Population history and genetic adaptation of the Fulani nomads: inferences from genome-wide data and the lactase persistence trait

Abstract

BackgroundHuman population history in the Holocene was profoundly impacted by changes in lifestyle following the invention and adoption of food-production practices. These changes triggered significant increases in population sizes and expansions over large distances. Here we investigate the population history of the Fulani, a pastoral population extending throughout the African Sahel/Savannah belt.ResultsBased on genome-wide analyses we propose that ancestors of the Fulani population experienced admixture between a West African group and a group carrying both European and North African ancestries. This admixture was likely coupled with newly adopted herding practices, as it resulted in signatures of genetic adaptation in contemporary Fulani genomes, including the control element of the LCT gene enabling carriers to digest lactose throughout their lives. The lactase persistence (LP) trait in the Fulani is conferred by the presence of the allele T-13910, which is also present at high frequencies in Europe. We establish that the T-13910 LP allele in Fulani individuals analysed in this study lies on a European haplotype background thus excluding parallel convergent evolution. We furthermore directly link the T-13910 haplotype with the Lactase Persistence phenotype through a Genome Wide Association study (GWAS) and identify another genomic region in the vicinity of the SPRY2 gene associated with glycaemic measurements after lactose intake.ConclusionsOur findings suggest that Eurasian admixture and the European LP allele was introduced into the Fulani through contact with a North African population/s. We furthermore confirm the link between the lactose digestion phenotype in the Fulani to the MCM6/LCT locus by reporting the first GWAS of the lactase persistence trait. We also explored other signals of recent adaptation in the Fulani and identified additional candidates for selection to adapt to herding life-styles.

Subsistence strategy was the main factor driving population differentiation in the bidirectional corridor of the African Sahel

“…Previously published data from autosomal SNP arrays and whole‐genome studies largely corroborate the genetic structure of Sahelian populations as inferred here from uniparental markers, that is, the presence of an eastern Sahelian and western Sahelian genetic component with an admixture zone in the Lake Chad basin, observed in our data, is in agreement with the findings of Triska et al (). Autosomal‐based studies also point to a unique genetic composition and low population stratification in the Fulani and to a West African genetic background of the Songhai (Triska et al, ; Vicente et al, ). Our data on uniparental markers, on the other hand, indicate differences in the population histories of male and female subpopulations.…”

“…It has been well established that in the populations of eastern and central Sahel there is a discernible Eurasian genetic component introduced over a long period of time by numerous migration events from different non‐African regions (Galego Llorente et al, ; Haber et al, ; Pickrell et al, ). Successive waves of migration are clearly reflected in both maternal and paternal genetic pools (Bučková et al, ; Černý et al, ; Podgorná et al, ; Shriner & Rotimi, ) and also in autosomal datasets as shown by allele frequency based methods (Triska et al, ; Vicente et al, ).…”

Sahelian pastoralism from the perspective of variants associated with lactase persistence

“…It has been suggested that the Fulani acquired the −13910*T haplotype by admixing with a North African population which had some Eurasian ancestry, so that this variant in the Fulani population has the same descent as the variant found in Eurasia (Coelho et al, 2005; Mulcare et al, 2004; Ranciaro et al, 2014). Furthermore, it has been estimated that two distinct admixture events took place, one 1,828 and the other 302 years ago (Vicente et al, 2019). Our estimates of the growth and selection of −13910*T haplotype in the Fulani indicate an earlier dating than the abovementioned admixture times (Vicente et al, 2019) and are consistent rather with the estimates of Coelho et al (2005), who proposes a period of 10,125–6,060 years ago.…”

“…Based on (probably different) Fulani DNA samples but again from northern Cameroon, it has been demonstrated that their −13910*T variant shares its haplotype backgrounds with Europeans (Coelho et al, 2005; Ranciaro et al, 2014), which suggests a single mutation event for this mutation and its introduction via admixture of non‐African sources and through gene flow. A recent study of Fulani pastoralists from Ziniaré, Burkina Faso (Vicente et al, 2019) confirmed these suggestions and showed that this variant shares its haplotype background with Eurasians and that ancestors of the Fulani probably acquired the haplotype via recent admixture events which took place in northern Africa.…”

“…By doing so, we included all three linguistic groups and both lifestyles currently found in the Sahel/Savannah belt, but a majority of our samples come from two pastoral populations: the Fulani and the Arabs. While Fulani are autochthonous sub‐Saharan population groups whose ancestors admixed with population(s) of Eurasian ancestry (Kulichová et al, 2017; Triska et al, 2015; Vicente et al, 2019), Arabs are an originally Eurasian population who arrived from Arabia from the seventh century CE onward. They were present in the Lake Chad basin in the 14th century (Zeltner, 2002) and nowadays, they are admixed with local sub‐Saharan populations (Priehodová, Abdelsawy, Heyer, & Černý, 2014; Priehodová et al, 2017).…”