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Cited by 28Forensic and Genetic ResearchGenetic diversity and population structureLanguage and cultural evolution

The DOI matches its Crossref record; 85 of the 85 references it cites were found in a registry or an index; none of the 137 sources its claims cite is checked for support yet.

Patrilineal segmentary systems provide a peaceful explanation for the post-Neolithic Y-chromosome bottleneck

Open access
Guyon, Léa, Guez, Jérémy, Toupance, Bruno, Heyer, Evelyne, Chaix, Raphaëlle·2024·Nature Communications
DOI 10.1038/s41467-024-47618-5PMC PMC11043392
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Abstract

Studies have found a pronounced decline in male effective population sizes worldwide around 3000–5000 years ago. This bottleneck was not observed for female effective population sizes, which continued to increase over time. Until now, this remarkable genetic pattern was interpreted as the result of an ancient structuring of human populations into patrilineal groups (gathering closely related males) violently competing with each other. In this scenario, violence is responsible for the repeated extinctions of patrilineal groups, leading to a significant reduction in male effective population size. Here, we propose an alternative hypothesis by modelling a segmentary patrilineal system based on anthropological literature. We show that variance in reproductive success between patrilineal groups, combined with lineal fission (i.e., the splitting of a group into two new groups of patrilineally related individuals), can lead to a substantial reduction in the male effective population size without resorting to the violence hypothesis. Thus, a peaceful explanation involving ancient changes in social structures, linked to global changes in subsistence systems, may be sufficient to explain the reported decline in Y-chromosome diversity.

Overview

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TL;DR

The paper uses forward-time simulations to test whether patrilineal segmentary systems, without violent competition, can explain the post-Neolithic Y-chromosome bottleneck. It finds that variance in reproductive success between patrilineal groups combined with lineal fission can substantially reduce male effective population size, producing female-to-male effective population size ratios up to around 19, comparable to the ratio of 17 reported by Karmin et al.

Key findings

  • In π-based estimates, adding variance in reproductive success between patrilineal descent groups (σ² = 0.1) and lineal fission reduced male effective population size by over 20 after 100 generations (scenarios 2g and 2h), regardless of whether violence was included.
  • Coalescent-based estimates showed the same relative pattern but smaller reduction factors: scenario 2g had a male effective population size reduction factor of 2.77 and scenario 2h of 3.09, compared with 0.82 for basic patrilineal descent with random fission and no variance (scenario 2a).
  • Lineal fission plus variance in reproductive success was more efficient at reducing male effective population size than violence alone; without variance in reproductive success, lineal and random fission had little difference.
  • A Kipsigis-like polygyny scenario reduced male effective population size much less than patrilineal lineal fission with violence and/or variance, with π-based and coalescent-based reduction factors around 4.

Methods

  • The authors built a socio-demographic model in SLiM v4.1: 1,500 individuals simulated for 20,000 generations of panmixia, then divided into five villages with patrilocal residence, bilateral or patrilineal descent, exponential growth of 1% per generation, and 100 generations of the kinship rule of interest; 200 replicates were run per scenario.
  • Males carried a 1 Mb Y chromosome and females a 10 kb mtDNA; mutations were generated at 2.5 × 10⁻⁸ mutations/nucleotide/generation for the Y chromosome and 5.5 × 10⁻⁷ for mtDNA. Scenarios varied fission type (random vs. lineal), variance in reproductive success between descent groups (σ² = 0, 0.05, 0.1, 0.2), violent competition (15% of males killed per generation), male migration (0 or 2%), post-fission migration, and polygyny.
  • Male and female effective population sizes were estimated using π-based nucleotide diversity over time and coalescent-based Bayesian skyline plots generated in BEAST v1.10.5.

Limitations

  • The paper states that past rates of violence remain uncertain, pre-Neolithic residence patterns are poorly known, and the model does not formally model long-range migrations such as the Steppe migration.
  • The paper states that the exact nature of the transition from segmentary patrilineal systems to kinship systems less efficient at reducing Y-chromosome diversity requires future study, and that coalescent-based maximum female-to-male effective population size ratios are underestimates because peaks do not occur simultaneously across replicates.
  • Evident from the text: the study is a simulation modelling exercise rather than an empirical test, with parameters calibrated from ethnographic and literature-based estimates; the source of violence in the model is not specified.

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Registry

Crossref · 10.1038/s41467-024-47618-5

Cites

85 of 85 references verified0 citation errors · 0 not checkable

Statistics

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Figures

Fig. 1 Steps of the simulated scenarios 1 and 2. At t0 = 100 generations ago (after 20,000 generations of panmixia), the kinship rules of interest are introduced. In scenario 1, the population is divided into 5 villages that follow a patrilocal residence rule, with 10% of females, and either 0 or 2% of males, migrating between villages at each generation. The descent rule is bilateral. In scenario 2, the population is divided into five patrilocal villages, themselves divided into patrilineal descent groups. Mating occurs between individuals from different descent groups (exogamy) unless all remaining mates are from the same group. Patrilineal descent groups can experience fission if their size is over Nmax individuals and if the last fission event has occurred more than three generations ago. They can also go extinct if they become empty. Cycles of migration/reproduction/fission and extinction are simulated for 100 generations.
Fig. 1 Steps of the simulated scenarios 1 and 2. At t0 = 100 generations ago (after 20,000 generations of panmixia), the kinship rules of interest are introduced. In scenario 1, the population is divided into 5 villages that follow a patrilocal residence rule, with 10% of females, and either 0 or 2% of males, migrating between villages at each generation. The descent rule is bilateral. In scenario 2, the population is divided into five patrilocal villages, themselves divided into patrilineal descent groups. Mating occurs between individuals from different descent groups (exogamy) unless all remaining mates are from the same group. Patrilineal descent groups can experience fission if their size is over Nmax individuals and if the last fission event has occurred more than three generations ago. They can also go extinct if they become empty. Cycles of migration/reproduction/fission and extinction are simulated for 100 generations.CC BY · PubMed Central
Fig. 2 Change in π-based male and female effective population sizes over time. Patrilocal residence and the descent rule of interest are introduced at t0, 100 generations before present, after a phase of panmixia. Unless specified otherwise, figures presented in this paper have been plotted considering a fission threshold of Nmax = 150 (when descent is patrilineal), a σ2 parameter controlling the variance in reproductive success between descent groups of 0.1 (in scenarios with variance), a male migration rate between villages set to 0 and no post fission migration. π-based male effective population size (a), female effective population size (b), and female-to-male effective population size ratio (c) averaged over 200 replicates are shown every 20 generations with 95% confidence interval. In all figures of this paper, the points were staggered along the x-axis to distinguish between scenarios. Values of means and their 95% confidence intervals are provided in the Source Data file.
Fig. 2 Change in π-based male and female effective population sizes over time. Patrilocal residence and the descent rule of interest are introduced at t0, 100 generations before present, after a phase of panmixia. Unless specified otherwise, figures presented in this paper have been plotted considering a fission threshold of Nmax = 150 (when descent is patrilineal), a σ2 parameter controlling the variance in reproductive success between descent groups of 0.1 (in scenarios with variance), a male migration rate between villages set to 0 and no post fission migration. π-based male effective population size (a), female effective population size (b), and female-to-male effective population size ratio (c) averaged over 200 replicates are shown every 20 generations with 95% confidence interval. In all figures of this paper, the points were staggered along the x-axis to distinguish between scenarios. Values of means and their 95% confidence intervals are provided in the Source Data file.CC BY · PubMed Central
Fig. 3 Effect of variance in reproductive success between descent groups (σ2) on the change in π-based male and female effective population sizes. Patrilocal residence and patrilineal descent (with settings of scenario 2g, i.e. lineal fission, variance in reproductive success between descent groups and no violence) are introduced at t0, 100 generations before present, after a phase of panmixia. See the legend of Fig. 2 for parameter values (except for the parameter controlling the variance in reproductive success between descent groups, which varies between 0 and 0.2). π-based male effective population size (a), female effective population size (b), and female-to-male effective population size ratio (c) averaged over 200 replicates are shown every 20 generations with 95% confidence interval. Values of means and their 95% confidence intervals are provided in the Source Data file.
Fig. 3 Effect of variance in reproductive success between descent groups (σ2) on the change in π-based male and female effective population sizes. Patrilocal residence and patrilineal descent (with settings of scenario 2g, i.e. lineal fission, variance in reproductive success between descent groups and no violence) are introduced at t0, 100 generations before present, after a phase of panmixia. See the legend of Fig. 2 for parameter values (except for the parameter controlling the variance in reproductive success between descent groups, which varies between 0 and 0.2). π-based male effective population size (a), female effective population size (b), and female-to-male effective population size ratio (c) averaged over 200 replicates are shown every 20 generations with 95% confidence interval. Values of means and their 95% confidence intervals are provided in the Source Data file.CC BY · PubMed Central
Fig. 4 Change in π-based male and female effective population sizes over time under the two transitions scenario. Between t0 and t1, the descent rule is bilateral, and the residence rule is either patrilocal, matrilocal, or multilocal. Then, at t1, there is a transition to patrilineal descent with patrilocal residence (with the settings of scenario 2g, i.e. lineal fission, variance in reproductive success between groups, no violence, and with the parameter values given in the legend of Fig. 2). π-based male effective population size (a), female effective population size (b) and female-to-male effective population size ratios (c) averaged over 200 replicates are shown every 20 generations with the 95% confidence interval. Values of means and their 95% confidence intervals are provided in the Source Data file.
Fig. 4 Change in π-based male and female effective population sizes over time under the two transitions scenario. Between t0 and t1, the descent rule is bilateral, and the residence rule is either patrilocal, matrilocal, or multilocal. Then, at t1, there is a transition to patrilineal descent with patrilocal residence (with the settings of scenario 2g, i.e. lineal fission, variance in reproductive success between groups, no violence, and with the parameter values given in the legend of Fig. 2). π-based male effective population size (a), female effective population size (b) and female-to-male effective population size ratios (c) averaged over 200 replicates are shown every 20 generations with the 95% confidence interval. Values of means and their 95% confidence intervals are provided in the Source Data file.CC BY · PubMed Central
Fig. 5 Change in coalescent-based estimation of male and female effective population sizes over time under different scenarios. Patrilocal residence and the descent rule of interest are introduced at t0, 100 generations before present, after a phase of panmixia. See the legend of Fig. 2 for parameter values. Average Bayesian skyline plots of male effective population size (a), female effective population size (b), and female-to-male Ne ratio (c) over 200 replicates are plotted for each scenario. The dashed grey line corresponds to the ratio of 17 obtained by Karmin et al.1. Values of means are provided in the Source Data file.
Fig. 5 Change in coalescent-based estimation of male and female effective population sizes over time under different scenarios. Patrilocal residence and the descent rule of interest are introduced at t0, 100 generations before present, after a phase of panmixia. See the legend of Fig. 2 for parameter values. Average Bayesian skyline plots of male effective population size (a), female effective population size (b), and female-to-male Ne ratio (c) over 200 replicates are plotted for each scenario. The dashed grey line corresponds to the ratio of 17 obtained by Karmin et al.1. Values of means are provided in the Source Data file.CC BY · PubMed Central
Fig. 6 Change in coalescent-based estimation of male and female effective population sizes over time under the two transition scenarios. Between t0 and t1, the descent rule is bilateral, and the residence rule is either patrilocal, matrilocal, or multilocal. Then, at t1, there is a transition to patrilineal descent with patrilocal residence (with the settings of scenario 2g, i.e. lineal fission, variance in reproductive success between groups, no violence, and with the parameter values given in the legend of Fig. 2). Average Bayesian skyline plots of male effective population size (a), female effective population size (b), and female-to-male Ne ratio (c) over 200 replicates are plotted for each scenario. The dashed grey line corresponds to the ratio of 17 obtained by Karmin et al.1. Values of means are provided in the Source Data file.
Fig. 6 Change in coalescent-based estimation of male and female effective population sizes over time under the two transition scenarios. Between t0 and t1, the descent rule is bilateral, and the residence rule is either patrilocal, matrilocal, or multilocal. Then, at t1, there is a transition to patrilineal descent with patrilocal residence (with the settings of scenario 2g, i.e. lineal fission, variance in reproductive success between groups, no violence, and with the parameter values given in the legend of Fig. 2). Average Bayesian skyline plots of male effective population size (a), female effective population size (b), and female-to-male Ne ratio (c) over 200 replicates are plotted for each scenario. The dashed grey line corresponds to the ratio of 17 obtained by Karmin et al.1. Values of means are provided in the Source Data file.CC BY · PubMed Central

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Citations

Cites

Research works printed but not linked: 12

  1. Bandelt, H.-J., Macaulay, V. & Richards, M. B. What molecules can’t tell us about the spread of languages and the neolithic. In Bellwood, P. & Renfrew, C. (eds.) Examining the Farming/Language Dispersal Hypothesis, McDonald Institute Monographs (Cambridge University Press, Cambridge, UK, 2002).
  2. Fox, R. Kinship and Marriage: An Anthropological Perspective. A Pelican Original (Cambridge University Press, Cambridge, 1967).
  3. Pinker, S. The Better Angels of Our Nature: The Decline of Violence in History and Its Causes (Penguin UK, London, 2011).
  4. Fontijn, D. Giving Up Weapons. 145–154 (Oxford: Archaeopress, Oxford, 2005).
  5. Aberle, D. F. Matrilineal Descent in Cross-cultural Perspective, 655–727 (University of California Press, Berkeley, 1961).
  6. Murdock, G. P. Social Structure. (Macmillan, Oxford, England, 1949).
  7. Forde, C. D. Fission and accretion in the patrilineal clans of a semi-bantu community in southern Nigeria. J. R. Anthropol. Inst. G.B. Irel. 68, 311–338 (1938).
  8. Pasternak, B. Descent and social complexity. In Introduction to Kinship and Social Organization, 111–123 (Prentice Hall, New Jersey, 1976).
  9. Goody, J. The European Family (Wiley, 2000).
  10. Oboler, R. S. Nandi. In Ember, C. R. & Ember, M. (eds.) Encyclopedia of Sex and Gender: Men and Women in the World’s Cultures Volume I: Topics and Cultures A-K Volume II: Cultures L-Z, 716–724 (Springer Boston, MA, USA, 2004).
  11. Tange, O. Gnu parallel - the command-line power tool. USENIX Mag. 36, 42–47 (2011).
  12. Davison, A. C. & Hinkley, D. V. Bootstrap Methods and their Application. Cambridge Series in Statistical and Probabilistic Mathematics (Cambridge University Press, Cambridge, 1997).

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Metadata

Authors
Guyon, L., Guez, J., Toupance, B., Heyer, E., & Chaix, R.
Affiliations
Centre National de la Recherche Scientifique (FR)
Corresponding author
  • Guyon, Léa
  • Chaix, Raphaëlle
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2024-04-24
Volume
15
Issue
1
Pages
3243-3243
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-024-47618-5
PMC
PMC11043392
OpenAlex
W4395081706
Cited by
28
References
85
Citations by year
2026: 14 · 2025: 11 · 2024: 3
FWCI
5.63
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
The PhD funding is a CDSN granted by the Ecole Normale Supérieure and delivered by the MNHN (Museum National d'Histoire Naturelle).
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Forensic and Genetic Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
  • Social Sciences › Cultural Studies › Language and cultural evolution
Keywords
social structure change, subsistence change, Y-chromosome diversity
MeSH terms
Female, Genetics, Population, Humans, Male, Population Density, Genetic Variation, Violence, Chromosomes, Human, Y, History, Ancient

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