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Human evolution

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March 25th 2013. QMUL SBCS.

March 25th 2013. QMUL SBCS.

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  • 1. Human evolution
  • 2. Human evolution
  • 3. Human evolutionAncestors, relatives & major transitions
  • 4. Human evolutionAncestors, relatives & major transitions Recent insights from genomics
  • 5. Human evolutionAncestors, relatives & major transitions Recent insights from genomics What about today?
  • 6. Benton (2005) Fig 10.47
  • 7. Relatives and recent ancestorsPLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDSSPIDER MONKEY MACAQUE SIAMANG GIBBON ORANGUTAN GORILLA HUMAN CHIMPANZEE Potential 6 MYA common PROCONSUL SIVAPITHECUS OURANOPITHECUS DRYOPITHECUS 14 MYA 9 MYA ancestors 19 MYA 16 MYA (Miocene) FAMILY TREE of hominoids encompasses the lesser apes (siamangs and 25 MYA gibbons), great apes (orangutans, gorillas and chimpanzees), and humans. Most Miocene apes were evolutionary dead ends. But researchers have identified a handful of them as candidate ancestors of living apes and humans. Proconsul, a primitive Miocene ape, is thought to have been the last common ancestor of the living hominoids; Sivapithecus, an early great ape, is widely regarded as an orangutan forebear; and either 40 MILLION YEARS AGO Dryopithecus or Ouranopithecus may have given rise to African apes and humans. simple chewing surfaces — a feeding ap- suspensory locomotion, especially in east Asia. Most phylogenetic analyses paratus well suited to a diet of soft, ripe the elbow joint, which was fully extend- concur that it is from Sivapithecus that © Scientific American
  • 8. Relatives and recent ancestorsPLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDSSPIDER MONKEY MACAQUE SIAMANG GIBBON ORANGUTAN GORILLA HUMAN CHIMPANZEE Potential 6 MYA common PROCONSUL SIVAPITHECUS OURANOPITHECUS DRYOPITHECUS 14 MYA 9 MYA ancestors 19 MYA 16 MYA (Miocene) FAMILY TREE of hominoids encompasses the lesser apes (siamangs and 25 MYA gibbons), great apes (orangutans, gorillas and chimpanzees), and humans. Most Miocene apes were evolutionary dead ends. But researchers have identified a handful of them as candidate ancestors of living apes and humans. Proconsul, a primitive Miocene ape, is thought to have been the last common ancestor of the living hominoids; Sivapithecus, an early great ape, is widely regarded as an orangutan forebear; and either 40 MILLION YEARS AGO Dryopithecus or Ouranopithecus may have given rise to African apes and humans. simple chewing surfaces — a feeding ap- suspensory locomotion, especially in east Asia. Most phylogenetic analyses paratus well suited to a diet of soft, ripe the elbow joint, which was fully extend- concur that it is from Sivapithecus that © Scientific American
  • 9. Proconsul
  • 10. Rift valley
  • 11. Relatives and recent ancestorsPLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDSSPIDER MONKEY MACAQUE SIAMANG GIBBON ORANGUTAN GORILLA HUMAN CHIMPANZEE Potential 6 MYA common PROCONSUL SIVAPITHECUS OURANOPITHECUS DRYOPITHECUS 14 MYA 9 MYA ancestors 19 MYA 16 MYA (Miocene) FAMILY TREE of hominoids encompasses the lesser apes (siamangs and 25 MYA gibbons), great apes (orangutans, gorillas and chimpanzees), and humans. Most Miocene apes were evolutionary dead ends. But researchers have identified a handful of them as candidate ancestors of living apes and humans. Proconsul, a primitive Miocene ape, is thought to have been the last common ancestor of the living hominoids; Sivapithecus, an early great ape, is widely regarded as an orangutan forebear; and either 40 MILLION YEARS AGO Dryopithecus or Ouranopithecus may have given rise to African apes and humans. simple chewing surfaces — a feeding ap- suspensory locomotion, especially in east Asia. Most phylogenetic analyses paratus well suited to a diet of soft, ripe the elbow joint, which was fully extend- concur that it is from Sivapithecus that © Scientific American
  • 12. Relatives and recent ancestorsPLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDSSPIDER MONKEY MACAQUE SIAMANG GIBBON ORANGUTAN GORILLA HUMAN CHIMPANZEE Potential 6 MYA common PROCONSUL SIVAPITHECUS OURANOPITHECUS DRYOPITHECUS 14 MYA 9 MYA ancestors 19 MYA 16 MYA (Miocene) FAMILY TREE of hominoids encompasses the lesser apes (siamangs and 25 MYA gibbons), great apes (orangutans, gorillas and chimpanzees), and humans. Most Miocene apes were evolutionary dead ends. But researchers have identified a handful of them as candidate ancestors of living apes and humans. Proconsul, a primitive Miocene ape, is thought to have been the last common ancestor of the living hominoids; Sivapithecus, an early great ape, is widely regarded as an orangutan forebear; and either 40 MILLION YEARS AGO Dryopithecus or Ouranopithecus may have given rise to African apes and humans. simple chewing surfaces — a feeding ap- suspensory locomotion, especially in east Asia. Most phylogenetic analyses paratus well suited to a diet of soft, ripe the elbow joint, which was fully extend- concur that it is from Sivapithecus that © Scientific American
  • 13. Major transitions in human evolution
  • 14. Major transitions in human evolution In which order?
  • 15. Major transitions in human evolution• Bipedalism (down from the trees) In which order?
  • 16. Major transitions in human evolution• Bipedalism (down from the trees)• Increased brain size In which order?
  • 17. Major transitions in human evolution• Bipedalism (down from the trees)• Increased brain size In which order?• Use of simple stone tools
  • 18. Major transitions in human evolution• Bipedalism (down from the trees)• Increased brain size In which order?• Use of simple stone tools• Fire
  • 19. Major transitions in human evolution• Bipedalism (down from the trees)• Increased brain size In which order?• Use of simple stone tools• Fire• Sophisticated tools (stone, bone...)
  • 20. Major transitions in human evolution• Bipedalism (down from the trees)• Increased brain size In which order?• Use of simple stone tools• Fire• Sophisticated tools (stone, bone...)• Language, culture, agriculture...
  • 21. Million! years! Glacial cycles! Homo! P. robustus! Arctic icecap! Australopithecus africanus/! A. afarensis! Ardipithecus ramidus! Antarctic icecap! Orrorin tugenensis! Cold! Warm! Climate!WP! Mid Miocene! Late Miocene! Climate! cooling! Habitat! fragmentation!
  • 22. Why bipedalism? Mid Miocene! Late Miocene! Climate! cooling! Habitat! fragmentation! Million! years! Glacial cycles! Homo! P. robustus! Arctic icecap! Australopithecus africanus/! A. afarensis! Ardipithecus ramidus! Antarctic icecap! Orrorin tugenensis! Cold! Warm! Climate!
  • 23. Why bipedalism? Mid Miocene! Late Miocene!• Energy efficient locomotion Climate! cooling! (for distant food sources) Habitat! fragmentation! Million! years! Glacial cycles! Homo! P. robustus! Arctic icecap! Australopithecus africanus/! A. afarensis! Ardipithecus ramidus! Antarctic icecap! Orrorin tugenensis! Cold! Warm! Climate!
  • 24. Why bipedalism? Mid Miocene! Late Miocene!• Energy efficient locomotion Climate! cooling! (for distant food sources) Habitat!• Less exposure to sun? fragmentation! Million! years! Glacial cycles! Homo! P. robustus! Arctic icecap! Australopithecus africanus/! A. afarensis! Ardipithecus ramidus! Antarctic icecap! Orrorin tugenensis! Cold! Warm! Climate!
  • 25. Why bipedalism? Mid Miocene! Late Miocene!• Energy efficient locomotion Climate! cooling! (for distant food sources) Habitat!• Less exposure to sun? fragmentation!• Free the hands? Million! years! Glacial cycles! Homo! P. robustus! Arctic icecap! Australopithecus africanus/! A. afarensis! Ardipithecus ramidus! Antarctic icecap! Orrorin tugenensis! Cold! Warm! Climate!
  • 26. Why bipedalism? Mid Miocene! Late Miocene!• Energy efficient locomotion Climate! cooling! (for distant food sources) Habitat!• Less exposure to sun? fragmentation!• Free the hands? Million! years! Glacial cycles! Homo!• Seeingfarther: Finding food & avoiding predators? P. robustus! Arctic icecap! Australopithecus africanus/! A. afarensis! Ardipithecus ramidus! Antarctic icecap! Orrorin tugenensis! Cold! Warm! Climate!
  • 27. Why bipedalism? Mid Miocene! Late Miocene!• Energy efficient locomotion Climate! cooling! (for distant food sources) Habitat!• Less exposure to sun? fragmentation!• Free the hands? Million! years! Glacial cycles! Homo!• Seeingfarther: Finding food & avoiding predators? P. robustus! Arctic icecap! Australopithecus africanus/! A. afarensis!• Sexual or anti-predator Ardipithecus ramidus! Antarctic icecap! displays? Orrorin tugenensis! Cold! Warm! Climate!
  • 28. Running
  • 29. Running• sweating for thermoregulation.
  • 30. Running• sweating for thermoregulation.• arched foot + achilles tendon
  • 31. Running• sweating for thermoregulation.• arched foot + achilles tendon• head stabilization
  • 32. Running• sweating for thermoregulation.• arched foot + achilles tendon• head stabilization• early Homo?
  • 33. Running• sweating for thermoregulation.• arched foot + achilles tendon• head stabilization• early Homo?• first: improved scavenging.
  • 34. Running• sweating for thermoregulation.• arched foot + achilles tendon• head stabilization• early Homo?• first: improved scavenging.• then persistence hunting
  • 35. Relatives and recent ancestorsPLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDSSPIDER MONKEY MACAQUE SIAMANG GIBBON ORANGUTAN GORILLA HUMAN CHIMPANZEE Potential 6 MYA common PROCONSUL SIVAPITHECUS OURANOPITHECUS DRYOPITHECUS 14 MYA 9 MYA ancestors 19 MYA 16 MYA (Miocene) FAMILY TREE of hominoids encompasses the lesser apes (siamangs and 25 MYA gibbons), great apes (orangutans, gorillas and chimpanzees), and humans. Most Miocene apes were evolutionary dead ends. But researchers have identified a handful of them as candidate ancestors of living apes and humans. Proconsul, a primitive Miocene ape, is thought to have been the last common ancestor of the living hominoids; Sivapithecus, an early great ape, is widely regarded as an orangutan forebear; and either 40 MILLION YEARS AGO Dryopithecus or Ouranopithecus may have given rise to African apes and humans. simple chewing surfaces — a feeding ap- suspensory locomotion, especially in east Asia. Most phylogenetic analyses paratus well suited to a diet of soft, ripe the elbow joint, which was fully extend- concur that it is from Sivapithecus that © Scientific American
  • 36. Most lineageswent extinct
  • 37. Proconsulidae Most lineages went extinct
  • 38. Proconsulidae Most lineages went extinct
  • 39. AustralopithecinesProconsulidae Most lineages went extinct
  • 40. H. erectus AustralopithecinesProconsulidae Most lineages went extinct
  • 41. H. sapiens H. erectus AustralopithecinesProconsulidae Most lineages went extinct
  • 42. H. neanderthalensis H. sapiens H. erectus AustralopithecinesProconsulidae Most lineages went extinct
  • 43. AustralopithecinesWikipedia
  • 44. Taung child1924 Australopithecus afarensis 2.5 mya
  • 45. Lucy - Australopithecus afarensis 1978 3.2 mya
  • 46. Australopithecines 30° 20° 10° 0° 10° 20° 30° 40° 50° 60°30° 30° Brain size: 35% of modern human20° 20° A. Bahrelghazali10° A. Afarensis 10° A. Gahri P. Aethiopicus P. Boisei A. Anamensis0° 0°10° 10°20° P. Robustus (Crassidens) A. Africanus30° 0 (km) 3 000 30°Wikipedia 0 (mi) Projection de Lambert azimutale équivalente 2 000 30° 20° 10° 0° 10° 20° 30° 40° 50° 60°
  • 47. Evidence for bipedalism in Australopithecines
  • 48. Evidence for bipedalism in Australopithecines
  • 49. Evidence for bipedalism in Australopithecines
  • 50. Evidence for bipedalism in Australopithecines• Pelvis short & broad (like humans), not long & narrow (like gorilla)
  • 51. Evidence for bipedalism in Australopithecines• Pelvis short & broad (like humans), not long & narrow (like gorilla)• Hip & walking muscles arranged like in a bipedal organism
  • 52. Evidence for bipedalism in Australopithecines• Pelvis short & broad (like humans), not long & narrow (like gorilla)• Hip & walking muscles arranged like in a bipedal organism• Femur angled as in humans, not straight as in chimps
  • 53. Evidence for bipedalism in Australopithecines• Pelvis short & broad (like humans), not long & narrow (like gorilla)• Hip & walking muscles arranged like in a bipedal organism• Femur angled as in humans, not straight as in chimps• Feet
  • 54. Fossilized tracks atLaetoli (Tanzania) Footprints preserved in volcanic ash from: 3 hominids (Australopithecus afarensis) Numerous other mammals
  • 55. Fossilized tracks atLaetoli (Tanzania) Footprints preserved in volcanic ash from: 3 hominids (Australopithecus afarensis) Numerous other mammals
  • 56. Tool use?
  • 57. Tool use?• generally: only simple tools (similarly to current non-human great apes).
  • 58. Tool use?• generally: only simple tools (similarly to current non-human great apes).• butAustralopithecus garhi (2.5 mya) may have made stone tools.
  • 59. Summary: Australopithecines• Major group of early bipedal hominids (4mya to 1 mya)• Small brains• Only in Africa• Many forms/species
  • 60. H. neanderthalensis H. sapiens H. erectus AustralopithecinesProconsulidae Most lineages went extinct
  • 61. Homo
  • 62. Homo habilis
  • 63. Tool useChimps and other animalsmay use objects as tools. H. sapiens! H. habilis! Australopithecine!
  • 64. Tool use H. habilis made toolsChimps and other animalsmay use objects as tools. H. sapiens! H. habilis! Australopithecine!
  • 65. Tool use H. habilis made toolsChimps and other animalsmay use objects as tools. Cutting H. sapiens! H. habilis! Australopithecine!
  • 66. Tool use H. habilis made toolsChimps and other animalsmay use objects as tools. Cutting Scraping H. sapiens! H. habilis! Australopithecine!
  • 67. Stages of humanevolution are defined bythe style andsophistication of stonetools….e.g.:•Oldowan (2.5-1.5 mya)•Achuelian (1.5-0.2 mya)
  • 68. Oldowan toolsHammerstone Choppers Scraper Flakes
  • 69. Brain sizes increase
  • 70. Out of Africa - H. erectus
  • 71. Homo erectus (Java, 1893)
  • 72. Acheulian toolsHandaxes! Cleaver! Handaxe Pick! Scraper! Trimming flakes!
  • 73. Nariokotome/Turkana boy H. erectus Found 1984 in Kenya. From1.5mya
  • 74. H. erectus lifestyle• …language?
  • 75. H. erectus lifestyle• Stone tools (Acheulian) • …language?
  • 76. H. erectus lifestyle• Stone tools (Acheulian)• Fire • …language?
  • 77. H. erectus lifestyle• Stone tools (Acheulian)• Fire• Sociality • …language?
  • 78. H. erectus lifestyle• Stone tools (Acheulian)• Fire• Sociality• Hunting • …language?
  • 79. Homo floresiensis “The Hobbit”
  • 80. Homo floresiensis “The Hobbit” H. florensis vs. H. sapiens skull
  • 81. Homo floresiensis “The Hobbit” H. florensis vs. H. sapiens skull
  • 82. Nature (2004) vol. 431, 1043-1044
  • 83. H. neanderthalensis H. sapiens H. erectus AustralopithecinesProconsulidae Most lineages went extinct
  • 84.
  • 85. Neanderthal 600,000-30,000 years ago
  • 86. Burial ritual?
  • 87. Neanderthals - Summary• Neanderthals were morphologically and genetically distinct from early H. sapiens• disappearedafter H. sapiens arrived - possibly because they were culturally less advanced.
  • 88. H. neanderthalensis H. sapiens H. erectus AustralopithecinesProconsulidae Most lineages went extinct
  • 89. H. sapiens out of Africa
  • 90. H. sapiens out of Africa• 50,000 years ago: fully “modern” with language, music etc.
  • 91. H. sapiens out of Africa• 50,000 years ago: fully “modern” with language, music etc.• Began migrating out of Africa 70,000 years ago
  • 92. H. sapiens out of Africa• 50,000 years ago: fully “modern” with language, music etc.• Began migrating out of Africa 70,000 years ago• Simultaneous decline of other Homo species (competition or hybridization?)
  • 93. Burial ritual in early H. sapiens• At Sungir, Russia, around 28,000 years ago• A 60 year old buried with an elaborate collection of beads, necklaces and bracelets
  • 94. Examples of early H. sapiens tools
  • 95. Lascaux
  • 96. Recent insights from genomics
  • 97. RESEARCH ARTICLE changed parts of their genome with the ances- tors of these groups.A Draft Sequence of the Several features of DNA extracted from Late Pleistocene remains make its study challenging. The DNA is invariably degraded to a small aver-Neandertal Genome age size of less than 200 base pairs (bp) (21, 22), it is chemically modified (21, 23–26), and extractsRichard E. Green,1*†‡ Johannes Krause,1†§ Adrian W. Briggs,1†§ Tomislav Maricic,1†§ almost always contain only small amounts of en-Udo Stenzel,1†§ Martin Kircher,1†§ Nick Patterson,2†§ Heng Li,2† Weiwei Zhai,3†|| dogenous DNA but large amounts of DNA fromMarkus Hsi-Yang Fritz,4† Nancy F. Hansen,5† Eric Y. Durand,3† Anna-Sapfo Malaspinas,3† microbial organisms that colonized the specimensJeffrey D. Jensen,6† Tomas Marques-Bonet,7,13† Can Alkan,7† Kay Prüfer,1† Matthias Meyer,1† after death. Over the past 20 years, methods forHernán A. Burbano,1† Jeffrey M. Good,1,8† Rigo Schultz,1 Ayinuer Aximu-Petri,1 Anne Butthof,1 ancient DNA retrieval have been developed (21, 22),Barbara Höber,1 Barbara Höffner,1 Madlen Siegemund,1 Antje Weihmann,1 Chad Nusbaum,2 largely based on the polymerase chain reactionEric S. Lander,2 Carsten Russ,2 Nathaniel Novod,2 Jason Affourtit,9 Michael Egholm,9 (PCR) (27). In the case of the nuclear genome ofChristine Verna,21 Pavao Rudan,10 Dejana Brajkovic,11 Željko Kucan,10 Ivan Gušic,10 Neandertals, four short gene sequences have beenVladimir B. Doronichev,12 Liubov V. Golovanova,12 Carles Lalueza-Fox,13 Marco de la Rasilla,14 determined by PCR: fragments of the MC1R geneJavier Fortea,14 ¶ Antonio Rosas,15 Ralf W. Schmitz,16,17 Philip L. F. Johnson,18† Evan E. Eichler,7† involved in skin pigmentation (28), a segment ofDaniel Falush,19† Ewan Birney,4† James C. Mullikin,5† Montgomery Slatkin,3† Rasmus Nielsen,3† the FOXP2 gene involved in speech and language loaded from www.sciencemag.org on March 24, 2013Janet Kelso,1† Michael Lachmann,1† David Reich,2,20*† Svante Pääbo1*† (29), parts of the ABO blood group locus (30), and a taste receptor gene (31). However, although PCRNeandertals, the closest evolutionary relatives of present-day humans, lived in large parts of Europe of ancient DNA can be multiplexed (32), it doesand western Asia before disappearing 30,000 years ago. We present a draft sequence of the Neandertal not allow the retrieval of a large proportion of thegenome composed of more than 4 billion nucleotides from three individuals. Comparisons of the genome of an organism.Neandertal genome to the genomes of five present-day humans from different parts of the world The development of high-throughput DNA se-identify a number of genomic regions that may have been affected by positive selection in ancestral quencing technologies (33, 34) allows large-scale,modern humans, including genes involved in metabolism and in cognitive and skeletal development. genome-wide sequencing of random pieces ofWe show that Neandertals shared more genetic variants with present-day humans in Eurasia than with DNA extracted from ancient specimens (35–37)present-day humans in sub-Saharan Africa, suggesting that gene flow from Neandertals into the and has recently made it feasible to sequence ge-ancestors of non-Africans occurred before the divergence of Eurasian groups from each other. 1 Department of Evolutionary Genetics, Max-Planck Institute forT Evolutionary Anthropology, D-04103 Leipzig, Germany. 2Broad he morphological features typical of Nean- sumed ancestors of present-day Europeans. Institute of MIT and Harvard, Cambridge, MA 02142, USA. dertals first appear in the European fossil Similarly, analysis of DNA sequence data from 3 Department of Integrative Biology, University of California, record about 400,000 years ago (1–3). present-day humans has been interpreted as evi- Berkeley, CA 94720, USA. 4European Molecular BiologyProgressively more distinctive Neandertal forms dence both for (12, 13) and against (14) a genetic Laboratory–European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, CB10 1SD, UK.subsequently evolved until Neandertals disap- contribution by Neandertals to present-day hu- 5 Genome Technology Branch, National Human Genome Re-peared from the fossil record about 30,000 years mans. The only part of the genome that has been search Institute, National Institutes of Health, Bethesda, MDago (4). During the later part of their history, examined from multiple Neandertals, the mito- 20892, USA. 6Program in Bioinformatics and Integrative Biology,Neandertals lived in Europe and Western Asia chondrial DNA (mtDNA) genome, consistently University of Massachusetts Medical School, Worcester, MA 01655, USA. 7Howard Hughes Medical Institute, Departmentas far east as Southern Siberia (5) and as far falls outside the variation found in present-day of Genome Sciences, University of Washington, Seattle, WAsouth as the Middle East. During that time, Nean- humans and thus provides no evidence for inter- 98195, USA. 8Division of Biological Sciences, University of
  • 98. RESEARCH ARTICLE changed parts of their genome with the ances- tors of these groups.A Draft Sequence of the Several features of DNA extracted from Late Pleistocene remains make its study challenging. The DNA is invariably degraded to a small aver-Neandertal Genome age size of less than 200 base pairs (bp) (21, 22), it is chemically modified (21, 23–26), and extractsRichard E. Green,1*†‡ Johannes Krause,1†§ Adrian W. Briggs,1†§ Tomislav Maricic,1†§ almost always contain only small amounts of en-Udo Stenzel,1†§ Martin Kircher,1†§ Nick Patterson,2†§ Heng Li,2† Weiwei Zhai,3†|| dogenous DNA but large amounts of DNA fromMarkus Hsi-Yang Fritz,4† Nancy F. Hansen,5† Eric Y. Durand,3† Anna-Sapfo Malaspinas,3† microbial organisms that colonized the specimensJeffrey D. Jensen,6† Tomas Marques-Bonet,7,13† Can Alkan,7† Kay Prüfer,1† Matthias Meyer,1† after death. Over the past 20 years, methods forHernán A. Burbano,1† Jeffrey M. Good,1,8† Rigo Schultz,1 Ayinuer Aximu-Petri,1 Anne Butthof,1 ancient DNA retrieval have been developed (21, 22),Barbara Höber,1 Barbara Höffner,1 Madlen Siegemund,1 Antje Weihmann,1 Chad Nusbaum,2 largely based on the polymerase chain reactionEric S. Lander,2 Carsten Russ,2 Nathaniel Novod,2 Jason Affourtit,9 Michael Egholm,9 (PCR) (27). In the case of the nuclear genome ofChristine Verna,21 Pavao Rudan,10 Dejana Brajkovic,11 Željko Kucan,10 Ivan Gušic,10 Neandertals, four short gene sequences have beenVladimir B. Doronichev,12 Liubov V. Golovanova,12 Carles Lalueza-Fox,13 Marco de la Rasilla,14 determined by PCR: fragments of the MC1R geneJavier Fortea,14 ¶ Antonio Rosas,15 Ralf W. Schmitz,16,17 Philip L. F. Johnson,18† Evan E. Eichler,7† involved in skin pigmentation (28), a segment ofDaniel Falush,19† Ewan Birney,4† James C. Mullikin,5† Montgomery Slatkin,3† Rasmus Nielsen,3† the FOXP2 gene involved in speech and language loaded from www.sciencemag.org on March 24, 2013Janet Kelso,1† Michael Lachmann,1† David Reich,2,20*† Svante Pääbo1*† (29), parts of the ABO blood group locus (30), and a taste receptor gene (31). However, although PCRNeandertals, the closest evolutionary relatives of present-day humans, lived in large parts of Europe of ancient DNA can be multiplexed (32), it doesand western Asia before disappearing 30,000 years ago. We present a draft sequence of the Neandertal not allow the retrieval of a large proportion of thegenome composed of more than 4 billion nucleotides from three individuals. Comparisons of the genome of an organism.Neandertal genome to the genomes of five present-day humans from different parts of the world The development of high-throughput DNA se-identify a number of genomic regions that may have been affected by positive selection in ancestral quencing technologies (33, 34) allows large-scale,modern humans, including genes involved in metabolism and in cognitive and skeletal development. genome-wide sequencing of random pieces ofWe show that Neandertals shared more genetic variants with present-day humans in Eurasia than with DNA extracted from ancient specimens (35–37)present-day humans in sub-Saharan Africa, suggesting that gene flow from Neandertals into the and has recently made it feasible to sequence ge-ancestors of non-Africans occurred before the divergence of Eurasian groups from each other. 1 Department of Evolutionary Genetics, Max-Planck Institute forT Evolutionary Anthropology, D-04103 Leipzig, Germany. 2Broad he morphological features typical of Nean- sumed ancestors of present-day Europeans. Institute of MIT and Harvard, Cambridge, MA 02142, USA. dertals first appear in the European fossil Similarly, analysis of DNA sequence data from 3 Department of Integrative Biology, University of California, record about 400,000 years ago (1–3). present-day humans has been interpreted as evi- Berkeley, CA 94720, USA. 4European Molecular BiologyProgressively more distinctive Neandertal forms dence both for (12, 13) and against (14) a genetic Laboratory–European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, CB10 1SD, UK.subsequently evolved until Neandertals disap- contribution by Neandertals to present-day hu- 5 Genome Technology Branch, National Human Genome Re-peared from the fossil record about 30,000 years mans. The only part of the genome that has been 2-4% of eurasian DNA comes from Neanderthals search Institute, National Institutes of Health, Bethesda, MDago (4). During the later part of their history, examined from multiple Neandertals, the mito- 20892, USA. 6Program in Bioinformatics and Integrative Biology,Neandertals lived in Europe and Western Asia chondrial DNA (mtDNA) genome, consistently University of Massachusetts Medical School, Worcester, MA 01655, USA. 7Howard Hughes Medical Institute, Departmentas far east as Southern Siberia (5) and as far falls outside the variation found in present-day of Genome Sciences, University of Washington, Seattle, WAsouth as the Middle East. During that time, Nean- humans and thus provides no evidence for inter- 98195, USA. 8Division of Biological Sciences, University of
  • 99. RESEARCH ARTICLE changed parts of their genome with the ances- tors of these groups.A Draft Sequence of the Several features of DNA extracted from Late Pleistocene remains make its study challenging. The DNA is invariably degraded to a small aver-Neandertal Genome age size of less than 200 base pairs (bp) (21, 22), it is chemically modified (21, 23–26), and extractsRichard E. Green,1*†‡ Johannes Krause,1†§ Adrian W. Briggs,1†§ Tomislav Maricic,1†§ almost always contain only small amounts of en-Udo Stenzel,1†§ Martin Kircher,1†§ Nick Patterson,2†§ Heng Li,2† Weiwei Zhai,3†|| dogenous DNA but large amounts of DNA fromMarkus Hsi-Yang Fritz,4† Nancy F. Hansen,5† Eric Y. Durand,3† Anna-Sapfo Malaspinas,3† microbial organisms that colonized the specimensJeffrey D. Jensen,6† Tomas Marques-Bonet,7,13† Can Alkan,7† Kay Prüfer,1† Matthias Meyer,1† after death. Over the past 20 years, methods forHernán A. Burbano,1† Jeffrey M. Good,1,8† Rigo Schultz,1 Ayinuer Aximu-Petri,1 Anne Butthof,1 ancient DNA retrieval have been developed (21, 22),Barbara Höber,1 Barbara Höffner,1 Madlen Siegemund,1 Antje Weihmann,1 Chad Nusbaum,2 largely based on the polymerase chain reactionEric S. Lander,2 Carsten Russ,2 Nathaniel Novod,2 Jason Affourtit,9 Michael Egholm,9 (PCR) (27). In the case of the nuclear genome ofChristine Verna,21 Pavao Rudan,10 Dejana Brajkovic,11 Željko Kucan,10 Ivan Gušic,10 Neandertals, four short gene sequences have beenVladimir B. Doronichev,12 Liubov V. Golovanova,12 Carles Lalueza-Fox,13 Marco de la Rasilla,14 determined by PCR: fragments of the MC1R geneJavier Fortea,14 ¶ Antonio Rosas,15 Ralf W. Schmitz,16,17 Philip L. F. Johnson,18† Evan E. Eichler,7† involved in skin pigmentation (28), a segment ofDaniel Falush,19† Ewan Birney,4† James C. Mullikin,5† Montgomery Slatkin,3† Rasmus Nielsen,3† the FOXP2 gene involved in speech and language loaded from www.sciencemag.org on March 24, 2013Janet Kelso,1† Michael Lachmann,1† David Reich,2,20*† Svante Pääbo1*† (29), parts of the ABO blood group locus (30), and a taste receptor gene (31). However, although PCRNeandertals, the closest evolutionary relatives of present-day humans, lived in large parts of Europe of ancient DNA can be multiplexed (32), it doesand western Asia before disappearing 30,000 years ago. We present a draft sequence of the Neandertal not allow the retrieval of a large proportion of thegenome composed of more than 4 billion nucleotides from three individuals. Comparisons of the genome of an organism.Neandertal genome to the genomes of five present-day humans from different parts of the world The development of high-throughput DNA se-identify a number of genomic regions that may have been affected by positive selection in ancestral quencing technologies (33, 34) allows large-scale,modern humans, including genes involved in metabolism and in cognitive and skeletal development. genome-wide sequencing of random pieces ofWe show that Neandertals shared more genetic variants with present-day humans in Eurasia than with DNA extracted from ancient specimens (35–37)present-day humans in sub-Saharan Africa, suggesting that gene flow from Neandertals into the and has recently made it feasible to sequence ge-ancestors of non-Africans occurred before the divergence of Eurasian groups from each other. 1 Department of Evolutionary Genetics, Max-Planck Institute forT Evolutionary Anthropology, D-04103 Leipzig, Germany. 2Broad he morphological features typical of Nean- sumed ancestors of present-day Europeans. Institute of MIT and Harvard, Cambridge, MA 02142, USA. dertals first appear in the European fossil Similarly, analysis of DNA sequence data from 3 Department of Integrative Biology, University of California, record about 400,000 years ago (1–3). present-day humans has been interpreted as evi- Berkeley, CA 94720, USA. 4European Molecular BiologyProgressively more distinctive Neandertal forms dence both for (12, 13) and against (14) a genetic Laboratory–European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire, CB10 1SD, UK.subsequently evolved until Neandertals disap- contribution by Neandertals to present-day hu- 5 Genome Technology Branch, National Human Genome Re-peared from the fossil record about 30,000 years mans. The only part of the genome that has been 2-4% of eurasian DNA comes from Neanderthals search Institute, National Institutes of Health, Bethesda, MDago (4). During the later part of their history, examined from multiple Neandertals, the mito- 20892, USA. 6Program in Bioinformatics and Integrative Biology,Neandertals lived in Europe and Western Asia chondrial DNA (mtDNA) genome, consistently University of Massachusetts Medical School, Worcester, MA 01655, USA. 7Howard Hughes Medical Institute, Departmentas far east as Southern Siberia (5) and as far falls outside the variation found in present-day of Genome Sciences, University of Washington, Seattle, WAsouth as the Middle East. During that time, Nean- humans and thus provides no evidence for inter- 98195, USA. 8Division of Biological Sciences, University of
  • 100. Strong reproductive isolation between humanStrong reproductive isolation between humansand Neanderthals inferred from observed Neanderthals inferred from observedpatterns of introgressionpatterns of introgressionMathias Currata,1 and Laurent Excoffierb,c,1Mathias Currata,1 and Laurent Excoffierb,c,1aa Anthropology, Anthropology, Genetics, and Peopling History Laboratory, Anthropology Unit, Department of of Genetics and Evolution, University G Genetics, and Peopling History Laboratory, Anthropology Unit, Department Genetics and Evolution, University of o1227 Geneva, Switzerland; bComputational and Molecular Population Genetics Laboratory, Institute Ecology and Evolution, Univers1227 Geneva, Switzerland; bComputational and Molecular Population Genetics Laboratory, Institute of of Ecology and Evolution, Uni3012 Berne, Switzerland; and cSwiss Institute of Bioinformatics, 1015 Lausanne, Switzerland3012 Berne, Switzerland; and cSwiss Institute of Bioinformatics, 1015 Lausanne, SwitzerlandEdited by Svante Pääbo, Max Planck Institute of Evolutionary Anthropology, Leipzig, Germany, and approved August 3, 2011 (receEdited by Svante Pääbo, Max Planck Institute of Evolutionary Anthropology, Leipzig, Germany, and approved August 3, 2011 (receiveMay 10, 2011)May 10, 2011)Recent studies have revealed that 2–3% of the genome of non-Recent studies have revealed that 2–3% of the genome of non- To examine these issues and clarify the proce To examine these issues and clarify the proAfricans might come from Neanderthals, suggesting a a more complexAfricans might come from Neanderthals, suggesting more complex between Neanderthals and modern humans, we between Neanderthals and modern humans,scenario of modern human evolution than previously anticipated. InInscenario of modern human evolution than previously anticipated. istic and spatially explicit model of of admixt istic and spatially explicit model admixturethis paper, we use a model of admixture during a a spatial expansionthis paper, we use a model of admixture during spatial expansion between modern humans and Neanderthals (3 between modern humans and Neanderthalsto study the hybridization of Neanderthals with modern humansto study the hybridization of Neanderthals with modern humans simulations, we have estimated the interbree simulations, we have estimated the interbduring their spread out of Africa. We find that observed low levelsduring their spread out of Africa. We find that observed low levels between humans and Neanderthals as as well t between humans and Neanderthals well as aof Neanderthal ancestry in Eurasians are compatible with a a very lowof Neanderthal ancestry in Eurasians are compatible with very low hybridization that is is compatible with the o hybridization that compatible with the obsrate of interbreeding (<2%), potentially attributable to a a very strongrate of interbreeding (<2%), potentially attributable to very strong Neanderthal ancestry in in contemporary huma Neanderthal ancestry contemporary humans,avoidance of interspecific matings, aa low fitness of hybrids, or both.avoidance of interspecific matings, low fitness of hybrids, or both. latter migrated out of of Africa into Eurasia 50 latter migrated out Africa into Eurasia 50 kyThese results suggesting the presence of very effective barriers totoThese results suggesting the presence of very effective barriersgene flow between the two species are robust to uncertainties aboutgene flow between the two species are robust to uncertainties about Results Resultsthe exact demography of the Paleolithic populations, and they are Low Rates of of Interbreeding Between Humathe exact demography of the Paleolithic populations, and they are Low Rates Interbreeding Between Humansalso found to be compatible with the observed lack of mtDNA in- Using spatially explicit simulations, wewealso found to be compatible with the observed lack of mtDNA in-trogression. Our model additionally suggests that similarly low levels Using spatially explicit simulations, havtrogression. Our model additionally suggests that similarly low levels expected amount of of Neanderthal ancestry pr expected amount Neanderthal ancestry in inof introgression in Europe and Asia may result from distinct admix-of introgression in Europe and Asia may result from distinct admix- from Europe (France) and Asia (China) forfoture events having occurred beyond the Middle East, after the split ofof from Europe (France) and Asia (China)ture events having occurred beyond the Middle East, after the split admixture with Neanderthals and over variou admixture with Neanderthals and over varEuropeans and Asians. This hypothesis could be tested because it it derthal ranges (Fig. 1).1). Under our modelEuropeans and Asians. This hypothesis could be tested becausepredicts that different components of Neanderthal ancestry should derthal ranges (Fig. Under our model ofpredicts that different components of Neanderthal ancestry should range expansion, we find that observed low leve range expansion, we find that observed low lbe present in Europeans and in Asians.be present in Europeans and in Asians. introgression into Eurasians imply the existe
  • 101. Denisovans
  • 102. Denisovans• Only known remains(all found since 2010): phalanx (finger bone), three teeth, a toe bone. From 41,000 years ago.
  • 103. Denisovans• Only known remains(all found since 2010): phalanx (finger bone), three teeth, a toe bone. From 41,000 years ago.• Amazinglywell preserved DNA (Siberia; average temperature 0°C). sequenced the genome.
  • 104. Denisovans• Only known remains(all found since 2010): phalanx (finger bone), three teeth, a toe bone. From 41,000 years ago.• Amazinglywell preserved DNA (Siberia; average temperature 0°C). sequenced the genome.• Common ancestor with Neanderthal: 600,000 years ago
  • 105. Denisovans• Only known remains(all found since 2010): phalanx (finger bone), three teeth, a toe bone. From 41,000 years ago.• Amazingly well preserved DNA (Siberia; average temperature 0°C). sequenced the genome.• Common ancestor with Neanderthal: 600,000 years ago• Interbreeding with Homo sapiens: 4-6% of Melanesian genomes are from Denisovan.
  • 106. H. neanderthalensis H. sapiens H. erectus AustralopithecinesProconsulidae Most lineages went extinct
  • 107. H. neanderthalensis H. sapiens Denisovan H. erectus AustralopithecinesProconsulidae Most lineages went extinct
  • 108. Stoneking & Krause 2011? No admixture detected despite probable overlap! detected admixture (location uncertain) African ori of mtDNA lations have of our spec the deepest sity 14,62–65. G view 7–9, and humans ind within mod from south mately 115 humans fir divergences 35–50 kya13 of a strong our genome close correlaStoneking & Krause 2011 in a populat ulation from
  • 109. A WINDING PATH H. sapiens spread from Africa toAfter early modern humans left Africa around 60,000 years ago (top western Asia and then to Europe andright), they spread across the globe and interbred with other southern Asia, eventually reachingdescendants of Homo heidelbergensis. Australasia and the Americas. 0 Homo sapiens Homo floresiensis Denisovans Neanderthals Homo erectus 0.4 Homo heidelbergensisMillion years ago 0.8 Homo antecessor H. heidelbergensis originated from 1.2 H. erectus in an unknown location and dispersed across Homo erectus Africa, southern Asia and southern Europe. 1.6 H. floresiensis originated H. erectus spread to western Asia, then in an unknown location east Asia and Indonesia. Its presence and reached remote in Europe is uncertain, but it gave rise 2.0 parts of Indonesia. to H. antecessor, found in Spain. Wavy branch edges suggest presumed fluctuations in population. PATCHWORK PLANET Most people’s genomes contain remnants of archaic DNA from ancient interbreeding3–6. 2% 2.5% 2.5% 5% Genes* African Unknown archaic African source 98% 97.5% 92.5% Neanderthal Denisovan Stringer 2012 *Figures are approximate, and for Africa, based on limited data6. Sub-Saharan Africa Eurasia and Americas Australia and New Guinea
  • 110. REPORTS Deep Human Genealogies Reveal a tracing back the founding events of new localities. As shown in Fig. 1, the inferred colonization pro- cess is a mixture of long-distance settlements Selective Advantage to Be on an creating an irregular wave front, followed by fur- ther, more progressive, short-range expansions, Expanding Wave Front which then filled gaps and created a more reg- ular wave front. On the basis of the computation of a wave Claudia Moreau,1 Claude Bhérer,1 Hélène Vézina,2 Michèle Jomphe,2 front index (WFI) (21), we find that the ancestors Damian Labuda,1,3* Laurent Excoffier1,4,5* of the Saguenay and the Lac-Saint-Jean people lived more often on or close to the wave front Since their origin, human populations have colonized the whole planet, but the demographic than expected by chance (WFI, P < 0.001 in both processes governing range expansions are mostly unknown. We analyzed the genealogy of more regions) (fig. S1). Indeed, the very high WFI of than one million individuals resulting from a range expansion in Quebec between 1686 and 1960 0.75 observed in Lac-Saint-Jean corresponds to and reconstructed the spatial dynamics of the expansion. We find that a majority of the present a situation in which half of the Lac-Saint-Jean Saguenay Lac-Saint-Jean population can be traced back to ancestors having lived directly on or ancestors had lived directly on the wave front and close to the wave front. Ancestors located on the front contributed significantly more to the current the other half just one generation away from it. gene pool than those from the range core, likely due to a 20% larger effective fertility of women In contrast, WFI is significantly lower in the on the wave front. This fitness component is heritable on the wave front and not in the core, Charlevoix region (P = 0.003) (fig. S1). These Downloaded from www.sciencemag.org on March 24, 2013 implying that this life-history trait evolves during range expansions. results are consistent with different colonization dynamics of SLSJ and Charlevoix. The wave front was always widespread in SLSJ where new M ost species go through environmental- Quebec parish registers that document the recent localities were continuously settled, whereas it was ly induced range expansions or range temporal and spatial expansion of the settle- much smaller in Charlevoix where most localities shifts (1), promoting the evolution of ment of the Charlevoix Saguenay Lac-Saint- remained in the range core until the 20th century traits associated with dispersal and reproduction Jean (ChSLSJ) region, northeast of Quebec City, (Fig. 1). New immigrants from outside ChSLSJ (2). Humans likely colonized the world by a Canada: a prime example of a recent, fast, and constituted an important minority of the people series of range expansions from Africa (3), pos- well-documented range expansion (17) (Fig. 1). getting married, with a greater proportion of im- sibly with episodes of interbreeding with now The European colonization of Quebec was ini- migrants settling on the wave front than on the extinct hominins (4, 5), leading to allele frequen- tiated in 1608 with the foundation of Quebec range core, especially before 1900 (up to 20% on cy and heterozygosity clines from entry points City, and the colony was well established by the the wave front and up to 10% in the range core) into several continents [e.g., (6, 7)]. Range ex- end of the 17th century (18). The peopling of the (table S2). Generally, more male than female im- pansions can also lead to drastic changes in allele Charlevoix region started from Baie-Saint-Paul, migration occurred in all regions, and this bias frequencies, sometimes mimicking the effect of and both a rapid demographic growth and the de- toward males is significantly higher in the core positive selection in recently colonized habitats velopment of the timber industry promoted further than on the wave front (table S3). Nevertheless, (8, 9), through a process called gene surfing (9). expansions after 1838 up the Saguenay River and the new territories of SLSJ have been largely col- Neutral, favorable, or even deleterious mutations the Lac-Saint-Jean region (SLSJ) (19, 20). The onized by people recruited directly on the wave can surf and increase in frequency (10, 11), im- spatial and temporal dynamics of the peopling of front or next to it, not by people from the range plying that wave fronts may harbor mutations the whole ChSLSJ region can be reconstructed by core (table S4). with a wider range of selective coefficients than core populations. The evolutionary consequences of range expansions have been studied in a wide array of species (2, 12), but studies of the dy- namics of range expansions have been generally restricted to species with short generation times Saguenay River (13, 14) or to invasive species (15, 16), because
  • 111. 185.2 16833 106 158.8 49.5 1.17* 112.9 25990 373 69.7 34.4 1.62*** 59.6 REPORTS 35613 1069 33.3 25.4 1.79*** 22.1 27061 1815 14.9 43.2 1.48*** Deep Human Genealogies Reveal a 8.6 10175 2438 4.2 tracing back the founding events of new localities. As shown in Fig. 1, the inferred colonization pro- cess is a mixture of 72.9 long-distance settlements 2.07*** Selective Advantage to Be on an2.9 4.6 25619 8784 49.9 creating an irregular wave front, followed by fur- ther, more progressive, short-range expansions, 1.58*** Expanding 44408 Front 2.3 Wave 26255 1.7 27.7 which then filled gaps and created a more reg- ular wave front. 1.38*** 40846 40.2 On the basis of the computation of a wave Claudia Moreau, Claude Bhérer, Hélène Vézina, Michèle Jomphe,2 1 1 2 front index (WFI) (21), we find that the ancestors SLSJ Damian Labuda,1,3* Laurent Excoffier1,4,5* of the Saguenay and the Lac-Saint-Jean people 7.4 their origin, human populations have colonized the whole planet, but the demographic Since 39 15 2.6 99.6 lived more often on or close to the wave front than expected by chance (WFI, P < 0.001 in both 2.8*** 4.6 governing range 15444 are mostly unknown. We analyzed the genealogy of more processes expansions 4420 3.5 62.3 regions) (fig. S1). Indeed, the very high WFI of 1.3*** than one million individuals resulting from a range expansion in Quebec between 1686 and 1960 0.75 observed in Lac-Saint-Jean corresponds to 2.4reconstructed the spatial dynamics of the expansion. We find that a majority of1.8present and 35777 19726 the 30.9 a situation in which half of the Lac-Saint-Jean 1.3*** Saguenay Lac-Saint-Jean population can be traced back to ancestors having lived directly on or ancestors had lived directly on the wave front and close to the wave front. Ancestors located on the front24161 significantly more to the current contributed 45.1 the other half just one generation away from it. gene pool than those from the range core, likely due to a 20% larger effective fertility of women In contrast, WFI is significantly lower in the on the wave front. This fitness component is heritable on the wave front and not in the core, Charlevoix region (P = 0.003) (fig. S1). These Downloaded from www.sciencemag.org on March 24, 2013 implying that this life-history trait evolves during range expansions. results are consistent with different colonization dynamics of SLSJ and Charlevoix. The wave of genes Table 2. Agethrough environmental- Quebec parish registers of children recent of reproduction and number that document the of women from SLSJ in the period 1840 to 1900. front was always widespread in SLSJ where new M ost species go localities were continuously settled, whereas it was genera- Note ly induced rangetable only includes women expansion of the settle- dates, such that age at marriage can be that this expansions or range temporal and spatial with known birth much smaller in Charlevoix where most localities shifts (1), promoting the evolution of ment of the Charlevoix Saguenay Lac-Saint- remained in the range core until the 20th century 1) for all computed. dispersal and reproduction Jean (ChSLSJ) region, northeast of Quebec City, traits associated with (Fig. 1). New immigrants from outside ChSLSJ between (2). Humans likely colonized the world by a Canada: a prime example of a recent, fast, and series of range expansions from Africa (3), pos- well-documented range expansion (17) (Fig. 1). constituted an important minority of the people getting married, with a greater proportion of im-front and Mean no. of sibly with episodes of interbreeding with now The European colonization of Quebec was ini- migrants settling on the wave front than on the Mean no. of Marriage find that No. of married Mean age at FS ratio EFS ratio extinct hominins (4, 5), leading to allele frequen- tiated in 1608 with the foundation of Quebec range core, especially before 1900 (up to 20% on children cy and heterozygosity clines from entry points City, and the colony was well established by the age ratio the wave front and up to 10% in the range core) ls on the women children marriage WF/RC into several continents [e.g., (6, 7)]. Range ex- end of the 17th century (18). The peopling of the WF/RC (table S2). Generally, more male than female im- (FS) pansions can also lead to drastic changes in allele Charlevoix region started from Baie-Saint-Paul, WF/RC migration occurred in all regions, and this biasore genes (EFS) frequencies, sometimes mimicking the effect of and both a rapid demographic growth and the de- toward males is significantly higher in the core positive selection in recently colonized habitats velopment of the timber industry promoted further than on the wave front (table S3). Nevertheless, e core, in Wave front (WF) 2663 9.1 4.9 (8, 9), through a process called gene surfing (9). expansions after 1838 up the Saguenay River and 20.5 the new territories of SLSJ have been largely col-ng alleles Neutral, favorable, or even deleterious mutations the Lac-Saint-Jean region (SLSJ) (19, 20). The 1.15*** 1.20*** onized by people recruited directly on the wave 0.95*** Range core (RC) 1783 7.9 4.1 can surf and increase in frequency (10, 11), im- spatial and temporal dynamics of the peopling of plying that wave fronts may harbor mutations the whole ChSLSJ region can be reconstructed by 21.6 front or next to it, not by people from the range core (table S4). ng on or with a wider range difference between means; P < 0.001 ***, t test of of selective coefficients than core populations. The evolutionary consequencesd similar of range expansions have been studied in a wide the SLSJ neutral surfing process but also to a net effect of array of species (2, 12), but studies of the dy- namics of range expansions have been generally spatial location of reproduction (front or core)zed more positive selection on the front. restricted to species with short generation times (P < 0.001 for the two effects) but that there is no Saguenay River (13, 14) or to invasive species (15, 16), because
  • 112. What about today?(better: are we still subjected to natural selection?)
  • 113. Natural selection in a contemporaryhuman populationSean G. Byarsa , Douglas Ewbankb , Diddahally R. Govindarajucc,, and Stephen C. Stearnsa,1 a b Diddahally R. Govindaraju and Stephen C. Stearnsa,1aaDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520-8102; bPopulation Studies Center, University of Pennsylvania Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520-8102; bPopulation Studies Center, University of Pennsylvania,Philadelphia, PA 19104-6299; and cDepartment of Neurology, Boston University School of Medicine, Boston, MA 02118-2526Philadelphia, PA 19104-6299; and cDepartment of Neurology, Boston University School of Medicine, Boston, MA 02118-2526Edited by Peter T. Ellison, Harvard University, Cambridge, MA, and approved September 16, 2009 (received for review June 25, 2009) University, Cambridge, MA, and approved September 16, 2009 (received for review June 25, 2009)Our aims were to demonstrate that natural selection is operating natural selection is operating sity to identify factors that contribute to cardiovascular disea sity to identify factors that contribute to cardiovascular disea evolutionary change foron contemporary humans, predict future evolutionary change for It is the longest running multigenerational study in med It is the longest running multigenerational study in medi and show that for somespecific traits with medical significance, and show that for some history. The people originally enrolled in the study were of p history. The people originally enrolled in the study were of ptraits we can make short-term predictions about our future evolu- about our future evolu- dominantly European ancestry (20% United Kingdom, 4 dominantly European ancestry (20% United Kingdom, 40tion. To do so, we measured the strength of selection, estimated of selection, estimated Ireland, 10% Italy, 10% Quebec). The original cohort (n Ireland, 10% Italy, 10% Quebec). The original cohort (ngenetic variation and covariation, and predicted the response to predicted the response to 5,209) has been examined every 2 years, a total of 29 tim 5,209) has been examined every 2 years, a total of 29 tim Heart Study, a project ofselection for women in the Framingham Heart Study, a project of between 1948 and 2008. The offspring cohort (n = 5,124) between 1948 and 2008. The offspring cohort (n = 5,124) h Institute and Boston Univer-the National Heart, Lung, and Blood Institute and Boston Univer- been examined approximately every 4 years, a total of eight tim been examined approximately every 4 years, a total of eight timsity that began in 1948. We found that natural selection is acting natural selection is acting between 1971 and 2008 (4). There is also a third generat between 1971 and 2008 (4). There is also a third generatito cause slow, gradual evolutionary change. The descendants of change. The descendants of cohort (n = 4,095) that is not included in this study because m cohort (n = 4,095) that is not included in this study because ma average slightly shorter andthese women are predicted to be on average slightly shorter and in it have not yet completed reproduction. At each examinat in it have not yet completed reproduction. At each examinati levels and systolic bloodstouter, to have lower total cholesterol levels and systolic blood many physical and blood chemistry traits are measured an many physical and blood chemistry traits are measured andpressure, to have their first child earlier, and to reach menopause and to reach menopause questionnaire is administered, yielding data on >70 traits. D questionnaire is administered, yielding data on >70 traits. Dlater than they would in the absence of evolution. Selection is evolution. Selection is are deidentified by the FHS and delivered to the Natio are deidentified by the FHS and delivered to the Natio period at both ends. Totending to lengthen the reproductive period at both ends. To Institutes of Health dbGaP database, from which we do Institutes of Health dbGaP database, from which we dow changes, the design of plannedbetter understand and predict such changes, the design of planned loaded them for analysis. In this study, we use only the data loaded them for analysis. In this study, we use only the data should include input fromlarge, long-term, multicohort studies should include input from individuals who were measured three or more times. individuals who were measured three or more times.evolutionary biologists. Measuring Selection in a Multicohort Medical Study Measuring Selection in a Multicohort Medical Study | | | sapiens medical traitsevolutionary rates heritability Homo sapiens medical traits Natural selection has been measured many times in natu Natural selection has been measured many times in natu populations of animals and plants (5) using methods inspired populations of animals and plants (5) using methods inspiredA natural selection re contemporary humans experiencing natural selection to that question and evolving in response to it? The answer to that question in the medicaldepends on whom one asks. A long tradition in the medical Robertson (6), developed by Lande and Arnold (7), and refi Robertson (6), developed by Lande and Arnold (7), and refin by Janzen and Stern (8), Hereford et al. (9), and others. To ap by Janzen and Stern (8), Hereford et al. (9), and others. To ap those methods to contemporary human populations requ those methods to contemporary human populations requi not operate oncommunity (1) holds that natural selection does not operate on consideration of several special features of data on huma consideration of several special features of data on huma medicine keepscontemporary human populations because medicine keeps Some, such as cultural variation related to education, smok Some, such as cultural variation related to education, smoki
  • 114. REVIEWSNATURE REVIEWS | GENETICSVOLUME 11 | FEBRUARY 2010 | 137 How culture shaped the human genome: bringing genetics and the human sciences together Kevin N. Laland*, John Odling-Smee‡ and Sean Myles§ || Abstract | Researchers from diverse backgrounds are converging on the view that human evolution has been shaped by gene–culture interactions. Theoretical biologists have used population genetic models to demonstrate that cultural processes can have a profound effect on human evolution, and anthropologists are investigating cultural practices that modify current selection. These findings are supported by recent analyses of human genetic variation, which reveal that hundreds of genes have been subject to recent positive selection, often in response to human activities. Here, we collate these data, highlighting the considerable potential for cross-disciplinary exchange to provide novel insights into how culture has shaped the human genome. Accounts of human evolution frequently assume that adult lactose tolerance12,13,15,16. Estimates for the number the selective events that shaped us were changes in the of human genes that have been subject to recent rapid external environment, stemming from events beyond evolution range from a few hundred to two thousand: human control. For instance, theories of the inception of Williamson et al.14 conclude that up to 10% of the human Homo species emphasize a global trend towards cooler, genome may be affected by linkage to targets of posi- drier climates, which pushed an arboreal ape out of con- tive selection. Although in the majority of cases it is not tracting forests into savannah1. Likewise, heat stress in known what phenotype was the target of the inferred the open is a plausible hypothesis for the evolution of selection, nor which environmental conditions favoured
  • 115. tans maintain normal aero- gories). The XP-EHH (light e profound arterial hypoxia blue) and iHS (dark blue) C EGLN1 D H he existence of changes in selection candidate sets in- system. For example, ele- clude genes in the top 1% REPORTS evels increase vasodilation of the empirical distribu-which, when combined with Genetic Evidence for High-Altitude tions of XP-EHH and iHS re- set of a priori functiona structed a list of Gene13), may increase the avail- sults, respectively, excluding categories (15) associated Adaptation in Tibet ells (4). Collectively, these those with evidence of posi- above (Table 1). We me tive selection in neighboring that Tibetans have adapted Simonson,1 Yingzhong Yang,2* Chad D. Huff,1 Haixia Yun,2* Ga Qin, * * 2 * with those in the Panth Tatum S. poxia response via activa populations (see SOM). The igh-altitude conditions. TheWitherspoon,1 Zhenzhong Bai,2* Felipe R. Lorenzo,3 Jinchuan Xing,1 David J. factor (HIF)” (16), a mdaptation, however, remains intersection of functional can- Lynn B. Jorde,1† Josef T. Prchal,1,3† RiLi Ge2*† lator of oxygen homeo ably associated with high didates with selection can- resulting set of 247 fun Tibetans have didatesvery high altitudes for thousands of years, and they have a distinctive lived at (outlined in black) is listed in table S2. suite of physiological traits that enable them to tolerate environmental hypoxia. These phenotypes enrichedadaptation to this environment, but their genetic basis remains for regions contain- We next identified enetics, University of Utah School the result of are clearly recent positive selection 2 unknown. ing genes that contribute to positive selection in several regions that UT 84112, USA. Research Center We report genome-wide scans that reveal sample of 31 unrelated T e, Qinghai University contain genes local adaptation to hypoxiainin Tibetans.adaptation. Positively selected Medical whose products are likely involved high-altitude The genes in the intersection for one million si typed of functional haplotypes of EGLN1 and PPARA were significantly associated with the decreased hemoglobin0001, People’s Republic of China. that is unique to this highland still exhibit genetic of these genes provides population. (B to D) C phenotype selection candidates population. Identification variability in the phisms (SNPs) using the Human SNP 6.0 Array. T Tibetan and CHB-JPT genomic regions identified in selection scans. evidence of and bo Department of Pathologysupport for previously hypothesized mechanisms of high-altitude adaptation and illuminates the (ARUP), no The top admixtu Medicine and VAH, Salt Lake City, of figure represent chromosome regions in the Tibetan (number of chromosomes complexity hypoxia-response pathways in humans. ulations [see supporting populations (62 randomly drawn chromosomes from 90 individuals), respectively,pin figs. S1 and S2]. To f T he one We used two intersecting criteria to identify selection, we first used gh-Altitude Medicine initiated the Tibetan highlands are (D) of the most genes identified in XPEHH, both scans, and iHS, respectiv extremeEGLN1, and inhabited by hu- genes potentially involved in high-altitude adap- tended haplotype homo environments HMOX2 imarily responsible for phenotyp- mans. Many present-day TibetaniHS and tation: First, ascores (indicated by an asterisk) were desi with the highest popula- XP-EHH priori candidates for adaptation to tistic (18) to make coe should be addressed.who have occupied the Tibetan each genomic region. All haplotypes were genome- toHapMap Chinese (CH tions are thought to be descendants of people high-altitude hypoxia were chosen because of Tibetanhorizontal m haplotype for sorted the highland popul E-mail: Plateau since their known functions (14). Second, a B.J); josef.prchal@hsc.utah.edu based on 7000 and 5000 years wide scan was conducted toto the reference sequence. See fig. the mid-Holocene, between the length of uninterrupted matches identify regions that lowland populations (19 .com (R.L.G.) the remaining seven regions and details about these regions. ago (1), and possibly since the late Pleistocene, show strong evidence of local positive selection assesses haplotype diffe ~21,000 years ago (2, 3). Compared with Andean in high-altitude Tibetans (Fig. 1). To generate a ulations and is designe populations living in similar high-altitude condi- tions, Tibetans exhibit a distinct suite of phys- 2 JULY 2010 arterial 329 SCIENCE www.sciencemag.org iologic traits: decreased VOL oxygen content, Fig. 1. Gene regions respon- A B increased resting ventilation, lack of hypoxic pul- sible for adaptation to high- Functional
  • 116. Infectious disease
  • 117. Infectious disease• “Spanish” Flu pandemic of 1918 killed 1-3% of the world’s population
  • 118. Infectious disease• “Spanish” Flu pandemic of 1918 killed 1-3% of the world’s population• AIDS
  • 119. Infectious disease• “Spanish” Flu pandemic of 1918 killed 1-3% of the world’s population• AIDS• Malaria, Dengue, Typhus...
  • 120. Evolutionary Psychology
  • 121. Evolutionary Psychology
  • 122. Evolutionary Psychology
  • 123. Evolutionary Psychology• Generosity higher if affects reputation
  • 124. Evolutionary Psychology• Generosity higher if affects reputation
  • 125. Evolutionary Psychology• Generosity higher if affects reputation
  • 126. Evolutionary Psychology• Generosity higher if affects reputation• Pheromones help identify our mates
  • 127. Summary• Human evolution is complicated but fascinating! • (just like any other species!!)
  • 128. For more info• http://humanorigins.si.edu/ (Smithonian Institution)• PBS Nova Becoming Human (on youtube)• Stoneking& Krause. Learning about human population history from ancient and modern genomes. Nature Reviews Genetics 2011.• Anything by Robert Trivers
  • 129. Any questions About first lectures?

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