Journal of Molecular Evolution

, Volume 57, Issue 1, pp 85–97 | Cite as

A Recent Shift from Polygyny to Monogamy in Humans Is Suggested by the Analysis of Worldwide Y-Chromosome Diversity

  • Isabelle Dupanloup
  • Luísa Pereira
  • Giorgio Bertorelle
  • Francesc Calafell
  • Maria João Prata
  • Antonio Amorim
  • Guido Barbujani
Article

Abstract

Molecular genetic data contain information on the history of populations. Evidence of prehistoric demographic expansions has been detected in the mitochondrial diversity of most human populations and in a Y-chromosome STR analysis, but not in a previous study of 11 Y-chromosome SNPs in Europeans. In this paper, we show that mismatch distributions and tests of mutation/drift equilibrium based on up to 166 Y-chromosome SNPs, in 46 samples from all continents, also fail to support an increase of the male effective population size. Computer simulations show that the low nuclear versus mitochondrial mutation rates cannot explain these results. However, ascertainment bias, i.e., when only highly variable SNP sites are typed, may be concealing any Y SNPs evidence for a recent, but not an ancient, increase in male effective population sizes. The results of our SNP analyses can be reconciled with the expansion of male effective population sizes inferred from STR loci, and with mitochondrial evidence, by admitting that humans were essentially polygynous during much of their history. As a consequence, until recently only a few men may have contributed a large fraction of the Y-chromosome pool at every generation. The number of breeding males may have increased, and the variance of their reproductive success may have decreased, through a recent shift from polygyny to monogamy, which is supported by ethnological data and possibly accompanied the shift from mobile to sedentary communities.

Keywords

Human populations Y chromosome Single-nucleotide polymorphisms Mismatch distributions Demographic expansions Polygyny 

References

  1. 1.
    Alonso, S, Armour, JA 2001A highly variable segment of human subterminal 16p reveals a history of population growth for modern humans outside Africa.Proc Natl Acad Sci USA98864869CrossRefPubMedGoogle Scholar
  2. 2.
    Badcock, C 1991Evolution and individual behavior: An introduction to human sociobiology.BlackwellOxfordGoogle Scholar
  3. 3.
    Bandelt, HJ, Forster, P 1997The myth of bumpy hunter-gatherer mismatch distributions.Am J Hum Genet61980983PubMedGoogle Scholar
  4. 4.
    Beaumont, MA 1999Detecting population expansion and decline using microsatellites.Genetics15320132019PubMedGoogle Scholar
  5. 5.
    Bellwood, P 2001Early agricultural diasporas?Annu Rev Anthropol30181207CrossRefGoogle Scholar
  6. 6.
    Bertorelle, G, Slatkin, M 1995The number of segregating sites in expanding human populations, with implications for estimates of demographic parameters.Mol Biol Evol12887892PubMedGoogle Scholar
  7. 7.
    Bertranpetit, J 2000Genome, diversity, and origins: The Y chromosome as a storyteller.Proc Natl Acad Sci USA9769276929CrossRefPubMedGoogle Scholar
  8. 8.
    Biraben, JN 1979Essai sur l'évolution du nombre des hommes.Population341325Google Scholar
  9. 9.
    Bonatto, SL, Salzano, FM 1997A single and early migration for the peopling of the Americas supported by mitochondrial DNA sequence data.Proc Natl Acad Sci USA9418661871PubMedGoogle Scholar
  10. 10.
    Brakez, Z, Bosch, E, Izaabel, H, Akhayat, O, Comas, D, Bertranpetit, J, Calafell, F 2001Human mitochondrial DNA sequence variation in the Moroccan population of the Souss area.Ann Hum Biol28295307CrossRefPubMedGoogle Scholar
  11. 11.
    Cavalli-Sforza, LL 1998The DNA revolution in population genetics.Trends Genet146065PubMedGoogle Scholar
  12. 12.
    Cavalli-Sforza, LL, Menozzi, P, Piazza, A 1994The history and geography of human genes.Princeton University PressPrinceton, NJGoogle Scholar
  13. 13.
    Cohen, MN 1989Health and the rise of civilization.Yale University PressNew Haven, CTGoogle Scholar
  14. 14.
    Crow, JF 1958Some possibilities for measuring selection intensities in man.Hum Biol30113PubMedGoogle Scholar
  15. 15.
    De Knijff, P 2000Messages through bottlenecks: On the combined use of slow and fast evolving polymorphic markers on the human Y chromosome.Am J Hum Genet6710551061PubMedGoogle Scholar
  16. 16.
    Donnelly, P 1996

    Interpreting genetic variability: The effects of shared evolutionary history.

    Weiss, K eds. Variation in the human genome.WileyChichester, UK2550
    Google Scholar
  17. 17.
    Donnelly, P, Tavaré, S, Balding, DJ, Griffiths, RC 1996Estimating the age of the common ancestor of men from the ZFY intron.Science27213571359PubMedGoogle Scholar
  18. 18.
    Excoffier, L 1990Evolution of human mitochondrial DNA: Evidence for departure from a pure neutral model of populations at equilibrium.J Mol Evol30125139PubMedGoogle Scholar
  19. 19.
    Excoffier, L, Schneider, S 1999Why hunter-gatherer populations do not show signs of Pleistocene demographic expansions.Proc Natl Acad Sci USA961059710602CrossRefPubMedGoogle Scholar
  20. 20.
    Excoffier, L, Novembre, J, Schneider, S 2000SIMCOAL: A general coalescent program for the simulation of molecular data in interconnected populations with arbitrary demography.J Hered91506509CrossRefPubMedGoogle Scholar
  21. 21.
    Flannery, K 1972a

    The origins of the village as a settlement type in Mesoamerica and the Near East.

    Uckho, PTringham, RDimbleby, GW eds. Man, settlement, and urbanism.SchenkmanCambridge, MA2353
    Google Scholar
  22. 22.
    Flannery, K 1972bThe cultural evolution of civilizations.Annu Rev Ecol Syst3399426Google Scholar
  23. 23.
    Fu, YX 1997Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection.Genetics147915925PubMedGoogle Scholar
  24. 24.
    Hammer, MF 1995A recent common ancestry for human Y chromosomes.Nature378376378Google Scholar
  25. 25.
    Harding, RM, Fullerton, SM, Griffiths, RC, Bond, J, Cox, MJ, Schneider, JA, Moulin, DS, Clegg, JB 1997Archaic African and Asian lineages in the genetic ancestry of modern humans.Am J Hum Genet60772789PubMedGoogle Scholar
  26. 26.
    Harpending, HC 1994Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution.Hum Biol66591600PubMedGoogle Scholar
  27. 27.
    Harpending, HC, Batzer, MA, Gurven, M, Jorde, JB, Rogers, AR, Sherry, ST 1998Genetic traces of ancient demography.Proc Natl Acad Sci USA9519611967PubMedGoogle Scholar
  28. 28.
    Harris, EE, Hey, J 1999aX chromosome evidence for ancient human histories.Proc Natl Acad Sci USA9633203324Google Scholar
  29. 29.
    Harris, EE, Hey, J 1999bHuman demography in the Pleistocene: Do mitochondrial and nuclear genes tell the same story?Evol Anthropol88186Google Scholar
  30. 30.
    Hudson, RR 1990

    Gene genealogies and the coalescent process.

    Futuyma, DAntonovics, J eds. Oxford surveys in evolutionary biology.Oxford University PressOxford144
    Google Scholar
  31. 31.
    James, WH 1987The human sex ratio, part 1: A review of the literature.Hum Biol59721752PubMedGoogle Scholar
  32. 32.
    Jazin, E, Soodyall, H, Jalonen, P, Lindholm, E, Stoneking, M, Gyllensten, U 1998Mitochondrial mutation rate revisited: Hot spots and polymorphism.Nat Genet18109110PubMedGoogle Scholar
  33. 33.
    Jobling, MA, Tyler-Smith, C 2000New uses for new haplotypes. The human Y chromosome, disease and selection.Trends Genet16356362CrossRefPubMedGoogle Scholar
  34. 34.
    Jobling, MA, Pandya, A, Tyler-Smith, C 1997The Y chromosome in forensic analysis and paternity testing.Int J Legal Med110118124PubMedGoogle Scholar
  35. 35.
    Keen, I 1982How some Murngin men marry ten wives.Man17620642Google Scholar
  36. 36.
    Lee, RB, DeVore, I 1968Man the hunter.AldineChicagoGoogle Scholar
  37. 37.
    Marjoram, P, Donnelly, P 1994Pairwise comparisons of mitochondrial DNA sequences in subdivided populations and implications for early human evolution.Genetics136673683PubMedGoogle Scholar
  38. 38.
    Nei, M 1987Molecular evolutionary genetics.Columbia University PressNew YorkGoogle Scholar
  39. 39.
    Nielsen, R 2000Estimation of population parameters and recombination rates from single nucleotide polymorphisms.Genetics154931942PubMedGoogle Scholar
  40. 40.
    Pereira, L, Dupanloup, I, Rosser, Z, Jobling, MA, Barbujani, G 2001Y-chromosome mismatch distributions in Europe.Mol Biol Evol1812591271PubMedGoogle Scholar
  41. 41.
    Pritchard, JK, Seielstad, MT, Perez-Lezaun, A, Feldman, MW 1999Population growth of human Y chromosomes: A study of Y chromosome microsatellites.Mol Biol Evol1617911798PubMedGoogle Scholar
  42. 42.
    Pussey, AE 2001

    Of genes and apes: Chimpanzee social organization and reproduction.

    de Waal, FBM eds. Tree of origin: What primate behavior can tell us about human social evolution.Harvard University PressCambridge, MA937
    Google Scholar
  43. 43.
    Reich, DE, Goldstein, DB 1998Genetic evidence for a Paleolithic human population expansion in Africa.Proc Natl Acad Sci USA9581198123PubMedGoogle Scholar
  44. 44.
    Rogers, AR, Harpending, H 1992Population growth makes waves in the distribution of pairwise genetic differences.Mol Biol Evol9552569PubMedGoogle Scholar
  45. 45.
    Rogers, AR, Jorde, LB 1995Genetic evidence on modern human origins.Hum Biol67136PubMedGoogle Scholar
  46. 46.
    Rogers, AR, Fraley, AE, Bamshad, MJ, Watkins, WS, Jorde, LB 1996Mitochondrial mismatch analysis is insensitive to the mutational process.Mol Biol Evol13895902PubMedGoogle Scholar
  47. 47.
    Ruiz-Linares, A, Ortiz-Barrientos, D, Figueroa, M,  et al. 1999Microsatellites provide evidence for Y-chromosome diversity among the founders of the New World.Proc Natl Acad Sci USA9663126317CrossRefPubMedGoogle Scholar
  48. 48.
    Schneider, S, Excoffier, L 1999Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: Application to human mitochondrial DNA.Genetics15210791089Google Scholar
  49. 49.
    Schneider, S, Roessli, D, Excoffier, L 2000Arlequin ver. 2.000: A software for population genetics data analysis.Genetics and Biometry Laboratory, University of GenevaGeneva, SwitzerlandGoogle Scholar
  50. 50.
    Seielstad, M, Minch, E, Cavalli-Sforza, LL 1998Genetic evidence for a higher female migration rate in humans.Nat Genet20278280CrossRefPubMedGoogle Scholar
  51. 51.
    Semino, O, Passarino, G, Oefner, PJ, Lin, AA, Arbuzova, S, Beckman, LE, De Benedictis, G,  et al. 2000The genetic legacy of Paleolithic Homo sapiens in extant Europeans: A Y chromosome perspective.Science29011551159PubMedGoogle Scholar
  52. 52.
    Shen, P, Wang, F, Underbill, PA, Franco, C, Yang, WH, Roxas, A, Sung, R,  et al. 2000Population genetic implications from sequence variation in four Y chromosome genes.Proc Natl Acad Sci USA9773547359CrossRefPubMedGoogle Scholar
  53. 53.
    Sigurgardottir, S, Helgason, A, Gulcher, JR, Stefansson, K, Donnelly, P 2000The mutation rate in the human mtDNA control region.Am J Hum Genet6615991609CrossRefPubMedGoogle Scholar
  54. 54.
    Simonsen, KL, Churchill, GA, Aquadro, CF 1995Properties of statistical tests of neutrality for DNA polymorphism data.Genetics141413429PubMedGoogle Scholar
  55. 55.
    Sokal, RR, Rohlf, FJ 1995Biometry.W.H. FreemanNew YorkGoogle Scholar
  56. 56.
    Soodyall, H, Jenkins, T, Mukherjee, A, du Toit, E, Roberts, DF, Stoneking, M 1997The founding mitochondrial DNA lineages of Tristan da Cunha Islanders.Am J Phys Anthropol104157166CrossRefPubMedGoogle Scholar
  57. 57.
    Tajima, F 1989aStatistical method for testing the neutral mutation hypothesis by DNA polymorphisms.Genetics123585595Google Scholar
  58. 58.
    Tajima, F 1989bThe effect of change in population size on DNA polymorphism.Genetics123597601Google Scholar
  59. 59.
    Takahata, N 1996Neutral theory of molecular evolution.Curr Opin Genet Devel6767772CrossRefGoogle Scholar
  60. 60.
    Takahata, N, Satta, Y, Klein, J 1995Divergence time and population size in the lineage leading to modern humans.Theor Pop Biol48198221CrossRefGoogle Scholar
  61. 61.
    Thomson, R, Pritchard, JK, Shen, P, Oefner, PJ, Feldman, MW 2000Recent common ancestry of human Y chromosomes: Evidence from DNA sequence data.Proc Natl Acad Sci USA9773607365CrossRefPubMedGoogle Scholar
  62. 62.
    Underhill, PA, Jin, L, Lin, AA,  et al. 1997Detection of numerous Y chromosome biallelic polymorphisms by denaturing high-performance liquid chromatography.Genome Res79961005PubMedGoogle Scholar
  63. 63.
    Underhill, PA, Shen, P, Lin, AA,  et al. 2000Y chromosome sequence variation and the history of human populations.Nat Genet26358361CrossRefPubMedGoogle Scholar
  64. 64.
    van den Berghe, P 1979Human family systems. An evolutionary view.Waveland PressProspect Heights, ILGoogle Scholar
  65. 65.
    von Haeseler, A, Sajantila, A, Pääbo, S 1996The genetical archaeology of the human genome.Nat Genet14135140PubMedGoogle Scholar
  66. 66.
    Wakeley, J, Nielsen, R, Liu-Cordero, SN, Ardlie, K 2001The discovery of single-nucleotide-polymorphisms—and inferences about the human demographic history.Am J Hum Genet6913321347CrossRefPubMedGoogle Scholar
  67. 67.
    Wall, JD, Przeworski, M 2000When did the human population start increasing?Genetics15518651874PubMedGoogle Scholar
  68. 68.
    Weiss, KM 1984On the number of members of the genus Homo who have ever lived, and some evolutionary implications.Hum Biol56637649PubMedGoogle Scholar
  69. 69.
    Zhao, Z, Jin, L, Fu, YX,  et al. 2000Worldwide DNA sequence variation in a 10-kilobase noncoding region of human chromosome 22.Proc Natl Acad Sci USA971135411358CrossRefPubMedGoogle Scholar
  70. 70.
    Zietkiewicz, E, Yotova, V, Jarnik, M,  et al. 1998Genetic structure of the ancestral population of modem humans.J Mol Evol47146155PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 2003

Authors and Affiliations

  • Isabelle Dupanloup
    • 1
  • Luísa Pereira
    • 2
  • Giorgio Bertorelle
    • 1
  • Francesc Calafell
    • 3
  • Maria João Prata
    • 2
  • Antonio Amorim
    • 2
  • Guido Barbujani
    • 1
  1. 1.Dipartimento di BiologiaUniversità di Ferrara, via L. Borsari 46, I-44100 FerraraItaly
  2. 2.Instituto de Patologia e Imunologia Molecular da Universidade do Porto (IPATIMUP), R. Dr. Roberto Frias, s/n, 4200 Porto, and Faculdade de Ciências da Universidade do Porto, Praça Gomes Teixeira, 4050 PortoPortugal
  3. 3.Unitat de Biologia EvolutivaUniversitat Pompeu Fabra, Doctor Aiguader 80, 08003 BarcelonaSpain

Personalised recommendations