Molecular Clocks and Archeogenomics of a Late Period Egyptian Date Palm Leaf Reveal Introgression from Wild Relatives and Add Timestamps on the Domestication.

Natalia Przelomska ,Michaela Preick,Muriel Gros-Balthazard,Alexandre Antonelli,Peter Petoe,Óscar Alejandro Pérez-Escobar ,Philippa Ryan,Steven Dodsworth,Rowan J Schley ,Sidonie Bellot,Manuela Lehmann,Barbara Gravendeel,Michael D Purugganan ,Rudy Diaz,Mark Nesbitt,Irka Hajdas,William J Baker ,Diego Bogarín,Tom Wells,Alexander S T Papadopulos ,María Fernanda Torres Jiménez ,Benedikt G Kuhnhäuser ,Ilia J Leitch ,Wolf L Eiserhardt ,Michael Hofreiter,Guillaume Chomicki,Susanne S Renner ,Rafał M Gutaker ,Jonathan M Flowers

doi:10.1093/molbev/msab188

Abstract

The date palm, Phoenix dactylifera, has been a cornerstone of Middle Eastern and North African agriculture for millennia. It was first domesticated in the Persian Gulf, and its evolution appears to have been influenced by gene flow from two wild relatives, P. theophrasti, currently restricted to Crete and Turkey, and P. sylvestris, widespread from Bangladesh to the West Himalayas. Genomes of ancient date palm seeds show that gene flow from P. theophrasti to P. dactylifera may have occurred by ∼2,200 years ago, but traces of P. sylvestris could not be detected. We here integrate archeogenomics of a ∼2,100-year-old P. dactylifera leaf from Saqqara (Egypt), molecular-clock dating, and coalescence approaches with population genomic tests, to probe the hybridization between the date palm and its two closest relatives and provide minimum and maximum timestamps for its reticulated evolution. The Saqqara date palm shares a close genetic affinity with North African date palm populations, and we find clear genomic admixture from both P. theophrasti, and P. sylvestris, indicating that both had contributed to the date palm genome by 2,100 years ago. Molecular-clocks placed the divergence of P. theophrasti from P. dactylifera/P. sylvestris and that of P. dactylifera from P. sylvestris in the Upper Miocene, but strongly supported, conflicting topologies point to older gene flow between P. theophrasti and P. dactylifera, and P. sylvestris and P. dactylifera. Our work highlights the ancient hybrid origin of the date palms, and prompts the investigation of the functional significance of genetic material introgressed from both close relatives, which in turn could prove useful for modern date palm breeding.

Highlights

The shift from a hunter-gatherer lifestyle to a settled, agricultural subsistence strategy some 10,000–12,000 years ago was arguably one of the most important processes in human history (Diamond 2002), and together with husbandry of animals it allowed the sustained nutrition of large sedentary human population settlements (Fuller et al 2014; Larson et al 2014; Richter et al 2017; Arranz-Otaegui et al 2018)
The first evidence of date cultivation comes from the end of the fourth millennium B.C.E. in the Persian Gulf region, and it is presumed that date palms were first domesticated in this region, perhaps from wild populations found in Oman (Gros-Balthazard et al 2017)
The clustering of Asian P. sylvestris with selected North African date palm cultivars in plastid phylogenies has been previously reported (Pintaud et al 2013; Chaluvadi et al 2019; Flowers et al 2019; Mohamoud et al 2019), opening the question of whether gene flow or ancestral polymorphisms are responsible for this pattern (Flowers et al 2019)

Summary

Introduction

The shift from a hunter-gatherer lifestyle to a settled, agricultural subsistence strategy some 10,000–12,000 years ago was arguably one of the most important processes in human history (Diamond 2002), and together with husbandry of animals it allowed the sustained nutrition of large sedentary human population settlements (Fuller et al 2014; Larson et al 2014; Richter et al 2017; Arranz-Otaegui et al 2018). The date palm (Phoenix dactylifera L.) has been a cornerstone of Middle Eastern and North African agriculture for millennia and remains a crop of major importance with more than 9 million tonnes of fruits produced in 2019 (FAO 2021). Archeological evidence, ancient texts, and iconographies all point to the use of date palms for millennia in North Africa, the Middle East, and as far as Pakistan (Tengberg 2012; Gros-Balthazard and Flowers 2021; Gros-Balthazard, Baker, et al 2021; Gros-Balthazard, Battesti, et al 2020). The first evidence of date cultivation comes from the end of the fourth millennium B.C.E. in the Persian Gulf region (reviewed in Tengberg [2012]), and it is presumed that date palms were first domesticated in this region, perhaps from wild populations found in Oman (Gros-Balthazard et al 2017). Population-genomic analyses of date palm cultivars and wild Phoenix species revealed extensive introgressive hybridization of the North African date palm with P. theophrasti Greuter from Crete and Turkey—up to 18% of the genome of North African cultivars was shared with this species (Flowers et al 2019), and an analysis of DNA from germinated $2,200-year-old seeds of P. dactylifera further supports this hybridization by $2,200 years ago (GrosBalthazard et al 2021)

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