I know this is a loooooooooong ass read but it's real science not "bro science"
Ancient X chromosomes reveal contrasting sex bias in Neolithic and Bronze Age Eurasian migrations
View ORCID ProfileAmy Goldberg,
View ORCID ProfileTorsten Günther, Noah A. Rosenberg, and Mattias Jakobsson
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PNAS March 7, 2017 114 (10) 2657-2662; first published February 21, 2017;
Ancient X chromosomes reveal contrasting sex bias in Neolithic and Bronze Age Eurasian migrations
- Edited by Wolfgang Haak, Max Planck Institute for the Science of Human History, Jena, Germany, and accepted by Editorial Board Member Richard G. Klein January 12, 2017 (received for review October 2, 2016)
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Significance
Studies of differing female and male demographic histories on the basis of ancient genomes can provide insight into the social structures and cultural interactions during major events in human prehistory. We consider the sex-specific demography of two of the largest migrations in recent European prehistory. Using genome-wide ancient genetic data from multiple Eurasian populations spanning the last 10,000 years, we find no evidence of sex-biased migrations from Anatolia, despite the shift to patrilocality associated with the spread of farming. In contrast, we infer a massive male-biased migration from the steppe during the late Neolithic and Bronze Age. The contrasting patterns of sex-specific migration during these two migrations suggest that different sociocultural processes drove the two events.
Abstract
Dramatic events in human prehistory, such as the spread of agriculture to Europe from Anatolia and the late Neolithic/Bronze Age migration from the Pontic-Caspian Steppe, can be investigated using patterns of genetic variation among the people who lived in those times. In particular, studies of differing female and male demographic histories on the basis of ancient genomes can provide information about complexities of social structures and cultural interactions in prehistoric populations. We use a mechanistic admixture model to compare the sex-specifically–inherited X chromosome with the autosomes in 20 early Neolithic and 16 late Neolithic/Bronze Age human remains. Contrary to previous hypotheses suggested by the patrilocality of many agricultural populations, we find no evidence of sex-biased admixture during the migration that spread farming across Europe during the early Neolithic. For later migrations from the Pontic Steppe during the late Neolithic/Bronze Age, however, we estimate a dramatic male bias, with approximately five to 14 migrating males for every migrating female. We find evidence of ongoing, primarily male, migration from the steppe to central Europe over a period of multiple generations, with a level of sex bias that excludes a pulse migration during a single generation. The contrasting patterns of sex-specific migration during these two migrations suggest a view of differing cultural histories in which the Neolithic transition was driven by mass migration of both males and females in roughly equal numbers, perhaps whole families, whereas the later Bronze Age migration and cultural shift were instead driven by male migration, potentially connected to new technology and conquest.
Genetic data suggest that modern European ancestry represents a mosaic of ancestral contributions from multiple waves of prehistoric migration events. Recent studies of genomic variation in prehistoric human remains have demonstrated that two mass migration events are particularly important to understanding European prehistory: the Neolithic spread of agriculture from Anatolia starting ∼9,000 y ago and migration from the Pontic-Caspian Steppe ∼5,000 y ago (
1⇓⇓⇓⇓⇓–
7). These migrations are coincident with large social, cultural, and linguistic changes, and each has been inferred to have replaced more than half of the contemporaneous gene pool of resident central Europeans.
During such events, males and females often experience different demographic histories owing to cultural factors, such as norms regarding inheritance and the residence locations of families in relation to parental residence, social hierarchy, sex-biased admixture, and inbreeding avoidance (
8⇓⇓⇓–
12). Empirical evidence suggests that sex-specific differences in migration and admixture have shaped patterns of human genomic variation worldwide, with notable examples occurring in Africa, Austronesia, Central Asia, and the Americas (
13⇓⇓–
16). These sex-specific behaviors leave signatures in the patterns of variation in genetic material that is differentially inherited between males and females in a population. Therefore, contrasting patterns of genetic variation for differentially inherited genetic material can be informative about past sociocultural and demographic events (
8⇓⇓⇓–
12,
17).
Analyses of the maternally inherited mitochondrial DNA (mtDNA) and the paternally inherited Y chromosome have lent differential support to the hypothesis that the Neolithic spread of agriculture from Anatolia occurred through a large population migration rather than a spread of technology (
18⇓⇓⇓–
22). In general, studies of Y-chromosomal data more than mtDNA have supported Anatolian migration. This pattern of results has been interpreted as evidence for male-biased migration of the population that introduced farming (
18,
20,
21). The hypothesis of male-biased migration of farming populations is consistent with ethnographic studies showing a higher frequency of patrilocality in farming than in hunter-gatherer (HG) populations, because an inheritance model through the paternal lineage would favor the persistence of farming-associated Y chromosomes as the source population would have greater flexibility in female mates. Isotopic studies from Neolithic European archeological sites suggest more female than male migration on a local scale, supporting the shift to patrilocality in the region (
10,
23). However, genetic evidence has been mixed; both Near Eastern-related mitochondrial and Y-chromosome haplotypes have been observed in European populations, which could indicate comparable male and female migration during the Neolithic spread of agriculture. For example, Haak et al. (
22) find that mitochondrial haplotype N1a, associated with Near Eastern farmers, occurs at about ∼25% frequency in Neolithic central Europeans. Later migrations from the steppe, which were previously not accounted for, may have obscured signal and interpretation (
22).
Based on archeological data, as well as ancient and modern Y chromosome data, the later migration from the Pontic-Caspian Steppe has also been hypothesized to be male-biased (
5,
24⇓⇓⇓⇓–
29). In particular, multiple large-scale studies of modern Y-chromosome data infer a rapid growth of R1a and R1b haplotypes ∼5,000 y ago (
27⇓–
29). Similarly, Haak et al. (
5) provide evidence that R1a and R1b were rare in central Europe before ∼4,500 y ago, but common soon thereafter. They also observe multiple R1b haplotypes in ancient Yamnaya individuals from the steppe. Populations in the Pontic-Caspian Steppe region, such as the Yamnaya or Pit Grave culture, are thought to have strong male-biased hierarchy, as inferred by overrepresentation of male burials, male deities, and kinship terms (
26,
30). The region is a putative origin for the domesticated horse in Europe, and the culture is known for its use of horse-driven wagons, a potential male-biased mechanism of dispersal into central Europe (
30).
Recent analytical advances in the understanding of admixture on the autosomes and the sex-specifically–inherited X chromosome and technological advances that have generated genome-wide data from many ancient samples now make it possible to consider the contrasting male and female genetic histories of prehistoric Europe. We test the hypotheses that migrations from Anatolia during the Neolithic transition and from the Pontic Steppe during the late Neolithic/Bronze Age period were male biased.
Results
Fig. 1 provides a schematic of the population admixture events that have previously been inferred (
1⇓⇓⇓⇓⇓–
7). Previous studies have inferred the relationship between the various ancient populations shown in the figure, but they did not consider a population history model. We compare genetic differentiation of the autosomes and the X chromosome between the migrating and admixed populations for each migration event: Anatolian farmers (AF) to early Neolithic central Europeans (CE) and Pontic Steppe pastoralists (SP) to late Neolithic and Bronze Age central Europeans (BA). We compute the statistic
Q (
31,
32), which is an estimator of the ratio of effective population size of the X chromosome with the ratio of effective population size of the autosomes based on the FST measure of genetic differentiation (
Materials and Methods). Under a simple demographic model with equal male and female effective sizes,
Q is expected to be 3/4, because there are three X chromosomes for every four autosomes in the population. Deviations from 3/4 may therefore show sex-biased effective population sizes, which indicate different population histories for males and females. Comparing AF and CE populations for the Neolithic transition, the ratio of X and autosomal differentiation is similar to what is expected for a non–sex-biased process (
Q = 0.700;
Table 1). In contrast, there is high relative differentiation on the X chromosome between SP and BA populations (
Q = 0.237;
Table 1), indicating strong male bias during the Pontic Steppe migration.