Abstract
Recent population genetic studies have provided valuable insights on the demographic history of our species. However, some issues such as the dating of the first demographic expansions in human populations remain puzzling. Indeed, although a few genetic studies argued that the first human expansions were concomitant with the Neolithic transition, many others found signals of expansion events starting during the Palaeolithic. Here we performed a simulation study to show that these contradictory findings may result from the differences in the genetic markers used, especially if two successive expansion events occurred. For a large majority of replicates for each scenario tested, microsatellite data allow only detecting the recent expansion event in that case, whereas sequence data allow only detecting the ancient expansion. Combined with previous real data analyses, our results bring support to the ideas that (i) a first human expansions started during the Palaeolithic period, (ii) a second expansion event occurred later, concomitantly with the Neolithic transition.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Kingman JFC : The coalescent. Stochast Proc App 1982; 13: 235–248.
Excoffier L, Heckel G : Computer programs for population genetics data analysis: a survival guide. Nat Rev Genet 2006; 7: 745–758.
Ho SYW, Shapiro B : Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol Ecol Res 2011; 11: 423–434.
Aimé C, Heyer E, Austerlitz F : Inference of sex-specific expansion patterns in human populations from Y-chromosome polymorphism. Am J Phys Anthropol 2015; 157: 217–225.
Wilder JA, Mobasher Z, Hammer MF : Genetic evidence for unequal effective population sizes of human females and males. Mol Biol Evol 2004; 21: 2047–2057.
Heyer E, Chaix R, Pavard S, Austerlitz F : Sex-specific demographic behaviours that shape human genomic variation. Mol Ecol 2012; 21: 597–612.
Zhivotovsky LA, Underhill PA, Cinnioglu C et al: The effective mutation rate at y chromosome short tandem repeats, with application to human population-divergence time. Am J Hum Genet 2004; 74: 50–61.
Ségurel L, Wyman MJ, Przeworki M : Determinants of mutation rate variation in the human germline. Annu Rev Genomics Hum Genet 2014; 15: 47–70.
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.
Beaumont MA, Zhang W, Balding DJ : Approximate Bayesian computation in population genetics. Genetics 2002; 162: 2025–2035.
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.
Schiffels S, Durbin R : Inferring human population size and separation history from multiple genome sequences. Nat Genet 2014; 46: 919–925.
Bocquet-Appel JP, Bar-Yosef O : The Neolithic Demographic Transition and its Consequences. Dordrecht, Netherlands: Springer, 2008.
Bocquet-Appel JP : When the world’s population took off: The springboard of the Neolithic demographic transition. Science 2011; 333: 560–561.
Mellars P : A new radiocarbon revolution and the dispersal of modern humans in Eurasia. Nature 2006; 439: 931–935.
Waters MR, Stafford TW : Redefining the age of Clovis: implications for the peopling of the Americas. Science 2007; 315: 1122–1126.
Goebel T, Waters MR, O’Rourke DH : The late Pleistocene dispersal of modern humans in the Americas. Science 2008; 319: 1497–1502.
Fagundes NJ, Kanitz R, Eckert R et al: Mitochondrial population genomics supports a single pre-Clovis origin with a coastal route for the peopling of the Americas. Am J Hum Genet 2008; 82: 583–592.
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.
Aimé C, Laval G, Patin E et al: Human genetic data show contrasting demographic patterns between sedentary and nomadic populations predating the emergence of farming. Mol Biol Evol 2013; 30: 2629–2644.
Cox MP, Morales DA, Woerner AE, Sozanski J, Wall JD, Hammer MF : 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.
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.
Soares P, Alshamali F, Pereira JB et al: The expansion of mtDNA haplogroup L3 within and out of Africa. Mol Biol Evol 2011; 29: 915–927.
Aimé C, Verdu P, Ségurel L, Martinez-Cruz B, Heyer E, Austerlitz F 2014 Microsatellite data show recent demographic expansions in sedentary but not in nomadic human populations in Africa and Eurasia. Eur J Hum Genet 2014; 22: 1201–1207.
Laval G, Excoffier L : Simcoal 2.0: A program to simulate genomic diversity over large recombining regions in a subdivided population with a complex history. Bioinformatics 2004; 20: 2485–2487.
Drummond AJ, Rambaut A : Beast: Bayesian evolutionary analysis by sampling trees. Bmc Evol Biol 2007; 7: 214.
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.
Pluzhnikov A, Di Rienzo A, Hudson R : Inferences about human demography based on multilocus analyses of noncoding sequences. Genetics 2002; 161: 1209–1218.
Howell N, Kubacka I, Mackey DA : How rapidly does the human mitochondrial genome evolve? Am J Hum Genet 1996; 59: 501–509.
Heyer E, Zietkiewick E, Rochowski A, Yotova V, Puymirat J, Labuda D : Phylogenetic and familial estimates of mitochondrial substitution rates: study of control region mutations in deep-rooting pedigrees. Am J Hum Genet 2001; 63: 1113–1126.
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.
Heyer E, Puymirat J, Dietjes P, Bakker E, De Knijff P : Estimating y chromosome specific microsatellite mutation frequencies using deep rooting pedigrees. Hum Mol Genet 1997; 6: 799–803.
Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV : Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 2012; 29: 2157–2167.
Shea JJ . The impact of projectile weaponry on Late Pleistocene hominin evolution. In: Hublin JJ, Richards MP (eds): Evolution of Hominin Diets. Dordrecht: Springer, 2009.
Weber JL, Wong C : Mutation of human short tandem repeats. Hum Mol Genet 1993; 2: 1123–1128.
Boitard S, Rodriguez W, Jay F, Mona S, Austerlitz F : Inferring population size history from large samples of genome-wide molecular data—an approximate Bayesian computation approach. PLoS Genet 2016; 12: e1005877.
Acknowledgements
This work was supported by the Agence Nationale de la Recherche grant Demochips (ANR-12-BSV7-0012). CA was financed by a PhD grant from the ‘Centre National de la Recherche Scientifique’. We thank Paul Verdu, the editor and two anonymous reviewers for helpful comments and suggestions on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on European Journal of Human Genetics website
Supplementary information
Rights and permissions
About this article
Cite this article
Aimé, C., Austerlitz, F. Different kinds of genetic markers permit inference of Paleolithic and Neolithic expansions in humans. Eur J Hum Genet 25, 360–365 (2017). https://doi.org/10.1038/ejhg.2016.191
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ejhg.2016.191


