How to build a Neandertal Jean-Jacques Hublin Science 344, 1338 (2014); DOI: 10.1126/science.1255554
This copy is for your personal, non-commercial use only.
Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here. The following resources related to this article are available online at www.sciencemag.org (this information is current as of June 19, 2014 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/content/344/6190/1338.full.html A list of selected additional articles on the Science Web sites related to this article can be found at: http://www.sciencemag.org/content/344/6190/1338.full.html#related This article cites 12 articles, 3 of which can be accessed free: http://www.sciencemag.org/content/344/6190/1338.full.html#ref-list-1
Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2014 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS.
Downloaded from www.sciencemag.org on June 19, 2014
If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here.
Understanding nanocrystal surfaces p. 1340
INSIGHTS
Crows challenge species concepts p. 1345
Morphological divergence. The skulls of a modern human (Cro-Magnon 1, far left) and a Neandertal (La Ferrassie 1, center left) show the morphological divergence between the two hominin species 500,000 to 600,000 years after their ancestral populations split. In contrast, after about 2 million years of separation, common chimpanzees (center right) and bonobos (far right) still display very similar morphologies, likely owing to strong stabilizing selection.
ANTHROPOLOGY
How to build a Neandertal Fossils from Sima de los Huesos show a mixture of Neandertal and more ancient features By Jean-Jacques Hublin
U
nder a desolate sierra of northern Spain, in the darkness of a deep shaft, lies the largest accumulation of hominin fossils ever found. On page 1358 of this issue, Arsuaga et al. (1) date this paleontological treasure at the Sima de los Huesos (see the photo) and shed new light on one of the most impassioned issues in the field of human evolution: How did Neandertals evolve? Four to five hundred thousand years ago, archaic humans in western Eurasia diverged from other groups of that period in Africa and eastern Asia. Their skull, jaw, and teeth began to display features that characterize later Neandertals. When modern humans— 1338
which had evolved in Africa—finally colonized Eurasia 50,000 years ago, they occasionally interbred with local Neandertals, but the two groups already showed some signs of reproductive incompatibility (2). The extent of their morphological divergence over such a short period of time is striking (see the figure). Polar bears and brown bears provide another example of rapid divergence over a few hundred thousand years (3). However, other sister species have stayed quite similar for much longer periods of time (see the figure), and among mid-sized mammals, complete reproductive isolation generally takes at least 1.4 million years to develop (4). Why did the Neandertals differentiate so quickly? Isolation and genetic drift likely played a key role (5, 6). Archaic Europeans
already dwelled, at least sporadically, at the edge of the boreal zone 850,000 years ago (7), but 200,000 years later, a major glaciation dramatically reduced their habitable domain. Since this time, extreme climatic conditions prevailed roughly every 100,000 years within the European cul-de-sac. The time period of the Sima de los Huesos population (~430,000 years ago) coincides with the onset of a long interglacial period that followed a severe glacial episode. Hominin groups dispersed again into higher latitudes. However, in areas like modern-day Germany and the British Isles, human occupations remained scarce and discontinuous, with periodic demographic crashes during subsequent climatic cycles. Paleogenetic data (8) confirm that Neandertal populations were small and sciencemag.org SCIENCE
20 JUNE 2014 • VOL 344 ISSUE 6190
Published by AAAS
FIGURE CREDIT: FOSSIL SKULLS AND CHIMPANZEE/J.-J. HUBLIN; BONOBO/ROYAL MUSEUM FOR CENTRAL AFRICA, TERVUREN, BELGIUM
PERSPECTIVES
generally isolated from one another, with very low genetic diversity. These conditions are the most favorable to the rapid and random fixation of features by genetic drift Obtaining an accurate picture of the European populations around 400,000 years ago remains challenging. The Sima de los Huesos stands alone with its 28 very complete individuals. At most other sites, isolated fragments make it impossible to assess local variability; accurate dating is also
Sima de los Huesos population is close in age to the split of the two Eurasian lineages. Because mitochondrial DNA does not recombine at each generation, an ancient lineage could have survived in the Denisovans but got lost in the Neandertals along successive genetic bottlenecks. Arsuaga et al. confirm that Neandertal features did not evolve as a block but rather were fixed at different rates and paces in different parts of the anatomy (5). In the
PHOTO: JAVIER TRUEBA/MADRID SCIENTIFIC FILMS
A treasure trove of hominin fossils. At the Sima de los Huesos (bone pit) in the Atapuerca Mountains in northern Spain, the remains of 28 hominins have been recovered. Arsuaga et al. date these fossils to around 430,000 years ago and show that they have Neandertal facial and dental features together with more primitive braincases.
often difficult. Still, the existing evidence suggests that at this early stage of the Neandertal lineage, European populations differed in their combinations of Neandertal and primitive traits. As Arsuaga et al. show, the Sima de los Huesos series displays an almost full set of Neandertal dental features. These features are less frequent at other sites of comparable age (9) and became ubiquitous in western Eurasia only after further pruning of the western European archaic populations. Repeated local extinctions may also explain the occurrence at the Sima de los Huesos of mitochondrial DNA similar to that sequenced in the Denisovans (10), an archaic group that diverged from the Neandertal lineage after its separation from the African groups and that peopled most of Asia. The Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig, 04103 Germany. E-mail: [email protected]
Sima de los Huesos fossils, Neandertal conditions are mostly evident in the face and teeth, whereas the braincase still retains primitive conditions. The fact is that one does not find Neandertal braincase shapes in Europe before ~200,000 years ago. Comparing brain sizes in late Neandertals and in the Sima de los Huesos hominins, Arsuaga et al. also document a substantial increase of the encephalic volume along this evolutionary branch. An independent increase in brain volume also took place along the African branch leading to modern humans, as well as in the late Homo erectus of East Asia. Hominins rely on technology and social complexity, and it is therefore not surprising to observe such parallel evolutions, because similar pressures of selection were at work in all of these lineages. However, their separation for several hundred thousand years resulted in different evolutionary pathways to achieve bigger brains. Neandertal and
SCIENCE sciencemag.org
modern brains are anatomically different. The former display a smaller cerebellum, less projecting parietal areas, smaller olfactory bulbs and temporal lobe poles, and a narrower orbitofrontal cortex (11). Furthermore, there is clear evidence that the growth pattern of modern human brains deviates from that of the Neandertals. In modern humans, parietal areas and cerebellum expand in early infancy, at a crucial stage for the establishment of cognitive skills (12). The different pathways for brain evolution are also perceptible in the DNA of both groups. Among the 87 genes that distinguish modern humans from Neandertals, a whole series are involved in brain function or development, particularly in its connectivity (13). Some of these genes belong to the most conservative part of the primate genome. They remained protected by stabilizing selection through millions of years of evolution before mutating along the modern human lineage. Although genes involved in behavior seem to have changed more in the modern human lineage than along the Neandertal line (8), it is difficult to say what this means for their phenotypic expression. The paleolithic archaeological record can yield a wealth of information regarding stone technologies or food procurement, but remains mute on key aspects of human behaviors, such as mating strategies, aggression, or large-scale cooperation. There is, however, no doubt that after more than half a million years of separate evolution, idiosyncratic features that developed in modern human groups played a key role in the almost complete replacement not only of the Neandertals but of all other archaic humans whom they met during their expansion out of Africa. ■ REF ERENCES AND NOTES
1. 2. 3. 4.
5. 6. 7. 8. 9.
10. 11. 12. 13.
J. L. Arsuaga et al., Science 344, 1358 (2014). S. Sankararaman et al., Nature 507, 354 (2014). S. Liu et al., Cell 157, 785 (2014). T. W. Holliday, in Neanderthals Revisited: New Approaches and Perspectives, K. Harvati, T. Harrison, Eds. (Springer, New York, 2006), pp. 281–298. J.-J. Hublin, Proc. Natl. Acad. Sci. U.S.A. 106, 16022 (2009). T. D. Weaver, C. C. Roseman, C. B. Stringer, J. Hum. Evol. 53, 135 (2007). S. A. Parfitt et al., Nature 466, 229 (2010). S. Castellano et al., Proc. Natl. Acad. Sci. U.S.A. 111, 6666 (2014). M. Martinón-Torres, J. M. Bermúdez de Castro, A. GómezRobles, L. Prado-Simón, J. L. Arsuaga, J. Hum. Evol. 62, 7 (2012). M. Meyer et al., Nature 505, 403 (2014). M. Bastir et al., Nat. Commun. 2, 588 (2011). P. Gunz et al., J. Hum. Evol. 62, 300 (2012). K. Prüfer et al., Nature 505, 43 (2014).
ACKNOWL EDGMENTS
I thank the Museum National d’Histoire Naturelle, Paris, for allowing the computed-tomography of the fossil skulls used here as an illustration. 10.1126/science.1255554 20 JUNE 2014 • VOL 344 ISSUE 6190
Published by AAAS
1339
This copy is for your personal, non-commercial use only.
Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here. The following resources related to this article are available online at www.sciencemag.org (this information is current as of June 19, 2014 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/content/344/6190/1338.full.html A list of selected additional articles on the Science Web sites related to this article can be found at: http://www.sciencemag.org/content/344/6190/1338.full.html#related This article cites 12 articles, 3 of which can be accessed free: http://www.sciencemag.org/content/344/6190/1338.full.html#ref-list-1
Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2014 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS.
Downloaded from www.sciencemag.org on June 19, 2014
If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here.
Understanding nanocrystal surfaces p. 1340
INSIGHTS
Crows challenge species concepts p. 1345
Morphological divergence. The skulls of a modern human (Cro-Magnon 1, far left) and a Neandertal (La Ferrassie 1, center left) show the morphological divergence between the two hominin species 500,000 to 600,000 years after their ancestral populations split. In contrast, after about 2 million years of separation, common chimpanzees (center right) and bonobos (far right) still display very similar morphologies, likely owing to strong stabilizing selection.
ANTHROPOLOGY
How to build a Neandertal Fossils from Sima de los Huesos show a mixture of Neandertal and more ancient features By Jean-Jacques Hublin
U
nder a desolate sierra of northern Spain, in the darkness of a deep shaft, lies the largest accumulation of hominin fossils ever found. On page 1358 of this issue, Arsuaga et al. (1) date this paleontological treasure at the Sima de los Huesos (see the photo) and shed new light on one of the most impassioned issues in the field of human evolution: How did Neandertals evolve? Four to five hundred thousand years ago, archaic humans in western Eurasia diverged from other groups of that period in Africa and eastern Asia. Their skull, jaw, and teeth began to display features that characterize later Neandertals. When modern humans— 1338
which had evolved in Africa—finally colonized Eurasia 50,000 years ago, they occasionally interbred with local Neandertals, but the two groups already showed some signs of reproductive incompatibility (2). The extent of their morphological divergence over such a short period of time is striking (see the figure). Polar bears and brown bears provide another example of rapid divergence over a few hundred thousand years (3). However, other sister species have stayed quite similar for much longer periods of time (see the figure), and among mid-sized mammals, complete reproductive isolation generally takes at least 1.4 million years to develop (4). Why did the Neandertals differentiate so quickly? Isolation and genetic drift likely played a key role (5, 6). Archaic Europeans
already dwelled, at least sporadically, at the edge of the boreal zone 850,000 years ago (7), but 200,000 years later, a major glaciation dramatically reduced their habitable domain. Since this time, extreme climatic conditions prevailed roughly every 100,000 years within the European cul-de-sac. The time period of the Sima de los Huesos population (~430,000 years ago) coincides with the onset of a long interglacial period that followed a severe glacial episode. Hominin groups dispersed again into higher latitudes. However, in areas like modern-day Germany and the British Isles, human occupations remained scarce and discontinuous, with periodic demographic crashes during subsequent climatic cycles. Paleogenetic data (8) confirm that Neandertal populations were small and sciencemag.org SCIENCE
20 JUNE 2014 • VOL 344 ISSUE 6190
Published by AAAS
FIGURE CREDIT: FOSSIL SKULLS AND CHIMPANZEE/J.-J. HUBLIN; BONOBO/ROYAL MUSEUM FOR CENTRAL AFRICA, TERVUREN, BELGIUM
PERSPECTIVES
generally isolated from one another, with very low genetic diversity. These conditions are the most favorable to the rapid and random fixation of features by genetic drift Obtaining an accurate picture of the European populations around 400,000 years ago remains challenging. The Sima de los Huesos stands alone with its 28 very complete individuals. At most other sites, isolated fragments make it impossible to assess local variability; accurate dating is also
Sima de los Huesos population is close in age to the split of the two Eurasian lineages. Because mitochondrial DNA does not recombine at each generation, an ancient lineage could have survived in the Denisovans but got lost in the Neandertals along successive genetic bottlenecks. Arsuaga et al. confirm that Neandertal features did not evolve as a block but rather were fixed at different rates and paces in different parts of the anatomy (5). In the
PHOTO: JAVIER TRUEBA/MADRID SCIENTIFIC FILMS
A treasure trove of hominin fossils. At the Sima de los Huesos (bone pit) in the Atapuerca Mountains in northern Spain, the remains of 28 hominins have been recovered. Arsuaga et al. date these fossils to around 430,000 years ago and show that they have Neandertal facial and dental features together with more primitive braincases.
often difficult. Still, the existing evidence suggests that at this early stage of the Neandertal lineage, European populations differed in their combinations of Neandertal and primitive traits. As Arsuaga et al. show, the Sima de los Huesos series displays an almost full set of Neandertal dental features. These features are less frequent at other sites of comparable age (9) and became ubiquitous in western Eurasia only after further pruning of the western European archaic populations. Repeated local extinctions may also explain the occurrence at the Sima de los Huesos of mitochondrial DNA similar to that sequenced in the Denisovans (10), an archaic group that diverged from the Neandertal lineage after its separation from the African groups and that peopled most of Asia. The Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig, 04103 Germany. E-mail: [email protected]
Sima de los Huesos fossils, Neandertal conditions are mostly evident in the face and teeth, whereas the braincase still retains primitive conditions. The fact is that one does not find Neandertal braincase shapes in Europe before ~200,000 years ago. Comparing brain sizes in late Neandertals and in the Sima de los Huesos hominins, Arsuaga et al. also document a substantial increase of the encephalic volume along this evolutionary branch. An independent increase in brain volume also took place along the African branch leading to modern humans, as well as in the late Homo erectus of East Asia. Hominins rely on technology and social complexity, and it is therefore not surprising to observe such parallel evolutions, because similar pressures of selection were at work in all of these lineages. However, their separation for several hundred thousand years resulted in different evolutionary pathways to achieve bigger brains. Neandertal and
SCIENCE sciencemag.org
modern brains are anatomically different. The former display a smaller cerebellum, less projecting parietal areas, smaller olfactory bulbs and temporal lobe poles, and a narrower orbitofrontal cortex (11). Furthermore, there is clear evidence that the growth pattern of modern human brains deviates from that of the Neandertals. In modern humans, parietal areas and cerebellum expand in early infancy, at a crucial stage for the establishment of cognitive skills (12). The different pathways for brain evolution are also perceptible in the DNA of both groups. Among the 87 genes that distinguish modern humans from Neandertals, a whole series are involved in brain function or development, particularly in its connectivity (13). Some of these genes belong to the most conservative part of the primate genome. They remained protected by stabilizing selection through millions of years of evolution before mutating along the modern human lineage. Although genes involved in behavior seem to have changed more in the modern human lineage than along the Neandertal line (8), it is difficult to say what this means for their phenotypic expression. The paleolithic archaeological record can yield a wealth of information regarding stone technologies or food procurement, but remains mute on key aspects of human behaviors, such as mating strategies, aggression, or large-scale cooperation. There is, however, no doubt that after more than half a million years of separate evolution, idiosyncratic features that developed in modern human groups played a key role in the almost complete replacement not only of the Neandertals but of all other archaic humans whom they met during their expansion out of Africa. ■ REF ERENCES AND NOTES
1. 2. 3. 4.
5. 6. 7. 8. 9.
10. 11. 12. 13.
J. L. Arsuaga et al., Science 344, 1358 (2014). S. Sankararaman et al., Nature 507, 354 (2014). S. Liu et al., Cell 157, 785 (2014). T. W. Holliday, in Neanderthals Revisited: New Approaches and Perspectives, K. Harvati, T. Harrison, Eds. (Springer, New York, 2006), pp. 281–298. J.-J. Hublin, Proc. Natl. Acad. Sci. U.S.A. 106, 16022 (2009). T. D. Weaver, C. C. Roseman, C. B. Stringer, J. Hum. Evol. 53, 135 (2007). S. A. Parfitt et al., Nature 466, 229 (2010). S. Castellano et al., Proc. Natl. Acad. Sci. U.S.A. 111, 6666 (2014). M. Martinón-Torres, J. M. Bermúdez de Castro, A. GómezRobles, L. Prado-Simón, J. L. Arsuaga, J. Hum. Evol. 62, 7 (2012). M. Meyer et al., Nature 505, 403 (2014). M. Bastir et al., Nat. Commun. 2, 588 (2011). P. Gunz et al., J. Hum. Evol. 62, 300 (2012). K. Prüfer et al., Nature 505, 43 (2014).
ACKNOWL EDGMENTS
I thank the Museum National d’Histoire Naturelle, Paris, for allowing the computed-tomography of the fossil skulls used here as an illustration. 10.1126/science.1255554 20 JUNE 2014 • VOL 344 ISSUE 6190
Published by AAAS
1339
