Understanding the genomic heterogeneity of North African Imazighen: from broad to microgeographical perspectives

Abstract

The strategic location of North Africa has led to cultural and demographic shifts, shaping its genetic structure. Historical migrations brought different genetic components that are evident in present-day North African genomes, along with autochthonous components. The Imazighen (plural of Amazigh) are believed to be the descendants of autochthonous North Africans and speak various Amazigh languages, which belong to the Afro-Asiatic language family. However, the arrival of different human groups, especially during the Arab conquest, caused cultural and linguistic changes in local populations, increasing their heterogeneity. We aim to characterize the genetic structure of the region, using the largest Amazigh dataset to date and other reference samples. Our findings indicate microgeographical genetic heterogeneity among Amazigh populations, modeled by various admixture waves and different effective population sizes. A first admixture wave is detected group-wide around the twelfth century, whereas a second wave appears in some Amazigh groups around the nineteenth century. These events involved populations with higher genetic ancestry from south of the Sahara compared to the current North Africans. A plausible explanation would be the historical trans-Saharan slave trade, which lasted from the Roman times to the nineteenth century. Furthermore, our investigation shows that assortative mating in North Africa has been rare.

Introduction

Over the course of history, North Africa has experienced a series of influential cultural and demographic events due to its strategic position located at the crossroads of three continental regions (Europe, Middle East, and the rest of the African continent), resulting in a complex and varied genetic structure in current populations. These migrations introduced genetic components from the neighboring regions, which are now detected in the genomes of present-day North Africans^{1,2,3,4,5,6,7,8,9}.

Ancient artifacts provide evidence of early hominin presence in North Africa dating back to ~ 2.4 Mya¹⁰, while the earliest human bones to be directly dated appeared 300 Kya¹¹. Although numerous fossils have been discovered in North Africa, Taforalt in Morocco (15,100–13,900 cal bp) is the oldest site for which genetic data is available, with human remains from the Iberomaurusian period in the Epipalaeolithic⁷. Additional Early, Middle and Late Neolithic genomes have also been retrieved from different sites in Morocco^6,8.

The process of Neolithization in North Africa was introduced by more than one migration wave. In the Early Neolithic, a first migration of European Neolithic farmers introduced farming and cultural knowledge^6,8,12,13,14. Genetic analyses, however, revealed that gene flow was unidirectional from autochthonous populations to newcomers⁸. Unlike this first migration, during the Middle Neolithic people migrated from the Levant^8,15,16 admixed with local populations from North Africa, and introduced a new ancestry, resulting in a heterogeneous landscape by the Late Neolithic. Nevertheless, low levels of genetic diversity and small effective population sizes, likely induced by periods of isolation, may have led to the Maghrebi genetic component that is present today⁸.

The Imazighen (singular Amazigh, also known by the misnomer of Berbers^17,18), are likely to be the descendants of the autochthonous inhabitants of North Africa, who inhabited the region prior to the demographic movements beginning in the Iron Age ~ 3000 years ago^18,19. At that time, languages of Afro-Asiatic language family may have already been spoken in the region, with little influence from non-African immigrants¹⁹. However, significant changes occurred as diverse human groups gradually arrived in the region. The series of historical arrivals began with the influx of Mediterranean-based populations, such as the Phoenicians (~ 900 BCE), Ionians (~ 700 BCE) and Romans (146 BCE)¹⁹. However, the Arab conquest, beginning in the seventh century, had a profound and lasting cultural impact by introducing the Arabic language and Islam, which plays an important role in the cultural landscape of the region¹⁹. Despite the fact that Arabization implied a cultural and linguistic assimilation of many autochthonous populations¹⁹, a wide variety of Amazigh languages that characterize the different groups are still preserved in the region²⁰. Besides Arabization, later population contacts such as the Ottoman and European colonial powers also had an influence in the region¹⁹.

Previous genetic studies using from classical markers to genome-wide data^{1,2,3,4,6,7,8,21,22,23,24,25,26} demonstrated that North Africa diverges from the rest of the African continent, and more closely resembles out-of-Africa (OOA) populations. Most inhabitants of North Africa carry a mix of four genetic ancestral components, including autochthonous components such as the Maghrebi component¹. Initial studies suggested that the Maghrebi component could have been introduced in a back-to-Africa movement, more than 12,000 years ago, although an in situ origin cannot be discarded^{1,27,28,29,30}. The comparison of contemporary genomes and ancient modern human samples from the region supported the presence of the local ancestral component, present in the Epipalaeolithic samples from Taforalt⁷. However, the impact of the Neolithic in North Africa reduced the proportion of this autochthonous component, although it did not erase it^2,8. Genetic studies have also demonstrated the genetic impact of the Arabic expansion and the trans-Saharan slave trade in current North Africans^2,3,31, as well as the genetic heterogeneity of North Africa, with different degrees of correlation between cultural background, geographic location, and genetics^3,5,32.

However, the lower number of genetic studies performed in North Africa compared to other continental territories plus the bias on the sampling in this vast geographic area might have prevented a clear genetic inference of its population history. The limited number of samples analyzed, in addition to the geographically and culturally distant populations under study might have biased some of the conclusions on its past demography. Most of these studies^1,