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

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Zeng, Tian Chen ^a   Aw, Alan J ^a   Feldman, Marcus W ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHROPOLOGY; CHROMOSOME; CULTURAL CHANGE; GENETIC VARIATION; GENOMICS; HUMAN EVOLUTION; INTERSPECIFIC COMPETITION; NUMERICAL MODEL; POPULATION BOTTLENECK; PREHISTORIC; SOCIAL CHANGE;

ARTICLE; COMPETITION; CONCEPTION; HUMAN; HUMAN EXPERIMENT; NEOLITHIC; SOCIAL EVOLUTION; THEORETICAL STUDY; Y CHROMOSOME; AFRICA; ASIA; BIOLOGICAL MODEL; COMPUTER SIMULATION; CULTURAL FACTOR; EUROPE; GENETIC VARIATION; GENETICS; HAPLOTYPE; MALE; POPULATION DYNAMICS; SOCIAL HIERARCHY;

AFRICA; ASIA; EURASIA; EUROPE;

MITOCHONDRIAL DNA;

AFRICA; ASIA; CHROMOSOMES, HUMAN, Y; COMPUTER SIMULATION; CULTURAL CHARACTERISTICS; DNA, MITOCHONDRIAL; EUROPE; GENETIC VARIATION; HAPLOTYPES; HIERARCHY, SOCIAL; HUMANS; MALE; MODELS, GENETIC; POPULATION DYNAMICS;

EID: 85047618323     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-018-04375-6     Document Type: Article

References (78)

1. Premo, L. S. & Hublin, J.-J. Culture, population structure, and low genetic diversity in Pleistocene hominins. Proc. Natl. Acad. Sci. USA 106, 33-37 (2009).
2. Premo, L. S. Hitchhiker's guide to genetic diversity in socially structured populations. Curr. Zool. 58, 287-297 (2012).
3. Durham, W. H. (ed.) In Coevolution: Genes, Culture, and Human Diversity, 286-361 (Stanford University Press, Palo Alto, CA, 1991).
4. Karmin, M. et al. A recent bottleneck of Y chromosome diversity coincides with a global change in culture. Genome Res. 25, 459-466 (2015).
5. Batini, C. et al. Large-scale recent expansion of European patrilineages shown by population resequencing. Nat. Commun. 6, 7152 (2015).
6. Poznik, G. D. et al. Punctuated bursts in human male demography inferred from 1,244 worldwide Y-chromosome sequences. Nat. Genet. 48, 593-599 (2016).
7. Drevenstedt, G.L., Crimmins, E. M., Vasunilashorn, S. & Finch, C. E. The rise and fall of excess male infant mortality. Proc. Natl. Acad. Sci. USA 105, 5016-5021 (2008).
8. Helle, S., Helama, S. & Lertola, K. Evolutionary ecology of human birth sex ratio under the compound influence of climate change, famine, economic crises and wars. J. Anim. Ecol. 78, 1226-1233 (2009).
9. Chikhi, L., Destro-Bisol, G., Bertorelle, G., Pascali, V. & Barbujani, G. Clines of nuclear DNA markers suggest a largely Neolithic ancestry of the European gene pool. Proc. Natl. Acad. Sci. USA 95, 9053-9058 (1998).
10. Barbujani, G., Pilastro, A., De Domenico, S. & Renfrew, C. Genetic variation in North Africa and Eurasia: neolithic demic diffusion vs. paleolithic colonisation. Am. J. Phys. Anthropol. 95, 137-154 (1994).
11. Hofmanová, Z. et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl. Acad. Sci. USA 113, 6886-6891 (2016).
12. Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409 (2014).
13. Diamond, J. & Bellwood, P. Farmers and their languages: The first expansions. Science 300, 597-603 (2003).
14. Forster, P. & Renfrew, C. Mother tongue and Y chromosomes. Science 333, 1390-1391 (2011).
15. Bellwood, P. S. & Renfrew, C. Examining the Farming/Language Dispersal Hypothesis (McDonald Institute for Archaeological Research, Cambridge, 2002).
16. Llorente, M. G. et al. The genetics of an early Neolithic pastoralist from the Zagros, Iran. Sci. Rep. 6, 31326 (2016).
17. Broushaki, F. et al. Early Neolithic genomes from the eastern Fertile Crescent. Science 353, 499-503 (2016).
18. Bar-Yosef, O. The Natufian culture in the Levant, threshold to the origins of agriculture. Evolut. Anthropol. 6, 159-177 (1998).
19. Flannery, K. V., Ucko, P. J. & Dimbleby, G. W. in The Domestication and Exploitation of Plants and Animals (eds Ucko, P. J. & Dimbleby, G. W.) 73-100 (Gerald Duckworth & Co., London, 1969).
20. Cohen, M. N. The Food Crisis in Prehistory: Overpopulation and the Origins of Agriculture (Yale University Press, New Haven, CT, 1977).
21. Bocquet-Appel, J.-P. The Neolithic demographic transition, population pressure and cultural change. Comp. Civiliz. Rev. 58, 6 (2008).
22. Haak, W. et al. Ancient DNA from European early Neolithic farmers reveals their Near Eastern affinities. PLoS Biol. 8, e1000536 (2010).
23. Fernández, E. et al. Ancient DNA analysis of 8000 BC Near Eastern farmers supports an early Neolithic pioneer maritime colonization of mainland Europe through Cyprus and the Aegean islands. PLoS Genet. 10, e1004401 (2014).
24. Fu, Q., Rudan, P., Pääbo, S. & Krause, J. Complete mitochondrial genomes reveal Neolithic expansion into Europe. PLoS ONE 7, e32473 (2012).
25. Siska, V. et al. Genome-wide data from two early Neolithic East Asian individuals dating to 7700 years ago. Sci. Adv. 3, e1601877 (2017).
26. Llorente, M. G. et al. Ancient Ethiopian genome reveals extensive Eurasian admixture in Eastern Africa. Science 350, 820-822 (2015).
27. Schlebusch, C. M. et al. Ancient genomes from southern Africa pushes modern human divergence beyond 260,000 years ago. Preprint at https://www.biorxiv.org/content/early/2017/06/05/145409 (2017).
28. Mulder, M. B. et al. Intergenerational wealth transmission and the dynamics of inequality in small-scale societies. Science 326, 682-688 (2009).
29. Smith, E. A. Status effects on men's reproductive success. Proc. Natl. Acad. Sci. USA 113, 10739-10741 (2016).
30. Nettle, D. & Pollet, T. V. Natural selection on male wealth in humans. Am. Nat. 172, 658-666 (2008).
31. Betzig, L. Means, variances, and ranges in reproductive success: comparative evidence. Evol. Human. Behav. 33, 309-317 (2012).
32. Heyer, E. et al. Patrilineal populations show more male transmission of reproductive success than cognatic populations in Central Asia, which reduces their genetic diversity. Am. J. Phys. Anthropol. 157, 537-543 (2015).
33. Caballero, A. On the effective size of populations with separate sexes, with particular reference to sex-linked genes. Genetics 139, 1007-1011 (1995).
34. Nagylaki, T. The inbreeding effective population number in dioecious populations. Genetics 139, 473-485 (1995).
35. von Rueden, C. R. & Jaeggi, A. V. Men's status and reproductive success in 33 nonindustrial societies: effects of subsistence, marriage system, and reproductive strategy. Proc. Natl. Acad. Sci. USA 113, 10824-10829 (2016).
36. Marlowe, F. W. The mating system of foragers in the standard cross-cultural sample. Cross-Cult. Res. 37, 282-306 (2003).
37. Boehm, C. et al. Egalitarian behavior and reverse dominance hierarchy [and comments and reply]. Curr. Anthropol. 34, 227-254 (1993).
38. Turchin, P., Currie, T. E., Turner, E. A. L. & Gavrilets, S. War, space, and the evolution of old world complex societies. Proc. Natl. Acad. Sci. USA 110, 16384-16389 (2013).
39. Clark, G. A Farewell to Alms: A Brief Economic History of the World (Princeton University Press, Princeton, NJ, 2008).
40. Fortes, M. The structure of unilineal descent groups. Am. Anthropol. 55, 17-41 (1953).
41. Oota, H., Settheetham-Ishida, W., Tiwawech, D., Ishida, T. & Stoneking, M. Human mtDNA and Y-chromosome variation is correlated with matrilocal versus patrilocal residence. Nat. Genet. 29, 20 (2001).
42. Ségurel, L. et al. Sex-specific genetic structure and social organization in Central Asia: insights from a multi-locus study. PLoS Genet. 4, e1000200 (2008).
43. Choi, J.-K. & Bowles, S. The coevolution of parochial altruism and war. Science 318, 636-640 (2007).
44. Richerson, P. J. & Christiansen, M. H. Cultural Evolution: Society, Technology, Language, and Religion (MIT Press, Cambridge, MA, 2013).
45. Palmstierna, M., Frangou, A., Wallette, A. & Dunbar, R. Family counts: deciding when to murder among the Icelandic Vikings. Evol. Human. Behav. 38, 175-180 (2017).
46. Chagnon, N. A. Life histories, blood revenge, and warfare in a tribal population. Science 239, 985 (1988).
47. Korotayev, A. V. Unilineal descent organization and deep Christianization: A cross-cultural comparison. Cross-Cult. Res. 37, 133-157 (2003).
48. Ember, C. R., Ember, M. & Pasternak, B. On the development of unilineal descent. J. Anthropol. Res. 30, 69-94 (1974).
49. Kelly, R. C. Warless Societies and the Origin of War (University of Michigan Press, Ann Arbor, MI, 2000).
50. Johnson, A. W. & Earle, T. K. The Evolution of Human Societies: From Foraging Group to Agrarian Sate (Stanford University Press, Palo Alto, CA, 2000).
51. Otterbein, K. F. & Otterbein, C. S. An eye for an eye, a tooth for a tooth: A cross-cultural study of feuding. Am. Anthropol. 67, 1470-1482 (1965).
52. Otterbein, K. F. Internal war: A cross-cultural study. Am. Anthropol. 70, 277-289 (1968).
53. Blumberg, R. L. & Winch, R. F. Societal complexity and familial complexity: evidence for the curvilinear hypothesis. Am. J. Sociol. 77, 898-920 (1972).
54. Sahlins, M. D. The segmentary lineage: An organization of predatory expansion. Am. Anthropol. 63, 322-345 (1961).
55. Ferguson, R. B. The Encyclopedia of War (John Wiley & Sons, Hoboken, NJ, 2012).
56. Yoffee, N. Myths of the Archaic State: Evolution of the Earliest Cities, States, and Civilizations (Cambridge University Press, Cambridge, 2005).
57. Kottak, C. P. The process of state formation in Madagascar. Am. Ethnol. 4, 136-155 (1977).
58. Kirch, P. V. The Evolution of the Polynesian Chiefdoms (Cambridge University Press, Cambridge, 1989).
59. Unterländer, M. et al. Ancestry and demography and descendants of Iron Age nomads of the Eurasian steppe. Nat. Commun. 8, 14615 (2017).
60. Balaresque, P. et al. Y-chromosome descent clusters and male differential reproductive success: young lineage expansions dominate Asian pastoral nomadic populations. Eur. J. Hum. Genet. 23, 1413 (2015).
61. Whitehead, H. Cultural selection and genetic diversity in matrilineal whales. Science 282, 1708-1711 (1998).
62. Whitehead, H., Vachon, F. & Frasier, T. R. Cultural hitchhiking in the matrilineal whales. Behav. Genet. 47, 324-334 (2017).
63. Mathieson, I. et al. The genomic history of southeastern Europe. Nature 555, 197-203 (2018).
64. Olalde, I. et al. The Beaker phenomenon and the genomic transformation of northwest Europe. Nature 555, 190-196 (2018).
65. Kristiansen, K. Prehistoric migrations: The case of the single grave and corded ware cultures. J. Dan. Archaeol. 8, 211-225 (1989).
66. Lindholm, C. Kinship structure and political authority: The Middle East and Central Asia. Comp. Stud. Soc. Hist. 28, 334-355 (1986).
67. Kivisild, T. The study of human Y chromosome variation through ancient DNA. Hum. Genet. 136, 529-546 (2017).
68. McEvoy, B. & Bradley, D. G. Y-chromosomes and the extent of patrilineal ancestry in Irish surnames. Hum. Genet. 119, 212-219 (2006).
69. Moore, L. T., McEvoy, B., Cape, E., Simms, K. & Bradley, D. G. A Y-chromosome signature of hegemony in Gaelic Ireland. Am. J. Human. Genet. 78, 334-338 (2006).
70. King, T. E., Ballereau, S. J., Schürer, K. E. & Jobling, M. A. Genetic signatures of coancestry within surnames. Curr. Biol. 16, 384-388 (2006).
71. King, T. E. & Jobling, M. A. Founders, drift, and infidelity: The relationship between Y-chromosome diversity and patrilineal surnames. Mol. Biol. Evol. 26, 1093-1102 (2009).
72. Kristiansen, K. in The World System and the Earth System: Global Socioenvironmental Change and Sustainability Since the Neolithic (ed. Hornborg, A.) 149-162 (Left Coast Press, Walnut Creek, CA, 2007).
73. Earle, T. The evolution of chiefdoms. Curr. Anthropol. 30, 84-88 (1989).
74. Fukuyama, F. The Origins of Political Order: From Prehuman Times to the French Revolution (Farrar, Straus and Giroux, New York, NY, 2011).
75. Hofbauer, J. & Sigmund, K. Evolutionary Games and Population Dynamics (Cambridge University Press, Cambridge, 1998).
76. Turchin, P. & Gavrilets, S. Evolution of complex hierarchical societies. Social. Evol. Hist. 8, 167-198 (2009).
77. Maruyama, T. & Kimura, M. Genetic variability and effective population size when local extinction and recolonization of subpopulations are frequent. Proc. Natl. Acad. Sci. USA 77, 6710-6714 (1980).
78. Batini, C. & Jobling, M. A. Detecting past male-mediated expansions using the Y chromosome. Hum. Genet. 136, 547-557 (2017).