Human Evolution

, Volume 21, Issue 1, pp 19–31 | Cite as

Molecular Views of Human Origins

  • R. StanyonEmail author
  • D. Caramelli
  • B. Chiarelli


Over the last half century, comparative genomics has increasingly contributed to the definition, resolution and interpretation of human evolution. Early comparisons demonstrated that African apes and humans were more closely related and diverged later than commonly thought. However, it was difficult to determine the branching between humans, chimpanzees and gorillas. By the 1990s, sufficient biomolecular data had accumulated to demonstrate that chimpanzees and humans shared a common ancestor after the divergence of the gorilla. Current reconstructions place the divergence of humans and chimpanzees at 6–8 million years. Comparative genomics from complete genome sequencing to chromosome painting provide a scenario for the origin of the human genome. Starting form the ancestral mammalian karyotype, we can determine the major steps over the last 90 million years leading to the formation of each human chromosome. Despite considerable technical problems, studies of ancient DNA now provide a direct genetic witness of human evolution and add a temporal dimension to reconstructions of our evolutionary history and phylogeny. Ancient DNA has shown that Neanderthals probably did not interbreed with anatomically modern humans and did not make a significant contribution to the gene pool of our species. Ancient DNA has also contributed to the studies of the colonization of the Americas and the Pacific Island, and the domestication of plants and animals. Understanding the genetic basis of the physical and behavioral traits that distinguish humans from other primates presents one of the great future challenges of science.


phylogeny evolution comparative genomics molecular cytogenetics ancient DNA 


  1. 1.
    Abbott A (2003) Anthropologists cast doubt on human DNA evidence. Nature 423:468Google Scholar
  2. 2.
    Barbujani G, Bertorelle G (2003) Were Cro-Magnons too like us for DNA to tell? Nature 424:127CrossRefGoogle Scholar
  3. 3.
    Beerli P, Edwards SV (2002) When did Neanderthals and modern humans diverge. Evol Anthropol Suppl 1:60–63CrossRefGoogle Scholar
  4. 4.
    Bersaglieri T, Sabeti PC, Patterson N, Vanderploeg T, Schaffner SF, Drake JA, Rhodes M, Reich DE, Hirschhorn JN (2004) Genetic signatures of strong recent positive selection at the lactase gene. Am J Hum Genet 74:1111–1120CrossRefGoogle Scholar
  5. 5.
    Brown P, Sutikna T, Morwood MJ, Soejono RP, Jatmiko, Saptomo EW, Due RA (2004) A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia. Nature 431:1055–1061CrossRefGoogle Scholar
  6. 6.
    Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239CrossRefGoogle Scholar
  7. 7.
    Bruce EJ, Ayala FJ (1978) Humans and apes are genetically very similar. Nature 276:264–265CrossRefGoogle Scholar
  8. 8.
    Bruford MW, Bradley DG, Luikart G (2003) DNA markers reveal the complexity of livestock domestication. Nat Rev Genet 4:900–910CrossRefGoogle Scholar
  9. 9.
    Caramelli D, Lalueza-Fox C, Vernesi C, Lari M, Casoli A, Mallegni F, Chiarelli B, Dupanloup I, Bertranpetit J, Barbujani G, Bertorelle G (2003) Evidence for a genetic discontinuity between Neanderthals and 24,000-year-old anatomically modern Europeans. Proc Natl Acad Sci USA 100:6593–6597CrossRefGoogle Scholar
  10. 10.
    Carroll SB (2003) Genetics and the making of Homo sapiens. Nature 422:849–857CrossRefGoogle Scholar
  11. 11.
    Cavalli-Sforza LL, Piazza A (1993) Human genomic diversity in Europe: A summary of recent research and prospects for the future. Eur J Hum Genet 1:3–18.Google Scholar
  12. 12.
    Chiarelli B (1962) Comparative morphometirc analysis of primate chromosomes. I. The chromosomes of the anthropoid apes and man. Caryologia 15:103–106Google Scholar
  13. 13.
    Chiarelli B (2004) Spongiform encephalopathy, cannibalism and Neanderthals extinction. Hum Evol 19(2):81–92CrossRefGoogle Scholar
  14. 14.
    Cooper A, Poinar HN (2000) Ancient DNA: do it right or not at all. Science 289:1139CrossRefGoogle Scholar
  15. 15.
    Currat M, Excoffier L (2005) The effect of the Neolithic expansion on European molecular diversity. Proc Biol Sci 272:679–688CrossRefGoogle Scholar
  16. 16.
    Deinard A, Kidd K (1999) Evolution of a HOXB6 intergenic region within the great apes and humans. J Hum Evol 36:687–703CrossRefGoogle Scholar
  17. 17.
    Dutrillaux B (1980) Chromosomal evolution of the great apes and man. J Reprod Fertil Suppl 28:105–111Google Scholar
  18. 18.
    Eizirik E, Murphy WJ, Springer MS, O'Brien SJ (2004) Molecular phylogeny and dating of early primate divergences. In: Ross CF, Kay RF (eds) Anthropoid Origins. Kluwer, New YorkGoogle Scholar
  19. 19.
    Endicott P, Gilbert MT, Stringer C, Lalueza-Fox C, Willerslev E, Hansen AJ, Cooper A (2003) The genetic origins of the Andaman Islanders. Am J Hum Genet 72:178–184CrossRefGoogle Scholar
  20. 20.
    Gibbons A (2001) Human anthropology. Modern men trace ancestry to African migrants. Science 292:1051–1052CrossRefGoogle Scholar
  21. 21.
    Goidts V, Szamalek JM, de Jong PJ, Cooper DN, Chuzhanova N, Hameister H, Kehrer-Sawatzki H (2005) Independent intrachromosomal recombination events underlie the pericentric inversions of chimpanzee and gorilla chromosomes homologous to human chromosome 16. Genome Res 15:1232–1242CrossRefGoogle Scholar
  22. 22.
    Goldman D, Giri PR, O'Brien SJ (1987) A molecular phylogeny of the hominoid primates as indicated by two-dimensional protein electrophoresis. Proc Natl Acad Sci USA 84:3307–3311CrossRefGoogle Scholar
  23. 23.
    Goodman M (1962) Immunochemistry of the primates and primate evolution. Ann NY Acad Sci 102:219–234CrossRefGoogle Scholar
  24. 24.
    Goodman M (1962) Evolution of the immunologic species specificity of human serum proteins. Hum Biol 34:104–150Google Scholar
  25. 25.
    Goodman M (1963) Serological analysis of the systematics of recent hominoids. Hum Biol 35:377–436Google Scholar
  26. 26.
    Goodman M, Braunitzer G, Stangl A, Schrank B (1983) Evidence on human origins from haemoglobins of African apes. Nature 303:546–548CrossRefGoogle Scholar
  27. 27.
    Gutierrez G, Sanchez D, Marin A (2002) A reanalysis of the ancient mitochondrial DNA sequences recovered from Neanderthal bones. Mol Biol Evol 19:1359–1366Google Scholar
  28. 28.
    Hasegawa M, Di Rienzo A, Kocher TD, Wilson AC (1993) Toward a more accurate time scale for the human mitochondrial DNA tree. J Mol Evol 37:347–354CrossRefGoogle Scholar
  29. 29.
    Hasegawa M, Kishino H, Yano T (1985) Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174CrossRefGoogle Scholar
  30. 30.
    Hasegawa M, Kishino H, Yano T (1987) Man's place in Hominoidea as inferred from molecular clocks of DNA. J Mol Evol 26:132–147CrossRefGoogle Scholar
  31. 31.
    Hawks J, Hunley K, Lee SH, Wolpoff M (2000) Population bottlenecks and Pleistocene human evolution. Mol Biol Evol 17:2–22Google Scholar
  32. 32.
    Higuchi R, Bowman B, Freiberger M, Ryder OA, Wilson AC (1984) DNA sequences from the quagga, an extinct member of the horse family. Nature 312:282–284CrossRefGoogle Scholar
  33. 33.
    Hixson JE, Brown WM (1986) A comparison of the small ribosomal RNA genes from the mitochondrial DNA of the great apes and humans: Sequence, structure, evolution, and phylogenetic implications. Mol Biol Evol 3:1–18Google Scholar
  34. 34.
    Horai S, Satta Y, Hayasaka K, Kondo R, Inoue T, Ishida T, Hayashi S, Takahata N (1992) Man's place in Hominoidea revealed by mitochondrial DNA genealogy. J Mol Evol 35:32–43CrossRefGoogle Scholar
  35. 35.
    Jobling MA, Gill P (2004) Encoded evidence: DNA in forensic analysis. Nat Rev Genet 5:739–751CrossRefGoogle Scholar
  36. 36.
    Jones M, Brown T (2000) Agricultural origins: the evidence of modern and ancient DNA. Holocene 10:769–776CrossRefGoogle Scholar
  37. 37.
    Jorde LB, Watkins WS, Bamshad MJ, Dixon ME, Ricker CE, Seielstad MT, Batzer MA (2000) The distribution of human genetic diversity: a comparison of mitochondrial, autosomal, and Y-chromosome data. Am J Hum Genet 66:979–988CrossRefGoogle Scholar
  38. 38.
    Kaestee FA, Horsburgh KA (2002) Ancient DNA in anthropology: methods, applications and ethics. Yearb Phys Anthropol 45:92–130CrossRefGoogle Scholar
  39. 39.
    Kehrer-Sawatzki H, Sandig CA, Goidts V, Hameister H (2005) Breakpoint analysis of the pericentric inversion between chimpanzee chromosome 10 and the homologous chromosome 12 in humans. Cytogenet Genome Res 108:91–97CrossRefGoogle Scholar
  40. 40.
    Kehrer-Sawatzki H, Szamalek JM, Tanzer S, Platzer M, Hameister H (2005) Molecular characterization of the pericentric inversion of chimpanzee chromosome 11 homologous to human chromosome 9. Genomics 85:542–550CrossRefGoogle Scholar
  41. 41.
    Koop BF, Goodman M, Xu P, Chan K, Slightom JL (1986) Primate eta-globin DNA sequences and man's place among the great apes. Nature 319:234–238CrossRefGoogle Scholar
  42. 42.
    Krings M, Capelli C, Tschentscher F, Geisert H, Meyer S, von Haeseler A, Grossschmidt K, Possnert G, Paunovic M, Paabo S (2000) A view of Neanderthal genetic diversity. Nat Genet 26:144–146CrossRefGoogle Scholar
  43. 43.
    Krings M, Stone A, Schmitz RW, Krainitzki H, Stoneking M, Paabo S (1997) Neanderthal DNA sequences and the origin of modern humans. Cell 90:19–30CrossRefGoogle Scholar
  44. 44.
    Lalueza-Fox C, Sampietro ML, Gilbert MT, Castri L, Facchini F, Pettener D, Bertranpetit J (2004) Unravelling migrations in the steppe: mitochondrial DNA sequences from ancient central Asians. Proc Biol Sci 271:941–947CrossRefGoogle Scholar
  45. 45.
    Lewontin RC (1972) The apportionment of human diversity. Evol Biol 6:381–398Google Scholar
  46. 46.
    Maca-Meyer N, Arnay M, Rando JC, Flores C, Gonzalez AM, Cabrera VM, Larruga JM (2004) Ancient mtDNA analysis and the origin of the Guanches. Eur J Hum Genet 12:155–162CrossRefGoogle Scholar
  47. 47.
    Marks J, Schimd CW, Sarich VM (1988) DNA hybridization as a guide to phylogeny: relations of the Hominoidea. J Hum Evol 17:769–786CrossRefGoogle Scholar
  48. 48.
    Miyamoto MM, Slightom JL, Goodman M (1987) Phylogenetic relations of humans and African apes from DNA sequences in the psi eta-globin region. Science 238:369–373CrossRefGoogle Scholar
  49. 49.
    Muller S, Finelli P, Neusser M, Wienberg J (2004) The evolutionary history of human chromosome 7. Genomics 84:458–467CrossRefGoogle Scholar
  50. 50.
    Murphy WJ, Stanyon R, O'Brien SJ (2001) Evolution of mammalian genome organization inferred from comparative gene mapping. Genome Biol 2: Reviews0005Google Scholar
  51. 51.
    Nickerson E, Nelson DL (1998) Molecular definition of pericentric inversion breakpoints occurring during the evolution of humans and chimpanzees. Genomics 50:368–372CrossRefGoogle Scholar
  52. 52.
    Nordborg M (1998) On the probability of Neanderthal ancestry. Am J Hum Genet 63:1237–1240CrossRefGoogle Scholar
  53. 53.
    Ovchinnikov IV, Gotherstrom A, Romanova GP, Kharitonov VM, Liden K, Goodwin W (2000) Molecular analysis of Neanderthal DNA from the northern Caucasus. Nature 404:490–493CrossRefGoogle Scholar
  54. 54.
    Paabo S (1985) Molecular cloning of ancient Egyptian mummy DNA. Nature 314:644–645CrossRefGoogle Scholar
  55. 55.
    Paabo S, Poinar H, Serre D, Jaenicke-Despres V, Hebler J, Rohland N, Kuch M, Krause J, Vigilant L, Hofreiter M (2004) Genetic analyses from ancient DNA. Annu Rev Genet 38:645–679CrossRefGoogle Scholar
  56. 56.
    Powell JR, Caccone A (1990) The TEACL method of DNA–DNA hybridization: technical considerations. J Mol Evol 30:267–272CrossRefGoogle Scholar
  57. 57.
    Raaum RL, Sterner KN, Noviello CM, Stewart CB, Disotell TR (2005) Catarrhine primate divergence dates estimated from complete mitochondrial genomes: concordance with fossil and nuclear DNA evidence. J Hum Evol 48:237–257CrossRefGoogle Scholar
  58. 58.
    Reed FA, Akey JM, Aquadro CF (2005) Fitting background-selection predictions to levels of nucleotide variation and divergence along the human autosomes. Genome Res 15:1211–1221CrossRefGoogle Scholar
  59. 59.
    Relethford JH (2001) Absence of regional affinities of Neanderthal DNA with living humans does not reject multiregional evolution. Am J Phys Anthropol 115:95–98CrossRefGoogle Scholar
  60. 60.
    Relethford JH (2001) Ancient DNA and the origin of modern humans. Proc Natl Acad Sci USA 98:390–391CrossRefGoogle Scholar
  61. 61.
    Rockman MV, Hahn MW, Soranzo N, Zimprich F, Goldstein DB, Wray GA (2005) Ancient and recent positive selection transformed opioid cis-regulation in humans. PLoS Biol 3:e387CrossRefGoogle Scholar
  62. 62.
    Romagno D, Chiarelli B, Sineo L (2004) Evolution of human chromosome 7: new information form the mapping of William–Breuren locus on ono-human primate chromosomes. Caryologia 57:39–43Google Scholar
  63. 63.
    Ruvolo M (1997) Molecular phylogeny of the hominoids: inferences from multiple independent DNA sequence data sets. Mol Biol Evol 14:248–265Google Scholar
  64. 64.
    Saitou N, Nei M (1986) The number of nucleotides required to determine the branching order of three species, with special reference to the human–chimpanzee–gorilla divergence. J Mol Evol 24:189–204CrossRefGoogle Scholar
  65. 65.
    Sakoyama Y, Hong KJ, Byun SM, Hisajima H, Ueda S, Yaoita Y, Hayashida H, Miyata T, Honjo T (1987) Nucleotide sequences of immunoglobulin epsilon genes of chimpanzee and orangutan: DNA molecular clock and hominoid evolution. Proc Natl Acad Sci USA 84:1080–1084CrossRefGoogle Scholar
  66. 66.
    Sarich VM, Wilson AC (1967) Immunological time scale for hominid evolution. Science 158:1200–1203CrossRefGoogle Scholar
  67. 67.
    Satta Y, Takahata N (2004) The distribution of the ancestral haplotype in finite stepping-stone models with population expansion. Mol Ecol 13:877–886CrossRefGoogle Scholar
  68. 68.
    Schmitz RW, Serre D, Bonani G, Feine S, Hillgruber F, Krainitzki H, Paabo S, Smith FH (2002) The Neanderthal type site revisited: Interdisciplinary investigations of skeletal remains from the Neander Valley, Germany. Proc Natl Acad Sci USA 99:13342–13347CrossRefGoogle Scholar
  69. 69.
    Serre D, Langaney A, Chech M, Teschler-Nicola M, Paunovic M, Mennecier P, Hofreiter M, Possnert G, Paabo S (2004) No evidence of Neanderthal mtDNA contribution to early modern humans. PLoS Biol 2:E57CrossRefGoogle Scholar
  70. 70.
    Shimada MK, Kim CG, Kitano T, Ferrell RE, Kohara Y, Saitou N (2005) Nucleotide sequence comparison of a chromosome rearrangement on human chromosome 12 and the corresponding ape chromosomes. Cytogenet Genome Res 108:83–90CrossRefGoogle Scholar
  71. 71.
    Sibley CG, Ahlquist JE (1984) The phylogeny of the hominoid primates, as indicated by DNA–DNA hybridization. J Mol Evol 20:2–15CrossRefGoogle Scholar
  72. 72.
    Sibley CG, Ahlquist JE (1987) DNA hybridization evidence of hominoid phylogeny: results from an expanded data set. J Mol Evol 26:99–121CrossRefGoogle Scholar
  73. 73.
    Sibley CG, Comstock JA, Ahlquist JE (1990) DNA hybridization evidence of hominoid phylogeny: a reanalysis of the data. J Mol Evol 30:202–236CrossRefGoogle Scholar
  74. 74.
    Smouse PE, Li WH (1987) Likelihood analysis of mitocondrial restriction-cleavage patterns for the human–chimpanzee–gorilla trichotomy. Evolution 41:1162–1176CrossRefGoogle Scholar
  75. 75.
    Stanyon R, Chiarelli B (1982) Phylogeny of the hominiodea: the chromosome evidence. J Hum Evol 11:493–504CrossRefGoogle Scholar
  76. 76.
    Stanyon R, Chiarelli B (1991) Human origins a brief summary of biomolecular and paleontological data (Selected Symposia and Monographs U.Z.I. 4). Mucchi, ModenaGoogle Scholar
  77. 77.
    Stringer C, Davies W (2001) Archaeology. Those elusive Neanderthals. Nature 413:791–792CrossRefGoogle Scholar
  78. 78.
    Stringer CB, Andrews P (1988) Genetic and fossil evidence for the origin of modern humans. Science 239:1263–1268CrossRefGoogle Scholar
  79. 79.
    Svartman M, Stone G, Page JE, Stanyon R (2004) A chromosome painting test of the basal eutherian karyotype. Chromosome Res 12:45–53CrossRefGoogle Scholar
  80. 80.
    Takahata N, Satta Y (1997) Evolution of the primate lineage leading to modern humans: Phylogenetic and demographic inferences from DNA sequences. Proc Natl Acad Sci USA 94:L4811–L4815CrossRefGoogle Scholar
  81. 81.
    Templeton A (1983) Phylogenetic inforence from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and apes. Evolution 37:221–244CrossRefGoogle Scholar
  82. 82.
    Templeton A (1985) The phylogeny of the hominoid primates: a statistical analysis of the DNA–DNA hybridization data. Mol Biol Evol 2:420–433Google Scholar
  83. 83.
    Templeton A (2002) Out of Africa again and again. Nature 416:45–51CrossRefGoogle Scholar
  84. 84.
    Vernesi C, Caramelli D, Dupanloup I, Bertorelle G, Lari M, Cappellini E, Moggi-Cecchi J, Chiarelli B, Castri L, Casoli A, Mallegni F, Lalueza-Fox C, Barbujani G (2004) The Etruscans: a population-genetic study. Am J Hum Genet 74:694–704CrossRefGoogle Scholar
  85. 85.
    Voight BF, Adams AM, Frisse LA, Qian Y, Hudson RR, Di Rienzo A (2005) A Interrogating multiple aspects of variation in a full resequencing data set to infer human population size changes. Proc Natl Acad Sci USA 102:18508–18513CrossRefGoogle Scholar
  86. 86.
    Willerslev E, Cooper A (2005) Ancient DNA. Proc Biol Sci 272:3–16CrossRefGoogle Scholar
  87. 87.
    Wimmer R, Kirsch S, Rappold GA, Schempp W (2002) Direct evidence for the Homo-Pan clade. Chromosome Res 10:55–61CrossRefGoogle Scholar
  88. 88.
    Wolpoff MH, Spuhler JN, Smith FH, Radovcic J, Pope G, Frayer DW, Eckhardt R, Clark G (1988) Modern human origins. Science 241:772–774CrossRefGoogle Scholar
  89. 89.
    Yunis JJ, Prakash O, (1982) The origin of man: a chromosomal pictorial legacy. Science 215:1525–1530CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media B.V. 2006

Authors and Affiliations

  1. 1.Laboratorio di Antropologia, Dipartimento di Biologia Animale e GeneticaUniversity of FlorenceFlorenceItaly

Personalised recommendations