African admixture in Europe


African admixture in Europe refers to the presence of admixture events attributable to dispersal of populations inhabiting Africa in the genetic history of Europe. Certain Y-DNA and mtDNA lineages are thought to have spread from Northeast Africa to the Near East during the later Pleistocene, and from there to Europe with the Neolithic Revolution. More recent, direct African admixtureprimarily Berber admixture from North Africais associated with the Carthaginian period as well as Muslim conquests of the early medieval period, and is primarily concentrated in western and southern Iberian peninsula, averaging from 2.4% in the North East to 10.6% in the South and West of the peninsula. North African admixture has also been detected in the Italian island of Sicily.

Neolithic

The change from hunting and gathering to agriculture during the Neolithic Revolution was a watershed in world history. The societies that first made the change to agriculture are believed to have lived in the Middle East around 10,000 BCE. Agriculture was introduced into Europe by migrating farmers from the Middle East. According to the demic diffusion model, these Middle Eastern farmers either replaced or interbred with the local hunter-gather populations that had been living in Europe since the Out of Africa migration.
It has been suggested that the first Middle Eastern farmers reflected North African influences. There have been suggestions that some genetic lineages found in the Middle East arrived there during this period. The first agricultural societies in the Middle East are generally thought to have emerged after, and perhaps from, the Natufian culture between 12,000 and 10,000 BCE. The latter group was widely semi-sedentary even before the introduction of agriculture. An important migration from North Africa across the Sinai also appears to have occurred before the formation of the Natufian..

Historical period

In historical times, there has been a period of North African influence in southern Europe, especially western-southern Iberia and parts of Southern Italy, during various Muslim conquests. The genetic effect of this period on modern European populations is the subject of discussion. In more recent history, the peoples of Europe and Africa came into contact during the exploration and colonization of Africa and as a consequence of the Atlantic slave trade.

Assessing African genetic contributions in non-Africans

The evolutionary forces that contribute to patterns of human genetic variation include new mutations, natural selection, sexual selection, genetic drift, population bottlenecks, founder effects, isolation by distance, genetic admixture and barriers to gene flow. The most influential factors affecting human genetic variation are founder effects and isolation by distance.
Founder effect occurs when a population is established by a small number of individuals who have departed from a much larger population. Several generations after the population has expanded, individuals will still possess the limited gene pool of the founders. Therefore, founder effects result in a loss of genetic diversity. Genetic evidence suggests that the Out of Africa migration involved only small numbers of individuals. The African migrants carried a small subset of the prehistoric African genetic diversity, resulting in a founder effect on the non-African population. As humans spread across the globe populating Europe, Asia, Oceania, and the Americas, there were several founder effects. As a result of these serial founder effects, genetic diversity tends to decrease with distance from Africa.
The other major factor contributing to patterns of human genetic variation is "isolation by distance". According to this model, populations that live near one another are more likely to exchange mates than populations that live farther apart. As a result, populations that live near one another are genetically more similar than populations that live far apart.
Africa OceaniaEast Asia Europe
Oceania 24.7
East Asia 20.6 10
Europe 16.6 13.5 9.7
America 22.6 14.6 8.9 9.5

Genetic distance is a measure used to compare the genetic relationship between populations. It is based on the principle that populations that share similar frequencies of a trait are more closely related than populations that have different frequencies of a trait. The genetic distance between two populations increases linearly with the geographic distance between them, due to isolation by distance and serial founder effects. Genetic admixture increases the genetic diversity of a population. When admixture occurs between populations, the genetic distance between the two populations is reduced.
applied genetic distance measures to various populations around the world to infer phylogenetic relationships. All non-African populations are more closely related to one another than they are to African populations. This is consistent with a founder effect on the non-African population in that only a few individuals participated in the initial Out of Africa migration. The largest genetic distances observed are between Africa and Oceania and between Africa and the Americas. This is consistent with the isolation by distance and serial founder effects.
suggests that the genetic distance between Sub-Saharan Africa and Europe is anomalously lower than it would be if the two populations had been evolving independently. The study suggests that the lower genetic distance between Europe and Africa can be explained by genetic admixture.

Defining African admixture

Generally, markers and lineages used to characterize African admixture are those that are believed to be specific to Africa. There are also DNA polymorphisms that are shared between populations native to Europe, West Asia, North Africa and the Horn of Africa, such as the y-chromosomal haplogroup E1b1b and the mitochondrial haplogroup M1.
With regard to the paternal haplogroup E1b1b and maternal haplogroup M1, derivatives of these clades have been observed in prehistoric human fossils excavated at the Ifri n'Amr or Moussa site in Morocco, which have been radiocarbon-dated to the Early Neolithic period. Ancient DNA analysis of these specimens indicates that they carried paternal haplotypes related to the E1b1b1b1a subclade and the maternal haplogroups U6a and M1, all of which are frequent among present-day communities in the Maghreb. These ancient individuals also bore an autochthonous Maghrebi genomic component that peaks among modern Berbers, indicating that they were ancestral to populations in the area. Additionally, fossils excavated at the Kelif el Boroud site near Rabat were found to carry the broadly-distributed paternal haplogroup T-M184 as well as the maternal haplogroups K1, T2 and X2, the latter of which were common mtDNA lineages in Neolithic Europe and Anatolia. These ancient individuals likewise bore the Berber-associated Maghrebi genomic component. This altogether indicates that the Late Neolithic Kelif el Boroud inhabitants were ancestral to contemporary populations in the area, but also likely experienced gene flow from Europe.
Other lineages that are now found in Africa and Europe may have a common origin in Asia. One subclade of haplogroup U, namely U6a1, is known to have expanded from northern and eastern Africa back into Europe even though haplogroup U6 is considered to have originated in the Middle East. Other lineages are known to have moved from Europe directly into Africa, for example mitochondrial haplogroups H1 and H3. Such bidirectional migrations between Africa and Eurasia complicate the task of defining admixture.

Y-DNA

One proposed example of Holocene gene flow from North Africa to Europe, via the Middle East, is thought to be E1b1b, which is thought to have emerged about 40,000 years ago in north-east Africa, and branches of it are thought to have migrated to the Middle East by 14,000 years ago during the late Pleistocene period.
Entering the late mesolithic Natufian culture, the E1b1b1a2 subclade has been associated with the spread of farming from the Middle East into Europe either during or just before the Neolithic transition. E1b1b1 lineages are found throughout Europe but are distributed along a south-to-north cline, with an E1b1b1a mode in the Balkans.
In separate migrations, E lineages in the form of the E1b1b1b subclade appear to have entered Europe from Northwest Africa into Iberia. In a sample of European males, Cruciani et al. observed haplogroup E at a frequency of 7.2%. The timing of this movement has been given widely varying estimates.
In much of Europe, frequencies of E lineages are very low, usually less than 1%. For example, Cruciani et al. report such lineages at 2% in southern Portugal, 4% in northern Portugal, 2.9% in Istanbul, and 4.3% among Turkish Cypriots. E1b1a is closely related to E1b1b, the most frequent clade in Europe. E lineages that are not E1b1a or E1b1b could therefore reflect either a recent expansion associated with E1b1a or ancient population movements associated with E1b1b. For example, haplogroup E1a lineages have been detected in Portugal, among Italians in Calabria, and among Albanians in Calabria. According to a study by, the distribution of haplogroup E1a lineages in Portugal was independent of the distribution of the younger and more ubiquitous E1b1a. The authors suggest that this distribution is consistent with a prehistoric migration from Africa to Iberia, possibly alongside mtDNA haplogroup U6.
Haplogroups A and B are thought to have been the predominant haplogroups in central and southern Africa prior to the Bantu Expansion. Currently these haplogroups are less common than E lineages. In a sample of 5,000 African men, haplogroup A had a frequency of 5%. Haplogroup A has rare occurrences in Europe, but recently the haplogroup was detected in seven indigenous British males with the same Yorkshire surname.
The subclade E3b1 has a wide distribution in North Africa, the Horn of Africa, the Middle East, and Europe. This haplogroup, in Italy, is represented by E-M78, E-M123 and E-M81 and reaches a frequency of 8% in northern and central Italy and slightly higher, 11%, in the south of that country.
It has also been argued that the European distribution of E3b1 is compatible with the Neolithic demic diffusion of agriculture; thus, two subclades—E3b1a-M78 and E3b1c-M123—present a higher occurrence in Anatolia, the Balkans, and the Italian peninsula. Another subclade, E3b1b-M81 is associated with Berber populations and is commonly found in regions that have had historical gene flow with northern Africa, such as the Iberian Peninsula, the Canary Islands, and Sicily.
North African Y-DNA E-M81 was found at a total of 41.1% among "pasiegos" from Cantabria, Spain. That is the highest frequency observed in Europe to date.
In Sardinians, Sub-Saharan Y-DNA lineages A1b1b2b and E1a1 were found at a total of 1.0%.
In Majorcans, Sub-Saharan Y-DNA lineage E-V38 was found at a total of 3.2%.
Sub-Saharan Y-DNA lineages E3a, E1, BC*, , and E3* are found between 1 and 5% in Portugal, Valencia, Majorca, Cantabria, Málaga, Seville, and Galicia.

mtDNA

lineages are relatively infrequent throughout Europe with the exception of Iberia, where frequencies as high as 22% have been reported, and some regions of Southern Italy, where frequencies as high as 2% and 3% have been found. According to a study in 2012 by Cerezo et al., about 65% of the European L lineages most likely arrived in rather recent historical times and about 35% of L mtDNAs form European-specific subclades, revealing that there was gene flow from Sub-Saharan Africa toward Europe as early as 11,000 years ago.
Map showing the distribution of Sub-Saharan mtDNA in Europe
Map is From Cerezo et al. 2012
Universidad de Santiago de Compostela
Iberia having the highest amount and strongest concentration of Sub-Saharan mtDNA in Europe.

In Iberia the mean frequency of haplogroup L lineages reaches 3.83%; the frequency is higher in Portugal than in Spain, and without parallel in the rest of Europe. In both countries, frequencies vary widely between regions, but with increased frequencies observed for Madeira, southern Portugal, Córdoba, Huelva, Canary Islands, Extremadura and Leon. In the Autonomous regions of Portugal, L haplogroups constituted about 13% of the lineages in Madeira, significantly more than in the Azores. In the Canary Islands, frequencies have been reported at 6.6%. Regarding Iberia, current debates are concerned with whether these lineages are associated with prehistoric migrations, the Islamic occupation of Iberia, or the slave trade. suggested that African lineages in Iberia were predominantly the result of the Atlantic slave tarade. revealed that most of the L lineages in Iberia matched Northwest African L lineages rather than contemporary Sub-Saharan L lineages. The authors suggest that this pattern indicates that most of the Sub-Saharan L lineages entered Iberia in prehistoric times rather than during the slave trade. According to, the Sub-Saharan lineages found in Iberia matched lineages from diverse regions in Africa. They suggest this pattern is more compatible with a recent arrival of these lineages after slave trading began in the 15th century. According to the study, alternative scenarios that invoke much older and demographically more significant introductions or that claim a substantial role of the Roman and/or Islamic periods on the introduction of Sub-Saharan lineages seem unlikely. extracted DNA from human remains that were exhumed from old burial sites in Al-Andalus, Spain. The remains date to between the 12th and 13th centuries. The frequency of Sub-Saharan lineages detected in the medieval samples was 14.6% and 8.3% in the present population of Priego de Cordoba. The authors suggest the Muslim occupation and prehistoric migrations before the Muslim occupation would have been the source of these lineages. The highest frequencies of Sub-Saharan lineages found so far in Europe were observed by Álvarez et al. in the comarca of Sayago which is, according to the authors, "comparable to that described for the South of Portugal" and by Pereira et al. 2010 in Alcácer do Sal.
In Italy, haplogroup L lineages are present at lower frequencies than in Iberia—between —between 2% and 3%— and are detected only in certain regions: Latium, Volterra, Basilicata, and Sicily.
In eastern Europe, haplogroup L lineages are present at very low frequencies. Though a high diversity of African mtDNA lineages have been detected, few lineages have accumulated enough mutations in Europe to form monophyletic clusters. detected only two monophyletic clusters, L1b and L3b, in Russians, with an estimated age no greater than 6,500 years. identified African L1b, L2a, L3b, L3d and M1 clades in Slavic populations at low frequencies. L1b, L3b and L3d had matches with West African populations, indicating that these lineages probably entered Europe through Iberia. One lineage, L2a1a, appeared to be much older, indicating that it may have entered Europe in prehistoric times. This clade was possibly related to L2a1 clades identified in ten individuals of Ashkenazi heritage from France, Germany, Poland, Romania, and Russia. L2a lineages are widespread throughout Africa; as a result, the origins of this lineage are uncertain.
Haplogroup M1 is also found in Europe at low frequencies. In a study by González et al., haplogroup M1 had a frequency of 0.3%. The origins of haplogroup M1 have yet to be conclusively established.
A 2015 study found that a prehistoric episode would be the main contributor to the sub-Saharan presence in Mediterranean Europe.

Frequencies of haplogroup L lineages

A similar study by Auton et al. —which also contains an admixture analysis chart but no cluster membership coefficients—shows little to no Sub-Saharan African influence in a wide array of European samples, i.e. Albanians,
Austrians, Belgians, Bosnians, Bulgarians, Croatians, Cypriots, Czechs, Danes, Finns, Frenchmen, Germans, Greeks,
Hungarians, Irish, Italians, Kosovars, Lithuanians, Latvians, Macedonians, Netherlanders, Norwegians, Poles, Portuguese,
Romanians, Russians, Scots, Serbians, Slovaks, Slovenians, Spaniards, Swedes, Swiss, Ukrainians, subjects of the United Kingdom, and Yugoslavians.
Haplogroup U6, to which a North African origin has been attributed, is largely distributed among Mozabites and Mauritanians. In other Northwest Africans, the frequency of U6 ranges from 4.2% in Tunisians to 8% in Moroccan Arabs. In Europe, U6 is most common in Spain and Portugal.

Frequencies of Haplogroup U6 lineages

Admixture

Further studies have shown that the presence of haplotype GM*1,17 23' 5* in southern Europe. This haplotype is considered a genetic marker of Sub-Saharan Africa, where it shows frequencies of about 80%. Whereas, in non-Mediterranean European populations, that value is about 0.3%, in Spain the average figure for this African haplotype is nearly eight times greater at 2.4%, and it shows a peak at 4.5% in Galicia. Values of around 4% have also been found in Huelva and in the Aran valley in the Pyrenees. According to Calderón et al. 2007, although some researchers have associated African traces in Iberia to Islamic conquest, the presence of GM*1,17 23' 5* haplotype in Iberia may in fact be due to more ancient processes as well as more recent ones through the introduction of genes from black slaves from Africa.

In Sicily the North African haplotype Gm 5*;1;17; ranges from 1.56% at Valledolmo to 5.5% at Alia. The hypothesis is that the presence of this haplotype suggests past contacts with people from North Africa. The introduction of African markers could be due to the Phoenician colonization at the end of the second millennium B.C. or to the more recent Arab conquest.

Sickle cell trait

Sickle cell genes of African origin have been detected in Europe, mostly in the Mediterranean region. The sickle cell trait is associated with resistance to malaria. Individuals with one copy of the sickle cell gene, heterozygotes, have higher resistance to malaria than individuals with no sickle cell genes. In regions affected by malaria, the fertility of sickle cell heterozygotes will be higher than average. Individuals with two copies of the sickle cell gene, homozygotes, will be affected by sickle cell disease and historically have had lower than average fertility. The sickle cell trait is thus an example of heterozygote advantage which is subject to balancing selection. When the sickle cell trait is introduced into a region affected by malaria, balancing selection will, on one hand, act to increase the frequency of the trait to counter malaria. On the other hand, if the frequency of the trait in the population becomes high enough so that homozygotes with sickle cell disease become common, balancing selection will act to limit the spread of the trait. Therefore, in regions affected by malaria, the sickle cell trait is maintained at intermediate frequencies relative to the incidence of malaria.
In Africa, malaria is believed to be one of the most important factors that contributed to restricting population growth in prehistoric times. Sickle cell mutations are believed to have occurred independently at least five times. Four variants are of African origin and one of Indian/Arabian origin. The African variants are referred to as Cameroon, Senegal, Benin and Bantu. The emergence of the sickle cell trait would have contributed to population expansion, with the emergence of farming into tropical regions where malaria was endemic.
Archeological and historical evidence suggests that malaria has been endemic in the
Mediterranean regions of Europe in historical times. In eastern Mediterranean regions—such as Italy, Greece, Albania, and Turkey—the Benin haplotype is the most frequent sickle cell variant. The Benin haplotype is also the most frequent variant in the Middle East and has been observed in Syrians, Palestinians, Italians, Israeli Arabs, Israeli Jews and western Saudi Arabians. This suggests that the Benin haplotype may have expanded from West Africa into North Africa and then into the Middle East and Europe. The spread of the Benin haplotype to the Mediterranean region has been associated with various events, including Late Stone Age expansions from West Africa into North Africa, the trans-Saharan trade, and the Arab Slave Trade. The occurrence of sickle cell trait is particularly high in Sicily, where frequencies of 13% have been reported. Portugal is the only region in Europe where the Senegal and Bantu haplotypes are frequent. These may be associated with Portuguese naval exploits, including the Atlantic Slave Trade and the colonization of various African countries.
In Europe, the highest prevalence of the disease has been observed in France as a result of population growth in African-Caribbean regions of overseas France, and now immigration essentially from North and Sub-Saharan Africa to mainland France. SCD has become the most common genetic disease in this country. In 2010, 31.5% of all newborns in mainland France had parents originated from a region defined "at risk" and were screened for SCD. The Paris metropolitan district is the region that accounts for the largest number of at-risk individuals. Indeed, 60% of all newborns in this area in 2010 had parents originated from a region defined as "at-risk" and were screened for SCD. The second largest number of at-risk individuals is in Provence-Alpes-Côte d'Azur, at nearly 43.2%, and the lowest number is in Brittany, at 5.5%.

Paleoanthropology

The migration of farmers from the Middle East into Europe is believed to have significantly influenced the genetic profile of present-day Europeans. Some recent studies have focused on corroborating current genetic data with the archeological evidence from Europe, the Middle East, and Africa. The Natufian culture, which existed about 12,000 years ago, has been the subject of various archeological investigations, as it is generally believed to be the source of the European and North African Neolithic.
According to a hypothesis stated by, the Natufian culture emerged from the mixing of two Stone Age cultures: the Kebaran, a culture indigenous to the Levant, and the Mushabian, a culture introduced into the Levant from North Africa†. It is suggested that the Mushabian culture originated in Africa, given that archeological sites with Mushabian industries in the Nile Valley predate those in the Levant†. The Mushabians would have then moved into the Sinai from the Nile Delta bringing with them their technologies†. states: "the population overflow from Northeast Africa played a definite role in the establishment of the Natufian adaptation, which in turn led to the emergence of agriculture as a new subsistence system".
A study by analysed human remains from the Natufian culture.
According to the study, there is evidence of Sub-Saharan influences in the Natufian samples. They argue that these influences would have been diluted by the interbreeding of the Neolithic farmers from the Near East with the indigenous foragers in Europe. associate the Sub-Saharan influences detected in the Natufian samples with the migration of E1b1b lineages from Northeast Africa to the Levant and then into Europe.
According to the most recent ancient DNA analyses conducted by Lazaridis et al. on Natufian skeletal remains from present-day northern Israel, the Natufians in fact shared no evident genetic affinity to sub-Saharan Africans. The authors also state that they were unable to test for affinity in the Natufians to early North African populations using present-day North Africans as a reference because present-day North Africans owe most of their ancestry to back-migration from Eurasia. The Natufians carried the Y-DNA haplogroups E1b1b1b2, CT, and E1b1. In terms of autosomal DNA, these Natufians carried around 50% of the Basal Eurasian and 50% of Western Eurasian Unknown Hunter Gather components. However, they were slightly distinct from the northern Anatolian populations that contributed to the peopling of Europe, who had higher Western Hunter-Gatherer inferred ancestry. Natufians were strongly genetically differentiated from Neolithic Iranian farmers from the Zagros Mountains, who were a mix of Basal Eurasians and Ancient North Eurasians. This might suggest that different strains of Basal Eurasians contributed to Natufians and Zagros farmers, as both Natufians and Zagros farmers descended from different populations of local hunter gatherers. Mating between Natufians, other Neolithic Levantines, Caucasus Hunter Gatherers, Anatolian and Iranian farmers is believed to have decreased genetic variability among later populations in the Middle East. The scientists suggest that the Levantine early farmers may have spread southward into East Africa, bringing along Western Eurasian and Basal Eurasian ancestral components separate from that which would arrive later in North Africa.
† The Mushabian industry is now known to have originated in the Levant from the previous lithic industries of the region of Lake Lisan. The Mushabian industry was originally thought to have originated in Africa because the microburin technique was not yet known to be much older in the eastern Levant. Currently there is no known industry to connect with the African migration that occurred 14,700 years ago, but it no doubt caused a population expansion in the Negev and Sinai which would not have accommodated an increase in population with the meager resources of a steppe/desert climate. Since all of the known cultures in the Levant at the time of the migration originated in the Levant and an archaeological culture cannot be associated with it, there must have been assimilation into a Levantine culture at the onset, most likely the Ramonian which was present in the Sinai 14,700 years ago.

Footnotes