Abstract
Genetic and paleoanthropological evidence is in accord that today’s human population is the result of a great demic (demographic and geographic) expansion that began approximately 45,000 to 60,000 y ago in Africa and rapidly resulted in human occupation of almost all of the Earth’s habitable regions. Genomic data from contemporary humans suggest that this expansion was accompanied by a continuous loss of genetic diversity, a result of what is called the “serial founder effect.” In addition to genomic data, the serial founder effect model is now supported by the genetics of human parasites, morphology, and linguistics. This particular population history gave rise to the two defining features of genetic variation in humans: genomes from the substructured populations of Africa retain an exceptional number of unique variants, and there is a dramatic reduction in genetic diversity within populations living outside of Africa. These two patterns are relevant for medical genetic studies mapping genotypes to phenotypes and for inferring the power of natural selection in human history. It should be appreciated that the initial expansion and subsequent serial founder effect were determined by demographic and sociocultural factors associated with hunter-gatherer populations. How do we reconcile this major demic expansion with the population stability that followed for thousands years until the inventions of agriculture? We review advances in understanding the genetic diversity within Africa and the great human expansion out of Africa and offer hypotheses that can help to establish a more synthetic view of modern human evolution.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Oppenheimer S (2012) A single southern exit of modern humans from Africa: Before or after Toba? Quat Int 258: 88–99.
Rasmussen M, et al. (2011) An Aboriginal Australian genome reveals separate human dispersals into Asia. Science 334(6052):94–98.
Macaulay V, et al. (2005) Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308(5724):1034–1036.
Bar-Yosef O (2000) The Middle and early Upper Paleolithic in Southwest Asia and neighboring regions. The Geography of Neandertais and Modern Humans in Europe and the Greater Mediterranean, eds Bar-Yosef O, Pilbeam D (Peabody Museum Press, Cambridge, MA), pp 107–156.
Klein R (2009) The Human Career. Human Biological and Cultural Origins (Univ Chicago Press, Chicago).
Hodgson JA, Bergey CM, Disotell TR (2010) Neandertal genome: The ins and outs of African genetic diversity. Curr Biol 20(12):R517–R519.
Mellars P (2006) Why did modern human populations disperse from Africa ca. 60,000 years ago? A new model. Proc Natl Acad Sci USA 103(25):9381–9386.
Mcbrearty S, Brooks AS (2000) The revolution that wasn’t: A new interpretation of the origin of modern human behavior. J Hum Evol 39(5):453–563.
Klein RG (2003) Paleoanthropology. Whither the Nean-derthaIs? Science 299(5612):1525–1527.
Stewart JR, Stringer CB (2012) Human evolution out of Africa: The role of refugia and climate change. Science 335(6074):1317–1321.
Cavalli-Sforza LL, Menozzi P, Piazza A (1994) The History and Geography of Human Genes (Princeton Univ Press, Princeton).
McEvoy BP, Powell JE, Goddard ME, Visscher PM (2011) Human population dispersal "Out of Africa" estimated from linkage disequilibrium and allele frequencies of SNPs. Genome fles 21(6):821–829.
Amos W, Hoffman JL (2010) Evidence that two main bottleneck events shaped modern human genetic diversity. Proc Biol Sci 277(1678):131–137.
Laval G, Patin E, Barreiro LB, Quintana-Murci L (2010) Formulating a historical and demographic model of recent human evolution based on resequencing data from noncoding regions. PLoS ONE 5(4):e10284.
Fagundes NJR, et al. (2007) Statistical evaluation of alternative models of human evolution. Proc Natl Acad Sci USA 104(45):17614–17619.
Gravel S, et al; 1000 Genomes Project (2011) Demographic history and rare allele sharing among human populations. Proc Natl Acad Sci USA 108(29):11983–11988.
Li H, Durbin R (2011) Inference of human population history from individual whole-genome sequences. Nature 475(7357):493–496.
Underhill PA, Kivisild T (2007) Use of y chromosome and mitochondrial DNA population structure in tracing human migrations. Annu Rev Genet 41:539–564.
Eller E, Hawks J, Relethford JH (2004) Local extinction and recoIonization, species effective population size, and modern human origins. Hum Biol 76:789–809.
Cann HM, et al. (2002) A human genome diversity cell line panel. Science 296(5566):261–262.
Ramachandran S, et al. (2005) Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc Natl Acad Sci USA 102(44): 15942–15947.
Rosenberg NA, et al. (2002) Genetic structure of human populations. Science 298(5602):2381–2385.
Li JZ, et al. (2008) Worldwide human relationships inferred from genome-wide patterns of variation. Science 319(5866):1100–1104.
DeGiorgio M, Jakobsson M, Rosenberg NA (2009) Out of Africa: Modern human origins special feature: explaining worldwide patterns of human genetic variation using a coalescent-based serial founder model of migration outward from Africa. Proc Natl Acad Sci USA 106(38): 16057–16062.
Deshpande O, Batzoglou S, Feldman MW, Cavalli-Sforza LL (2009) A serial founder effect model for human settlement out of Africa. Proc Biol Sci 276(1655):291–300.
Henn BM, Gravel S, Moreno-Estrada A, Acevedo-Acevedo S, Bustamante CD (2010) Fine-scale population structure and the era of next-generation sequencing. Hum Mol Genet 19(R2):R221–R226.
Tishkoff SA, et al. (2009) The genetic structure and history of Africans and African Americans. Science 324(5930):1035–1044.
Vigilant L, Stoneking M, Harpending H, Hawkes K, Wilson AC (1991) African populations and the evolution of human mitochondrial DNA. Science 253(5027):1503–1507.
Endicott P, Ho SYW, Stringer C (2010) Using genetic evidence to evaluate four palaeoanthropological hypotheses for the timing of Neanderthal and modern human origins. J Hum Evol 59(1):87–95.
Ghirotto S, Tassi F, Benazzo A, Barbujani G (2011) No evidence of Neandertal admixture in the mitochondrial genomes of early European modern humans and contemporary Europeans. Am J Phys Anthropol 146(2): 242–252.
Krause J, et al. (2010) The complete mitochondrial DNA genome of an unknown hominin from southern Siberia. Nature 464(7290):894–897.
Green RE, et al. (2010) A draft sequence of the Neandertal genome. Science 328(5979):710–722.
Reich D, et al. (2010) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468(7327):1053–1060.
Brauer G (2008) The origin of modern anatomy: by speciation or intraspecific evolution? Evol Anthropol 17:22–37.
Pearson OM (2008) Statistical and biological definitions of “anatomically modern” humans: Suggestions for a unified approach to modern morphology. Evol Anthropol 17:38–48
Weaver TD (2012) Did a discrete event 200,000-100,000 years ago produce modern humans? J Hum Evol 63(1):121–126.
McDougall I, Brown FH, Fleagle JG (2005) Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature 433(7027):733–736.
Gignoux CR, Henn BM, Mountain JL (2011) Rapid, global demographic expansions after the origins of agriculture. Proc Natl Acad Sci USA 108(15):6044–6049.
Marth GT, Czabarka E, Murvai J, Sherry ST (2004) The allele frequency spectrum in genome-wide human variation data reveals signals of differential demographic history in three large world populations. Genetics 166(1):351–372.
Voight BF, et al. (2005) Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc Natl Acad Sci USA 102(51):18508–18513.
Zhivotovsky LA, Rosenberg NA, Feldman MW (2003) Features of evolution and expansion of modern humans, inferred from genomewide microsatellite markers. Am J Hum Genet 72(5):1171–1186.
Kidd JM, et al. (2012) Population genetic inference from personal genome data: Impact of ancestry and admixture on human genomic variation. Am J Hum Genet 91:660–671.
Blum MGB, Jakobsson M (2011) Deep divergences of human gene trees and models of human origins. Mo! Biol EVD/28(2):889–898.
Atkinson QD, Gray RD, Drummond AJ (2009) Bayesian coalescent inference of major human mitochondrial DNA haplogroup expansions in Africa. Proc Biol Sci 276(1655):367–373.
Soares P, et al. (2012) The Expansion of mtDNA Haplogroup L3 within and out of Africa. Mol Biol Evol 29 (3):915-927.
Patin E, et al. (2009) Inferring the demographic history of African farmers and pygmy hunter-gatherers using a multilocus resequencing data set. PLoS Genet 5(4): e1000448.
Cox MP, et al. (2009) Autosomal resequence data reveal Late Stone Age signals of population expansion in sub-Saharan African foraging and farming populations. PLoSONE 4(7):e6366.
Batini C, et al. (2011) Insights into the demographic history of African Pygmies from complete mitochondrial genomes. Mol Biol Evol 28(2):1099–1110.
Verdu P, et al. (2009) Origins and genetic diversity of pygmy hunter-gatherers from Western Central Africa. CurrBiol 19(4):312–318.
Harding RM, McVean G (2004) A structured ancestral population for the evolution of modern humans. Curr Opin Genet Dev 14(6):667–674.
Henn BM, et al. (2011) Hunter-gatherer genomic diversity suggests a southern African origin for modern humans. Proc Natl Acad Sci USA 108(13):5154–5162.
Gronau I, Hubisz MJ, Gulko B, Danko CG, Siepel A (2011) Bayesian inference of ancient human demography from individual genome sequences. Nat Genet 43(10):1031–1034.
Schlebusch CM, et al. (2012) Genomic variation in seven Khoe-San groups reveals adaptation and complex African history. Science, 10.1126/science.1227721.
Henn BM, Bustamante CD, Mountain JL, Feldman MW (2011) Reply to Hublin and Klein: Locating a geographic point of dispersion in Africa for contemporary humans. Proc Natl Acad Sci USA 108:E278.
Hublin JJ, Klein RG (2011) Northern Africa could also have housed the source population for living humans. Proc Natl Acad Sci USA 108(28):E277.
Henn BM, et al. (2012) Genomic ancestry of North Africans supports back-to-Africa migrations. PLoS Genet 8(1): e1002397.
Tanabe K, et al. (2010) Plasmodium falciparum accompanied the human expansion out of Africa. Curr Biol 20(14):1283–1289.
Linz B, et al. (2007) An African origin for the intimate association between humans and Helicobacter pylori. Nature 445(7130):915–918.
Betti L, Balloux F, Amos W, Hanihara T, Manica A (2009) Distance from Africa, not climate, explains within-population phenotypic diversity in humans. Proc Biol Sci 276(1658):809–814.
Manica A, Amos W, Balloux F, Hanihara T (2007) The effect of ancient population bottlenecks on human phenotypic variation. Nature 448(7151):346–348.
von Cramon-Taubadel N, Lycett SJ (2008) Brief communication: Human cranial variation fits iterative founder effect model with African origin. Am J Phys Anthropol 136(1):108–113.
Darwin C (1860) The Origin of Species (John Murray, London), 2nd Ed, Chap 14, pp 392–393.
Cavalli-Sforza LL, Piazza A, Menozzi P, Mountain J (1988) Reconstruction of human evolution: Bringing together genetic, archaeological, and linguistic data. Proc Natl Acad Sci USA 85(16):6002–6006.
Cavalli-Sforza LL, Minch E, Mountain JL (1992) devolution of genes and languages revisited. Proc Natl Acad Sci USA 89(12):5620–5624.
Atkinson QD (2011) Phonemic diversity supports a serial founder effect model of language expansion from Africa. Science 332(6027):346–349.
Gell-Mann M, Ruhlen M (2011) The origin and evolution of word order. Proc Natl Acad Sci USA 108(42): 17290–17295.
Ruhlen M (1994) The Origin of Language: Tracing the Evolution of the Mother Tongue (Wiley, New York).
Hamilton MJ, et al. (2009) Population stability, cooperation, and the invasibility of the human species. Proc Natl Acad Sci USA 106(30): 12255–12260.
Coventry A, et al. (2010) Deep resequencing reveals excess rare recent variants consistent with explosive population growth. Nat Commun 1:131.
Tennessen JA, etal; Broad GO; Seattle GO; NHLBI Exome Sequencing Project (2012) Evolution and functional impact of rare coding variation from deep sequencing of human exomes. Science 337(6090):64–69.
Keinan A, Clark AG (2012) Recent explosive human population growth has resulted in an excess of rare genetic variants. Science 336(6082):740–743.
Read DW, LeBlanc SA (2003) Population growth, carrying capacity, and conflict. Curr Anthropol 44:59–85.
Hill KR, et al. (2011) Co-residence patterns in hunter-gatherer societies show unique human social structure. Science 331(6022):1286–1289.
Lee RB, DeVore I, eds (1968) Man the Hunter (Aldine, Chicago).
Birdsell JB (1973) A basic demographic unit. Curr An thropol 14:337–356.
Verdu P, et al. (2010) Limited dispersal in mobile hunter-gatherer Baka Pygmies. Biol Lett 6(6):858–861.
Pampiglione S, Ricciardi ML (1986) Parasitological surveys of Pygmy groups. African Pygmies, ed Cavalli-Sforza LL (Academic, New York), pp 153–165.
Howell N (1979) Demography of the Dobe IKung (Academic, New York).
Blurton Jones NG, Hawkes K, O’Connell JF (2002) Antiquity of postreproductive life: Are there modern impacts on hunter-gatherer postreproductive life spans? Am J Hum Biol 14(2):184–205.
Ferguson R (1928) Tuberculosis Among the Indians of the Great Canadian Plains (Adlard, London).
Pepperell CS, et al. (2011) Dispersal of Mycobacterium tuberculosis via the Canadian fur trade. Proc Natl Acad Sci USA 108(16):6526–6531.
Hewlett BS, Hewlett BL (2010) Sex and searching for children among Aka foragers and Ngandu farmers of Central Africa. AfrStudy Monogr 31:107–125.
Mace RH, Alvergne A (2012) Female reproductive competition within families in rural Gambia. Proc R Soc B Biol Sci 279(1736):2219–2227.
Acknowledgments
The authors thank Christopher Gignoux for assistance in creating the map (Fig. 1). This research was supported in part by National Institutes of Health Grants GM28016, HG003329, and 3R01HG003229.
Author information
Authors and Affiliations
Contributions
Author contributions: B.M.H., L.L.C.-S., and M.W.F. designed research, performed research, analyzed data, and wrote the paper.
Corresponding author
Additional information
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Rights and permissions
About this article
Cite this article
Henn, B.M., Cavalli-Sforza, L.L. & Feldman, M.W. The great human expansion. Reson 24, 711–718 (2019). https://doi.org/10.1007/s12045-019-0830-4
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12045-019-0830-4