Genome-Wide Diversity in the Levant Reveals Recent Structuring by Culture

The Levant is a region in the Near East with an impressive record of continuous human existence and major cultural developments since the Paleolithic period. Genetic and archeological studies present solid evidence placing the Middle East and the Arabian Peninsula as the first stepping-stone outside Africa. There is, however, little understanding of demographic changes in the Middle East, particularly the Levant, after the first Out-of-Africa expansion and how the Levantine peoples relate genetically to each other and to their neighbors. In this study we analyze more than 500,000 genome-wide SNPs in 1,341 new samples from the Levant and compare them to samples from 48 populations worldwide. Our results show recent genetic stratifications in the Levant are driven by the religious affiliations of the populations within the region. Cultural changes within the last two millennia appear to have facilitated/maintained admixture between culturally similar populations from the Levant, Arabian Peninsula, and Africa. The same cultural changes seem to have resulted in genetic isolation of other groups by limiting admixture with culturally different neighboring populations. Consequently, Levant populations today fall into two main groups: one sharing more genetic characteristics with modern-day Europeans and Central Asians, and the other with closer genetic affinities to other Middle Easterners and Africans. Finally, we identify a putative Levantine ancestral component that diverged from other Middle Easterners ~23,700–15,500 years ago during the last glacial period, and diverged from Europeans ~15,900–9,100 years ago between the last glacial warming and the start of the Neolithic. Population stratification caused by nonrandom mating between groups of the same species is often due to geographical distances leading to physical separation followed by genetic drift of allele frequencies in each group. In humans, population structures are also often driven by geographical barriers or distances; however, humans might also be structured by abstract factors such as culture, a consequence of their reasoning and self-awareness. Religion in particular, is one of the unusual conceptual factors that can drive human population structures. This study explores the Levant, a region flanked by the Middle East and Europe, where individual and population relationships are still strongly influenced by religion. We show that religious affiliation had a strong impact on the genomes of the Levantines. In particular, conversion of the region's populations to Islam appears to have introduced major rearrangements in populations' relations through admixture with culturally similar but geographically remote populations, leading to genetic similarities between remarkably distant populations like Jordanians, Moroccans, and Yemenis. Conversely, other populations, like Christians and Druze, became genetically isolated in the new cultural environment. We reconstructed the genetic structure of the Levantines and found that a pre-Islamic expansion Levant was more genetically similar to Europeans than to Middle Easterners.