a dynamic model for the emergence of agriculture in the fertile crescent.

Peter Civáň,Zuzana Ivaničová,Terence A Brown,Randall P Niedz

doi:10.1371/journal.pone.0081955

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.

Highlights

After the Younger Dryas (12,800–11,600 BP) – the closing cold and dry echo of the last glaciation – the nomadic hunter-gatherer communities of southwest Asia adopted a sedentary lifestyle
To re-assess the origins of domesticated emmer we developed a novel typing method based on detection of DNA polymorphisms associated with the insertion of long terminal repeat (LTR) retrotransposons in the repetitive 5S and 5.8S ribosomal RNA gene arrays
Wild emmers with alleles from the smaller clusters I and II are geographically localized in the southern Levant and the NW Fertile Crescent, respectively (Figure A part A in File S1)

Summary

Introduction

After the Younger Dryas (12,800–11,600 BP) – the closing cold and dry echo of the last glaciation – the nomadic hunter-gatherer communities of southwest Asia adopted a sedentary lifestyle. The attractive idea that a single group of enlightened people could have been responsible for the domestication of one or more staple crops within a few human generations [11] was supported by the first comprehensive genetic comparison of wild and cultivated cereal genotypes [12], which was interpreted as indicating a rapid domestication of einkorn in the Karaca Dağ region of southeast Turkey [6,13,14]. Archaeological research began to provide conflicting evidence in the form of archaeobotanical data suggesting that cereal domestication was a protracted process that began with a lengthy period of wild plant management before a slow and piecemeal emergence of the domestication phenotypes, the whole process taking several millennia [8,18,19]

Methods

Results

Conclusion