Abstract
The transition from hunting and gathering to plant and animal domestication was one of the most important cultural and technological revolutions in human history. According to archeologists and paleoanthropologists, this transition triggered major demographic expansions. However, few genetic studies have found traces of Neolithic expansions in the current repartition of genetic polymorphism, pointing rather toward Paleolithic expansions. Here, we used microsatellite autosomal data to investigate the past demographic history of 87 African and Eurasian human populations with contrasted lifestyles (nomadic hunter-gatherers, semi-nomadic herders and sedentary farmers). Likely due to the combination of a higher mutation rate and the possibility to analyze several loci as independent replicates of the coalescent process, the analysis of microsatellite data allowed us to infer more recent expansions than previous genetic studies, potentially resulting from the Neolithic transition. Despite the variability in their location and environment, we found consistent expansions for all sedentary farmers, while we inferred constant population sizes for all hunter-gatherers and most herders that could result from constraints linked to a nomadic or semi-nomadic lifestyle and/or competition for land between herders and farmers. As an exception, we inferred expansions for Central Asian herders. This might be linked with the arid environment of this area that may have been more favorable to nomadic herders than to sedentary farmers. Alternatively, current Central Asian herders may descent from populations who have first experienced a transition from hunter-gathering to sedentary agropastoralism, and then a second transition to nomadic herding.
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References
Bar-Yosef O, Belfer-Cohen A : From sedentary hunter-gatherers to territorial farmers in the Levant; In: Gregg SA (ed):: Between Bands and States. Carbondale, IL, USA: Center for Archaeological Investigations, University at Carbondale, 1991, pp 181–202.
Mazoyer M, Roudart L : A History of World Agriculture: From the Neolithic Age to the Current Crisis. London, 2006.
Bocquet-Appel JP, Bar-Yosef O : The Neolithic Demographic Transition and Its Consequences. Springer, 2008.
Bocquet-Appel JP : When the world’s population took off: the springboard of the Neolithic demographic transition. Science 2011; 333: 560–561.
Caldwell JC, Caldwell BK : Was there a Neolithic mortality crisis? J Popul Res 2003; 20: 153–168.
Kingman JFC : The coalescent. Stochast Proc App 1982; 13: 235–248.
Emerson BC, Paradis E, Thebaud C : Revealing the demographic histories of species using DNA sequences. Trends Ecol Evol 2001; 16: 707–716.
Excoffier L, Heckel G : Computer programs for population genetics data analysis: a survival guide. Nat Rev Genet 2006; 7: 745–758.
Kuhner MK : Coalescent genealogy samplers: windows into population history. Trends Ecol Evol 2008; 24: 86–93.
Soares P, Alshamali F, Pereira JB et al: The Expansion of mtDNA Haplogroup L3 within and out of Africa. Mol Biol Evol 2012; 29: 915–927.
Chaix R, Austerlitz F, Hegay T, Quintana-Murci L, Heyer E : Genetic traces of east-to-west human expansion waves in Eurasia. Am J Phys Anthropol 2008; 136: 309–317.
Pritchard JK, Seielstad MT, Perez-Lezaun A, Feldman MW : Population growth of human Y chromosomes: a study of Y chromosome microsatellites. Mol Biol Evol 1999; 16: 1791–1798.
Cox MP, Morales DA, Woerner AE et al: Autosomal resequence data reveal late stone age signals of population expansion in Sub-Saharan African foraging and farming populations. PLoS One 2009; 4: e6366.
Laval G, Patin E, Barreiro LB, Quintana-Murci L : Formulating a historical and demographic model of recent human evolution based on resequencing data from noncoding regions. Plos One 2010; 5: e10284.
Gignoux CR, Henn BM, Mountain JL : Rapid, global demographic expansions after the origins of agriculture. Proc Natl Acad Sci USA 2011; 108: 6044–6049.
Batini C, Lopes J, Behar DM et al: Insights into the demographic history of African pygmies from complete mitochondrial genomes. Mol Biol Evol 2011; 28: 1099–1110.
Aime C, Laval G, Patin E et al: Human genetic data reveal contrasting demographic patterns between sedentary and nomadic populations that predate the emergence of farming. Mol Biol Evol 2013; 30: 2629–2644.
Lavery S, Moritz C, Fielder DR : Genetic patterns suggest exponential population growth in a declining species. Mol Biol Evol 1996; 13: 1106–1113.
Zhivotovsky LA, Rosenberg NA, Feldman MW : Features of evolution and expansion of modern humans, inferred from genomewide microsatellite markers. Am J Hum Genet 2003; 72: 1171–1186.
Cornuet JM, Ravigne V, Estoup A : Inference on population history and model checking using DNA sequence and microsatellite data with the software diyabc (v1.0). BMC Bioinformatics 2010; 11: 401.
Hu Y, Guo Y, Qi D et al: Genetic structuring and recent demographic history of red pandas (Ailurus fulgens) inferred from microsatellite and mitochondrial DNA. Mol Ecol 2011; 20: 2662–2675.
Fontaine MC, Snirc A, Frantzis A et al: History of expansion and anthropogenic collapse in a top marine predator of the black sea estimated from genetic data. Proc Natl Acad Sci USA 2012; 109: E2569–E2576.
Patin E, Laval G, Barreiro LB et al: Inferring the demographic history of African farmers and Pygmy hunter-gatherers using a multilocus resequencing data set. PLoS Genet 2009; 5: e1000448.
Verdu P, Austerlitz F, Estoup A et al: Origins and genetic diversity of Pygmy hunter-gatherers from Western Central Africa. Curr Biol 2009; 19: 312–318.
Phillipson D : African Archaeology. Cambridge: Cambridge University Press, 1993.
Oslisly R : The history of human settlement in the Middle Ogooue Valley, in Weber W, White LJT, Vedder A, Naughton-Treves L (eds): African Rain Forest Ecology and Conservation: An Interdisciplinary Perspective. New Haven (Connecticut) and London: Yale University Press, 2001, Chapter 7, pp 101–118.
Dirksen VG, Van Geel B : Mid to late Holocene climate change and its influence on cultural development in South Central Siberia; in Scott EM, Alekseev AY, Zaitseva GI (eds): Impact of the Environment on Human Migration in Eurasia. NATO Science Series: IV: Earth and Environmental Sciences Vol 42. Kluver Academic Publishers, 2004, pp 291–307.
Nei M, Roychoudhury AK : Evolutionary relationships of human populations on a global scale. Mol Biol Evol 1993; 10: 927–943.
Cavalli-Sforza LL, Menozzi P, Piazza A : The history and geography of human genes. Princeton University Press: Princeton.
Harris DR : The origins and spread of agriculture and pastoralism in Eurasia: an overview; In: Harris DR (ed): The Origins and Spread of Agriculture and Pastoralism in Eurasia. London, UK: UCL Press University College, 1996.
Verdu P, Becker NS, Froment A et al: Sociocultural behavior, sex-biased admixture, and effective population sizes in Central African Pygmies and non-Pygmies. Mol Biol Evol 2013; 30: 918–937.
Tishkoff SA, Reed FA, Friedlaender FR et al: The genetic structure and history of Africans and African Americans. Science 2009; 324: 1035–1044.
Cann HM, De Toma C, Cazes L et al: A human genome diversity cell line panel. Science 2002; 296: 261–262.
Rosenberg NA, Pritchard JK, Weber JL et al: Genetic structure of human populations. Science 2002; 298: 2381–2385.
Ségurel L, Martinez-Cruz B, Quintana-Murci L et al: Sex-specific genetic structure and social organization in central Asia: insights from a multi-locus study. PLoS Genet 2008; 4: e1000200.
Heyer E, Georges M, Pachner M, Endicott P : Genetic diversity of four Filipino Negrito populations from Luzon: comparison of male and female effective population sizes and differential integration of immigrants into Aeta and Agta communities. Hum Biol 2013; 85: 189–208.
Heyer E, Balaresque P, Jobling MA et al: Genetic diversity and the emergence of ethnic groups in Central Asia. Bmc Genet 2009; 10: 49.
Weber JL, Broman KW : Genotyping for human whole-genome scans: past, present, and future. Adv Genet 2001; 42: 77–96.
Kuhner MK, Yamato J, Felsenstein J : Estimating effective population size and mutation rate from sequence data using Metropolis-Hastings sampling. Genetics 1995; 140: 1421–1430.
Drummond AJ, Rambaut A : BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007; 7: 214.
Wu CH, Drummond AJ : Joint inference of microsatellite mutation models, population history and genealogies using transdimensional Markov Chain Monte Carlo. Genetics 2011; 188: 151–164.
Rambaut A, Drummond AJ Tracer, ver. 1.5. Available at http://beast.bio.ed.ac.uk/Tracer, 2007.
Gelman A, Rubin DB : Inference from iterative simulation using multiple sequences (with discussion). Stat Sci 1992; 7: 457–511.
R Development Core Team: R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing, 2011.
Plummer M, Best N, Cowles K, Vines K : Coda: convergence diagnosis and output analysis for MCMC. R News 2006; 6: 7–11.
Dib C, Faure S, Fizames C et al: A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature 1996; 380: 152–154.
Loader C : Local Regression and Likelihood. New-York: Springer, 1999.
Spiegelhalter DJ, Best NG, Carlin BR, Van Der Linde A : Bayesian measures of model complexity and fit. J R Stat Soc B Stat Meth 2002; 64: 583–616.
Bolker B : Ecological Models and Data in R. Princeton: Princeton University Press, 2008.
Short R : The biological basis for the contraceptive effects of breast feeding. Int J Gynaecol Obstet 1982; 25: 207–217.
Cerny V, Pereira L, Musilova E et al: Genetic structure of pastoral and farmer populations in the African Sahel. Mol Biol Evol 2011; 28: 2491–2500.
Excoffier L, Schneider S : Why hunter-gatherer populations do not show signs of Pleistocene demographic expansions. Proc Natl Acad Sci USA 1999; 96: 10597–10602.
Renfrew C : Language families and the spread of farming; in Harris DR (ed): The Origins and Spread of Agriculture and Pastoralism in Eurasia. London: UCL Press, 1996, pp 70–92.
Tremblay M, Vezina H : New estimates of intergenerational time intervals for the calculation of age and origins of mutations. Am J Hum Genet 2000; 66: 651–658.
Atkinson QD, Gray RD, Drummond AJ : Bayesian coalescent inference of major human mitochondrial DNA haplogroup expansions in Africa. Proc Biol Sci 2009; 276: 367–373.
Fu Q, Rudan P, Paabo S, Krause J : Complete mitochondrial genomes reveal Neolithic expansion into Europe. PLoS One 2012; 7: e32473.
Acknowledgements
We warmly thank all volunteer participants. We are also grateful to Michael Fontaine for his help on some data analyses, and Friso Palstra for his assistance with English language use. We also thank the editor and two anonymous reviewers for helpful comments and suggestions. All computationally intensive analyses were run on the Linux cluster of the ‘Museum National d’Histoire Naturelle’ (administrated by Julio Pedraza). This work was supported by ATM-MNHN grant ‘Les relations Sociétés-Natures dans le long terme’, by the ANR grant ‘Altérité culturelle’ (ANR-10-ESVS-0010) and by the ANR grant DemoChips (12-BSV7-0012). CA was financed by a PhD grant from the ‘Centre National de la Recherche Scientifique’. CA and FA received a travel grant from the NEFREX project funded by the European Union (People Marie Curie Actions, International Research Staff Exchange Scheme, call FP7-PEOPLE-2012-IRSES) to visit Alexei Drummond's group (developer of Beast) in New Zealand.
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Aimé, C., Verdu, P., Ségurel, L. et al. Microsatellite data show recent demographic expansions in sedentary but not in nomadic human populations in Africa and Eurasia. Eur J Hum Genet 22, 1201–1207 (2014). https://doi.org/10.1038/ejhg.2014.2
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DOI: https://doi.org/10.1038/ejhg.2014.2
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