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Human evolution

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Yannick Wurm
Yannick Wurm

March 25th 2013. QMUL SBCS.

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Human evolution
Human evolution
Human evolution Ancestors, relatives & major transitions
Human evolution Ancestors, relatives & major transitions Recent insights from genomics
Human evolution Ancestors, relatives & major transitions Recent insights from genomics What about today?
Benton (2005) Fig 10.47
Relatives and recent ancestors PLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDS SPIDER 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
Relatives and recent ancestors PLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDS SPIDER 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
Proconsul
Rift valley
Relatives and recent ancestors PLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDS SPIDER 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
Relatives and recent ancestors PLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDS SPIDER 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
Major transitions in human evolution
Major transitions in human evolution In which order?
Major transitions in human evolution • Bipedalism (down from the trees) In which order?
Major transitions in human evolution • Bipedalism (down from the trees) • Increased brain size In which order?
Major transitions in human evolution • Bipedalism (down from the trees) • Increased brain size In which order? • Use of simple stone tools
Major transitions in human evolution • Bipedalism (down from the trees) • Increased brain size In which order? • Use of simple stone tools • Fire
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...)
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...
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!
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!
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!
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!
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!
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!
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!
Running
Running • sweating for thermoregulation.
Running • sweating for thermoregulation. • arched foot + achilles tendon
Running • sweating for thermoregulation. • arched foot + achilles tendon • head stabilization
Running • sweating for thermoregulation. • arched foot + achilles tendon • head stabilization • early Homo?
Running • sweating for thermoregulation. • arched foot + achilles tendon • head stabilization • early Homo? • first: improved scavenging.
Running • sweating for thermoregulation. • arched foot + achilles tendon • head stabilization • early Homo? • first: improved scavenging. • then persistence hunting
Relatives and recent ancestors PLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDS SPIDER 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
Most lineages went extinct
Proconsulidae Most lineages went extinct
Proconsulidae Most lineages went extinct
Australopithecines Proconsulidae Most lineages went extinct
H. erectus Australopithecines Proconsulidae Most lineages went extinct
H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
H. neanderthalensis H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
Australopithecines Wikipedia
Taung child 1924 Australopithecus afarensis 2.5 mya
Lucy - Australopithecus afarensis 1978 3.2 mya
Australopithecines 30° 20° 10° 0° 10° 20° 30° 40° 50° 60° 30° 30° Brain size: 35% of modern human 20° 20° A. Bahrelghazali 10° A. Afarensis 10° A. Gahri P. Aethiopicus P. Boisei A. Anamensis 0° 0° 10° 10° 20° P. Robustus (Crassidens) A. Africanus 30° 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°
Evidence for bipedalism in Australopithecines
Evidence for bipedalism in Australopithecines
Evidence for bipedalism in Australopithecines
Evidence for bipedalism in Australopithecines • Pelvis short & broad (like humans), not long & narrow (like gorilla)
Evidence for bipedalism in Australopithecines • Pelvis short & broad (like humans), not long & narrow (like gorilla) • Hip & walking muscles arranged like in a bipedal organism
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
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
Fossilized tracks at Laetoli (Tanzania) Footprints preserved in volcanic ash from: 3 hominids (Australopithecus afarensis) Numerous other mammals
Fossilized tracks at Laetoli (Tanzania) Footprints preserved in volcanic ash from: 3 hominids (Australopithecus afarensis) Numerous other mammals
Tool use?
Tool use? • generally: only simple tools (similarly to current non-human great apes).
Tool use? • generally: only simple tools (similarly to current non-human great apes). • butAustralopithecus garhi (2.5 mya) may have made stone tools.
Summary: Australopithecines • Major group of early bipedal hominids (4mya to 1 mya) • Small brains • Only in Africa • Many forms/species
H. neanderthalensis H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
Homo
Homo habilis
Tool use Chimps and other animals may use objects as tools. H. sapiens! H. habilis! Australopithecine!
Tool use H. habilis made tools Chimps and other animals may use objects as tools. H. sapiens! H. habilis! Australopithecine!
Tool use H. habilis made tools Chimps and other animals may use objects as tools. Cutting H. sapiens! H. habilis! Australopithecine!
Tool use H. habilis made tools Chimps and other animals may use objects as tools. Cutting Scraping H. sapiens! H. habilis! Australopithecine!
Stages of human evolution are defined by the style and sophistication of stone tools…. e.g.: •Oldowan (2.5-1.5 mya) •Achuelian (1.5-0.2 mya)
Oldowan tools Hammerstone Choppers Scraper Flakes
Brain sizes increase
Out of Africa - H. erectus
Homo erectus (Java, 1893)
Acheulian tools Handaxes! Cleaver! Handaxe Pick! Scraper! Trimming flakes!
Nariokotome/Turkana boy H. erectus Found 1984 in Kenya. From1.5mya
H. erectus lifestyle • …language?
H. erectus lifestyle • Stone tools (Acheulian) • …language?
H. erectus lifestyle • Stone tools (Acheulian) • Fire • …language?
H. erectus lifestyle • Stone tools (Acheulian) • Fire • Sociality • …language?
H. erectus lifestyle • Stone tools (Acheulian) • Fire • Sociality • Hunting • …language?
Homo floresiensis “The Hobbit”
Homo floresiensis “The Hobbit” H. florensis vs. H. sapiens skull
Homo floresiensis “The Hobbit” H. florensis vs. H. sapiens skull
Nature (2004) vol. 431, 1043-1044
H. neanderthalensis H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
•
Neanderthal 600,000-30,000 years ago
Burial ritual?
Neanderthals - Summary • Neanderthals were morphologically and genetically distinct from early H. sapiens • disappearedafter H. sapiens arrived - possibly because they were culturally less advanced.
H. neanderthalensis H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
H. sapiens out of Africa
H. sapiens out of Africa • 50,000 years ago: fully “modern” with language, music etc.
H. sapiens out of Africa • 50,000 years ago: fully “modern” with language, music etc. • Began migrating out of Africa 70,000 years ago
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?)
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
Examples of early H. sapiens tools
Lascaux
Recent insights from genomics
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 extracts Richard 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 from Markus Hsi-Yang Fritz,4† Nancy F. Hansen,5† Eric Y. Durand,3† Anna-Sapfo Malaspinas,3† microbial organisms that colonized the specimens Jeffrey 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 for Hernán 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 reaction Eric S. Lander,2 Carsten Russ,2 Nathaniel Novod,2 Jason Affourtit,9 Michael Egholm,9 (PCR) (27). In the case of the nuclear genome of Christine Verna,21 Pavao Rudan,10 Dejana Brajkovic,11 Željko Kucan,10 Ivan Gušic,10 Neandertals, four short gene sequences have been Vladimir B. Doronichev,12 Liubov V. Golovanova,12 Carles Lalueza-Fox,13 Marco de la Rasilla,14 determined by PCR: fragments of the MC1R gene Javier 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 of Daniel 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, 2013 Janet 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 PCR Neandertals, the closest evolutionary relatives of present-day humans, lived in large parts of Europe of ancient DNA can be multiplexed (32), it does and 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 the genome 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 of We 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 for T 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 Biology Progressively 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, MD ago (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, Department as far east as Southern Siberia (5) and as far falls outside the variation found in present-day of Genome Sciences, University of Washington, Seattle, WA south as the Middle East. During that time, Nean- humans and thus provides no evidence for inter- 98195, USA. 8Division of Biological Sciences, University of
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 extracts Richard 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 from Markus Hsi-Yang Fritz,4† Nancy F. Hansen,5† Eric Y. Durand,3† Anna-Sapfo Malaspinas,3† microbial organisms that colonized the specimens Jeffrey 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 for Hernán 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 reaction Eric S. Lander,2 Carsten Russ,2 Nathaniel Novod,2 Jason Affourtit,9 Michael Egholm,9 (PCR) (27). In the case of the nuclear genome of Christine Verna,21 Pavao Rudan,10 Dejana Brajkovic,11 Željko Kucan,10 Ivan Gušic,10 Neandertals, four short gene sequences have been Vladimir B. Doronichev,12 Liubov V. Golovanova,12 Carles Lalueza-Fox,13 Marco de la Rasilla,14 determined by PCR: fragments of the MC1R gene Javier 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 of Daniel 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, 2013 Janet 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 PCR Neandertals, the closest evolutionary relatives of present-day humans, lived in large parts of Europe of ancient DNA can be multiplexed (32), it does and 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 the genome 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 of We 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 for T 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 Biology Progressively 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, MD ago (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, Department as far east as Southern Siberia (5) and as far falls outside the variation found in present-day of Genome Sciences, University of Washington, Seattle, WA south as the Middle East. During that time, Nean- humans and thus provides no evidence for inter- 98195, USA. 8Division of Biological Sciences, University of
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 extracts Richard 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 from Markus Hsi-Yang Fritz,4† Nancy F. Hansen,5† Eric Y. Durand,3† Anna-Sapfo Malaspinas,3† microbial organisms that colonized the specimens Jeffrey 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 for Hernán 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 reaction Eric S. Lander,2 Carsten Russ,2 Nathaniel Novod,2 Jason Affourtit,9 Michael Egholm,9 (PCR) (27). In the case of the nuclear genome of Christine Verna,21 Pavao Rudan,10 Dejana Brajkovic,11 Željko Kucan,10 Ivan Gušic,10 Neandertals, four short gene sequences have been Vladimir B. Doronichev,12 Liubov V. Golovanova,12 Carles Lalueza-Fox,13 Marco de la Rasilla,14 determined by PCR: fragments of the MC1R gene Javier 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 of Daniel 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, 2013 Janet 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 PCR Neandertals, the closest evolutionary relatives of present-day humans, lived in large parts of Europe of ancient DNA can be multiplexed (32), it does and 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 the genome 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 of We 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 for T 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 Biology Progressively 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, MD ago (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, Department as far east as Southern Siberia (5) and as far falls outside the variation found in present-day of Genome Sciences, University of Washington, Seattle, WA south as the Middle East. During that time, Nean- humans and thus provides no evidence for inter- 98195, USA. 8Division of Biological Sciences, University of
Strong reproductive isolation between human Strong reproductive isolation between humans and Neanderthals inferred from observed Neanderthals inferred from observed patterns of introgression patterns of introgression Mathias Currata,1 and Laurent Excoffierb,c,1 Mathias Currata,1 and Laurent Excoffierb,c,1 a a 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 o 1227 Geneva, Switzerland; bComputational and Molecular Population Genetics Laboratory, Institute Ecology and Evolution, Univers 1227 Geneva, Switzerland; bComputational and Molecular Population Genetics Laboratory, Institute of of Ecology and Evolution, Uni 3012 Berne, Switzerland; and cSwiss Institute of Bioinformatics, 1015 Lausanne, Switzerland 3012 Berne, Switzerland; and cSwiss Institute of Bioinformatics, 1015 Lausanne, Switzerland Edited by Svante Pääbo, Max Planck Institute of Evolutionary Anthropology, Leipzig, Germany, and approved August 3, 2011 (rece Edited by Svante Pääbo, Max Planck Institute of Evolutionary Anthropology, Leipzig, Germany, and approved August 3, 2011 (receive May 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 pro Africans might come from Neanderthals, suggesting a a more complex Africans 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. InIn scenario of modern human evolution than previously anticipated. istic and spatially explicit model of of admixt istic and spatially explicit model admixture this paper, we use a model of admixture during a a spatial expansion this paper, we use a model of admixture during spatial expansion between modern humans and Neanderthals (3 between modern humans and Neanderthals to study the hybridization of Neanderthals with modern humans to study the hybridization of Neanderthals with modern humans simulations, we have estimated the interbree simulations, we have estimated the interb during their spread out of Africa. We find that observed low levels during 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 a of Neanderthal ancestry in Eurasians are compatible with a a very low of Neanderthal ancestry in Eurasians are compatible with very low hybridization that is is compatible with the o hybridization that compatible with the obs rate of interbreeding (<2%), potentially attributable to a a very strong rate 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 ky These results suggesting the presence of very effective barriers toto These results suggesting the presence of very effective barriers gene flow between the two species are robust to uncertainties about gene flow between the two species are robust to uncertainties about Results Results the exact demography of the Paleolithic populations, and they are Low Rates of of Interbreeding Between Huma the exact demography of the Paleolithic populations, and they are Low Rates Interbreeding Between Humans also found to be compatible with the observed lack of mtDNA in- Using spatially explicit simulations, wewe also found to be compatible with the observed lack of mtDNA in- trogression. Our model additionally suggests that similarly low levels Using spatially explicit simulations, hav trogression. Our model additionally suggests that similarly low levels expected amount of of Neanderthal ancestry pr expected amount Neanderthal ancestry in in of 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) forfo ture 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 var Europeans and Asians. This hypothesis could be tested because it it derthal ranges (Fig. 1).1). Under our model Europeans and Asians. This hypothesis could be tested because predicts that different components of Neanderthal ancestry should derthal ranges (Fig. Under our model of predicts that different components of Neanderthal ancestry should range expansion, we find that observed low leve range expansion, we find that observed low l be present in Europeans and in Asians. be present in Europeans and in Asians. introgression into Eurasians imply the existe
Denisovans
Denisovans • Only known remains(all found since 2010): phalanx (finger bone), three teeth, a toe bone. From 41,000 years ago.
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.
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
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.
H. neanderthalensis H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
H. neanderthalensis H. sapiens Denisovan H. erectus Australopithecines Proconsulidae Most lineages went extinct
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 correla Stoneking & Krause 2011 in a populat ulation from
A WINDING PATH H. sapiens spread from Africa to After early modern humans left Africa around 60,000 years ago (top western Asia and then to Europe and right), they spread across the globe and interbred with other southern Asia, eventually reaching descendants of Homo heidelbergensis. Australasia and the Americas. 0 Homo sapiens Homo floresiensis Denisovans Neanderthals Homo erectus 0.4 Homo heidelbergensis Million 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
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
Human evolution
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Human evolution

  • 1.
  • 5. Human evolution Ancestors, relatives & major transitions Recent insights from genomics
  • 6. Human evolution Ancestors, relatives & major transitions Recent insights from genomics What about today?
  • 7. Benton (2005) Fig 10.47
  • 8. Relatives and recent ancestors PLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDS SPIDER 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. Relatives and recent ancestors PLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDS SPIDER 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 ancestors PLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDS SPIDER 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. Relatives and recent ancestors PLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDS SPIDER 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
  • 14. Major transitions in human evolution
  • 15. Major transitions in human evolution In which order?
  • 16. Major transitions in human evolution • Bipedalism (down from the trees) In which order?
  • 17. Major transitions in human evolution • Bipedalism (down from the trees) • Increased brain size In which order?
  • 18. Major transitions in human evolution • Bipedalism (down from the trees) • Increased brain size In which order? • Use of simple stone tools
  • 19. Major transitions in human evolution • Bipedalism (down from the trees) • Increased brain size In which order? • Use of simple stone tools • Fire
  • 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...)
  • 21. 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...
  • 22. 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!
  • 23. 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!
  • 24. 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!
  • 25. 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!
  • 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! 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! Ardipithecus ramidus! Antarctic icecap! Orrorin tugenensis! Cold! Warm! Climate!
  • 28. 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!
  • 30. Running • sweating for thermoregulation.
  • 31. Running • sweating for thermoregulation. • arched foot + achilles tendon
  • 32. Running • sweating for thermoregulation. • arched foot + achilles tendon • head stabilization
  • 33. Running • sweating for thermoregulation. • arched foot + achilles tendon • head stabilization • early Homo?
  • 34. Running • sweating for thermoregulation. • arched foot + achilles tendon • head stabilization • early Homo? • first: improved scavenging.
  • 35. Running • sweating for thermoregulation. • arched foot + achilles tendon • head stabilization • early Homo? • first: improved scavenging. • then persistence hunting
  • 36.
  • 37. Relatives and recent ancestors PLATYRRHINI CATARRHINI CERCOPITHECOIDS HOMINOIDS HYLOBATIDS HOMINIDS SPIDER 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
  • 39. Proconsulidae Most lineages went extinct
  • 40. Proconsulidae Most lineages went extinct
  • 41. Australopithecines Proconsulidae Most lineages went extinct
  • 42. H. erectus Australopithecines Proconsulidae Most lineages went extinct
  • 43. H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
  • 44. H. neanderthalensis H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
  • 45.
  • 47. Taung child 1924 Australopithecus afarensis 2.5 mya
  • 48. Lucy - Australopithecus afarensis 1978 3.2 mya
  • 49. Australopithecines 30° 20° 10° 0° 10° 20° 30° 40° 50° 60° 30° 30° Brain size: 35% of modern human 20° 20° A. Bahrelghazali 10° A. Afarensis 10° A. Gahri P. Aethiopicus P. Boisei A. Anamensis 0° 0° 10° 10° 20° P. Robustus (Crassidens) A. Africanus 30° 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°
  • 50.
  • 51. Evidence for bipedalism in Australopithecines
  • 52. Evidence for bipedalism in Australopithecines
  • 53. Evidence for bipedalism in Australopithecines
  • 54. Evidence for bipedalism in Australopithecines • Pelvis short & broad (like humans), not long & narrow (like gorilla)
  • 55. Evidence for bipedalism in Australopithecines • Pelvis short & broad (like humans), not long & narrow (like gorilla) • Hip & walking muscles arranged like in a bipedal organism
  • 56. 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
  • 57. 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
  • 58. Fossilized tracks at Laetoli (Tanzania) Footprints preserved in volcanic ash from: 3 hominids (Australopithecus afarensis) Numerous other mammals
  • 59. Fossilized tracks at Laetoli (Tanzania) Footprints preserved in volcanic ash from: 3 hominids (Australopithecus afarensis) Numerous other mammals
  • 61. Tool use? • generally: only simple tools (similarly to current non-human great apes).
  • 62. Tool use? • generally: only simple tools (similarly to current non-human great apes). • butAustralopithecus garhi (2.5 mya) may have made stone tools.
  • 63. Summary: Australopithecines • Major group of early bipedal hominids (4mya to 1 mya) • Small brains • Only in Africa • Many forms/species
  • 64.
  • 65. H. neanderthalensis H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
  • 66. Homo
  • 68. Tool use Chimps and other animals may use objects as tools. H. sapiens! H. habilis! Australopithecine!
  • 69. Tool use H. habilis made tools Chimps and other animals may use objects as tools. H. sapiens! H. habilis! Australopithecine!
  • 70. Tool use H. habilis made tools Chimps and other animals may use objects as tools. Cutting H. sapiens! H. habilis! Australopithecine!
  • 71. Tool use H. habilis made tools Chimps and other animals may use objects as tools. Cutting Scraping H. sapiens! H. habilis! Australopithecine!
  • 72. Stages of human evolution are defined by the style and sophistication of stone tools…. e.g.: •Oldowan (2.5-1.5 mya) •Achuelian (1.5-0.2 mya)
  • 73. Oldowan tools Hammerstone Choppers Scraper Flakes
  • 75.
  • 76. Out of Africa - H. erectus
  • 78. Acheulian tools Handaxes! Cleaver! Handaxe Pick! Scraper! Trimming flakes!
  • 79. Nariokotome/Turkana boy H. erectus Found 1984 in Kenya. From1.5mya
  • 80. H. erectus lifestyle • …language?
  • 81. H. erectus lifestyle • Stone tools (Acheulian) • …language?
  • 82. H. erectus lifestyle • Stone tools (Acheulian) • Fire • …language?
  • 83. H. erectus lifestyle • Stone tools (Acheulian) • Fire • Sociality • …language?
  • 84. H. erectus lifestyle • Stone tools (Acheulian) • Fire • Sociality • Hunting • …language?
  • 85.
  • 87. Homo floresiensis “The Hobbit” H. florensis vs. H. sapiens skull
  • 88. Homo floresiensis “The Hobbit” H. florensis vs. H. sapiens skull
  • 89. Nature (2004) vol. 431, 1043-1044
  • 90.
  • 91. H. neanderthalensis H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
  • 92. •
  • 93. Neanderthal 600,000-30,000 years ago
  • 94.
  • 96. Neanderthals - Summary • Neanderthals were morphologically and genetically distinct from early H. sapiens • disappearedafter H. sapiens arrived - possibly because they were culturally less advanced.
  • 97. H. neanderthalensis H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
  • 98. H. sapiens out of Africa
  • 99. H. sapiens out of Africa • 50,000 years ago: fully “modern” with language, music etc.
  • 100. H. sapiens out of Africa • 50,000 years ago: fully “modern” with language, music etc. • Began migrating out of Africa 70,000 years ago
  • 101. 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?)
  • 102.
  • 103. 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
  • 104. Examples of early H. sapiens tools
  • 106.
  • 107. Recent insights from genomics
  • 108. 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 extracts Richard 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 from Markus Hsi-Yang Fritz,4† Nancy F. Hansen,5† Eric Y. Durand,3† Anna-Sapfo Malaspinas,3† microbial organisms that colonized the specimens Jeffrey 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 for Hernán 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 reaction Eric S. Lander,2 Carsten Russ,2 Nathaniel Novod,2 Jason Affourtit,9 Michael Egholm,9 (PCR) (27). In the case of the nuclear genome of Christine Verna,21 Pavao Rudan,10 Dejana Brajkovic,11 Željko Kucan,10 Ivan Gušic,10 Neandertals, four short gene sequences have been Vladimir B. Doronichev,12 Liubov V. Golovanova,12 Carles Lalueza-Fox,13 Marco de la Rasilla,14 determined by PCR: fragments of the MC1R gene Javier 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 of Daniel 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, 2013 Janet 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 PCR Neandertals, the closest evolutionary relatives of present-day humans, lived in large parts of Europe of ancient DNA can be multiplexed (32), it does and 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 the genome 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 of We 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 for T 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 Biology Progressively 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, MD ago (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, Department as far east as Southern Siberia (5) and as far falls outside the variation found in present-day of Genome Sciences, University of Washington, Seattle, WA south as the Middle East. During that time, Nean- humans and thus provides no evidence for inter- 98195, USA. 8Division of Biological Sciences, University of
  • 109. 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 extracts Richard 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 from Markus Hsi-Yang Fritz,4† Nancy F. Hansen,5† Eric Y. Durand,3† Anna-Sapfo Malaspinas,3† microbial organisms that colonized the specimens Jeffrey 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 for Hernán 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 reaction Eric S. Lander,2 Carsten Russ,2 Nathaniel Novod,2 Jason Affourtit,9 Michael Egholm,9 (PCR) (27). In the case of the nuclear genome of Christine Verna,21 Pavao Rudan,10 Dejana Brajkovic,11 Željko Kucan,10 Ivan Gušic,10 Neandertals, four short gene sequences have been Vladimir B. Doronichev,12 Liubov V. Golovanova,12 Carles Lalueza-Fox,13 Marco de la Rasilla,14 determined by PCR: fragments of the MC1R gene Javier 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 of Daniel 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, 2013 Janet 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 PCR Neandertals, the closest evolutionary relatives of present-day humans, lived in large parts of Europe of ancient DNA can be multiplexed (32), it does and 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 the genome 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 of We 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 for T 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 Biology Progressively 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, MD ago (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, Department as far east as Southern Siberia (5) and as far falls outside the variation found in present-day of Genome Sciences, University of Washington, Seattle, WA south as the Middle East. During that time, Nean- humans and thus provides no evidence for inter- 98195, USA. 8Division of Biological Sciences, University of
  • 110. 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 extracts Richard 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 from Markus Hsi-Yang Fritz,4† Nancy F. Hansen,5† Eric Y. Durand,3† Anna-Sapfo Malaspinas,3† microbial organisms that colonized the specimens Jeffrey 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 for Hernán 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 reaction Eric S. Lander,2 Carsten Russ,2 Nathaniel Novod,2 Jason Affourtit,9 Michael Egholm,9 (PCR) (27). In the case of the nuclear genome of Christine Verna,21 Pavao Rudan,10 Dejana Brajkovic,11 Željko Kucan,10 Ivan Gušic,10 Neandertals, four short gene sequences have been Vladimir B. Doronichev,12 Liubov V. Golovanova,12 Carles Lalueza-Fox,13 Marco de la Rasilla,14 determined by PCR: fragments of the MC1R gene Javier 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 of Daniel 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, 2013 Janet 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 PCR Neandertals, the closest evolutionary relatives of present-day humans, lived in large parts of Europe of ancient DNA can be multiplexed (32), it does and 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 the genome 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 of We 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 for T 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 Biology Progressively 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, MD ago (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, Department as far east as Southern Siberia (5) and as far falls outside the variation found in present-day of Genome Sciences, University of Washington, Seattle, WA south as the Middle East. During that time, Nean- humans and thus provides no evidence for inter- 98195, USA. 8Division of Biological Sciences, University of
  • 111. Strong reproductive isolation between human Strong reproductive isolation between humans and Neanderthals inferred from observed Neanderthals inferred from observed patterns of introgression patterns of introgression Mathias Currata,1 and Laurent Excoffierb,c,1 Mathias Currata,1 and Laurent Excoffierb,c,1 a a 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 o 1227 Geneva, Switzerland; bComputational and Molecular Population Genetics Laboratory, Institute Ecology and Evolution, Univers 1227 Geneva, Switzerland; bComputational and Molecular Population Genetics Laboratory, Institute of of Ecology and Evolution, Uni 3012 Berne, Switzerland; and cSwiss Institute of Bioinformatics, 1015 Lausanne, Switzerland 3012 Berne, Switzerland; and cSwiss Institute of Bioinformatics, 1015 Lausanne, Switzerland Edited by Svante Pääbo, Max Planck Institute of Evolutionary Anthropology, Leipzig, Germany, and approved August 3, 2011 (rece Edited by Svante Pääbo, Max Planck Institute of Evolutionary Anthropology, Leipzig, Germany, and approved August 3, 2011 (receive May 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 pro Africans might come from Neanderthals, suggesting a a more complex Africans 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. InIn scenario of modern human evolution than previously anticipated. istic and spatially explicit model of of admixt istic and spatially explicit model admixture this paper, we use a model of admixture during a a spatial expansion this paper, we use a model of admixture during spatial expansion between modern humans and Neanderthals (3 between modern humans and Neanderthals to study the hybridization of Neanderthals with modern humans to study the hybridization of Neanderthals with modern humans simulations, we have estimated the interbree simulations, we have estimated the interb during their spread out of Africa. We find that observed low levels during 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 a of Neanderthal ancestry in Eurasians are compatible with a a very low of Neanderthal ancestry in Eurasians are compatible with very low hybridization that is is compatible with the o hybridization that compatible with the obs rate of interbreeding (<2%), potentially attributable to a a very strong rate 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 ky These results suggesting the presence of very effective barriers toto These results suggesting the presence of very effective barriers gene flow between the two species are robust to uncertainties about gene flow between the two species are robust to uncertainties about Results Results the exact demography of the Paleolithic populations, and they are Low Rates of of Interbreeding Between Huma the exact demography of the Paleolithic populations, and they are Low Rates Interbreeding Between Humans also found to be compatible with the observed lack of mtDNA in- Using spatially explicit simulations, wewe also found to be compatible with the observed lack of mtDNA in- trogression. Our model additionally suggests that similarly low levels Using spatially explicit simulations, hav trogression. Our model additionally suggests that similarly low levels expected amount of of Neanderthal ancestry pr expected amount Neanderthal ancestry in in of 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) forfo ture 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 var Europeans and Asians. This hypothesis could be tested because it it derthal ranges (Fig. 1).1). Under our model Europeans and Asians. This hypothesis could be tested because predicts that different components of Neanderthal ancestry should derthal ranges (Fig. Under our model of predicts that different components of Neanderthal ancestry should range expansion, we find that observed low leve range expansion, we find that observed low l be present in Europeans and in Asians. be present in Europeans and in Asians. introgression into Eurasians imply the existe
  • 113. Denisovans • Only known remains(all found since 2010): phalanx (finger bone), three teeth, a toe bone. From 41,000 years ago.
  • 114. 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.
  • 115. 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
  • 116. 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.
  • 117. H. neanderthalensis H. sapiens H. erectus Australopithecines Proconsulidae Most lineages went extinct
  • 118. H. neanderthalensis H. sapiens Denisovan H. erectus Australopithecines Proconsulidae Most lineages went extinct
  • 119. 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 correla Stoneking & Krause 2011 in a populat ulation from
  • 120. A WINDING PATH H. sapiens spread from Africa to After early modern humans left Africa around 60,000 years ago (top western Asia and then to Europe and right), they spread across the globe and interbred with other southern Asia, eventually reaching descendants of Homo heidelbergensis. Australasia and the Americas. 0 Homo sapiens Homo floresiensis Denisovans Neanderthals Homo erectus 0.4 Homo heidelbergensis Million 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
  • 121. 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