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. 2018 May 25;9(1):2077.
doi: 10.1038/s41467-018-04375-6.

Cultural hitchhiking and competition between patrilineal kin groups explain the post-Neolithic Y-chromosome bottleneck

Tian Chen Zeng  1   2 , Alan J Aw  2   3 , Marcus W Feldman  4
Affiliations

Cultural hitchhiking and competition between patrilineal kin groups explain the post-Neolithic Y-chromosome bottleneck

Tian Chen Zeng et al. Nat Commun. .

Abstract

In human populations, changes in genetic variation are driven not only by genetic processes, but can also arise from cultural or social changes. An abrupt population bottleneck specific to human males has been inferred across several Old World (Africa, Europe, Asia) populations 5000-7000 BP. Here, bringing together anthropological theory, recent population genomic studies and mathematical models, we propose a sociocultural hypothesis, involving the formation of patrilineal kin groups and intergroup competition among these groups. Our analysis shows that this sociocultural hypothesis can explain the inference of a population bottleneck. We also show that our hypothesis is consistent with current findings from the archaeogenetics of Old World Eurasia, and is important for conceptions of cultural and social evolution in prehistory.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Cumulative Bayesian skyline plots of Y-chromosome and mtDNA diversity by world regions. Reprinted from Karmin et al. with permission from Monika Karmin and under a Creative Commons License (Attribution-NonCommercial 4.0 International)
Fig. 2
Fig. 2
Explosive male-lineage expansions of the last 15,000 years. Each circle represents a phylogenetic node whose branching pattern suggests rapid expansion. The horizontal axis indicates the timings of the expansions, and circle radii reflect growth rates, namely the minimum number of sons per generation, as estimated by a two-phase growth model of Poznik et al.. Nodes are grouped by continental superpopulation (AFR: African, AMR: admixed American, EAS: East Asian, EUR: European, SAS: South Asian) and coloured by haplogroup. Line segments connect phylogenetically nested lineages. Reprinted from Poznik et al. with permission from Carlos D. Bustamante and Nature Publishing Group
Fig. 3
Fig. 3
Male-specific Y (MSY) chromosome phylogeny from next-generation sequencing data, and associated demographic reconstruction. a MSY phylogeny based on 456 samples and 35,700 SNPs. Major haplogroups are labelled. The orange box highlights recent expansions identified in several haplogroups, and the yellow box highlights more ancient expansion of deep-rooting lineages. b MSY Bayesian Skyline Plots (of effective population size against time), with different world regions indicated by colours as shown in the key. Reprinted from Batini and Jobling with permission from Mark A. Jobling and Springer Science+Business Media
Fig. 4
Fig. 4
Schematic of the steps in the simulation, according to the order described in the algorithm. a (i) Patrilineal (PT) starting conditions, where cultural groups strictly determine haplogroup type. a (ii) The non-patrilineal (NPT) condition where they are perfectly uncorrelated. b The killing step, with a more (PT) and less (NPT) patrilineal starting condition. The number of deaths in each group is inversely related to group size. The blue cultural group goes extinct in both cases. This causes the haplogroup represented by the diamonds to go extinct in PT, but no haplogroup extinction occurs in NPT. c The mutation step, where a small number of individuals in the largest haplogroup change their haplogroup. d The regeneration step, where (i) is a replica of (b) PT (iii), and (d) (ii) shows how the original number of individuals before the killing step is restored by proportionally increasing the number of individuals in all cells. e Group fission step. Where an empty row occurs, the largest cultural group splits, and half the individuals form a new cultural group in the empty row. The step in which we remove cultural groups that are too small—between (c, d) (see Methods)—is not shown
Fig. 5
Fig. 5
Cultural group and haplogroup dynamics in competing completely non-patrilineal groups (NPT) and in competing patrilineal kin groups (PT). These correspond to Figs. 2 and 3 of Supplementary Note 3. There are 100 cultural groups, or ‘tribes,’ each with size 100 at the beginning, and 500 possible haplogroups. Dynamics of the number of distinct cultural groups, cultural group diversity, the number of distinct haplogroups and haplogroup diversity are obtained by averaging over 100 simulation runs (details in Supplementary Note 3). Left panels: a Number of distinct haplogroups. b Haplogroup diversity. c Number of distinct cultural groups. d Cultural group diversity. Each graph consists of 100 pink trajectories representing 100 distinct simulation runs, and one thick solid red trajectory representing the average of the 100 pink trajectories. Black dotted lines representing confidence intervals covering two standard deviations from this mean trajectory. Note that the total number of haplogroups does not increase in this model as each haplogroup-cultural group pair has too few representatives for the mutation step of our algorithm to operate on; this is a methodological artifact and not a significant result. e The mean dynamics of the size of each of the 500 haplogroups over T = 60 generations. f The dynamics of each of the 500 haplogroups for one single run. Right panel: g–j Dynamics for the patrilineal configuration, correspond to a–d of the non-patrilineal configuration. Similarly, k, l correspond to e, f
Fig. 6
Fig. 6
Tree of Y-chromosome genotypes from samples found among cultures with hunter-gatherer subsistence, and agropastoralist subsistence. The blue background represents hunter-gatherer subsistence while the green background represents agropastoralist subsistence. Letters in red circles match individuals from sites with their archaeological context. Note that R1b-P321 is synonymous with R1b-S116.  Adapted from Figs. 3, 4, 5 and 6 of Kivisild, with addition of information from Olalde et al.. The vertical axis represents time; the position of branch points represent the ages of branch-defining mutations, with nomenclature and age from yfull (https://www.yfull.com/tree/)
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