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Out of Africa, into Australia
Current Biology
Magazine Feature
Out of Africa, into Australia Genomics combined with climate modelling and linguistic analysis provides rapidly improving scenarios of how, when, and why modern humans expanded out of Africa and swiftly conquered the world. Australia has long been neglected by genome research, but in its unique situation as a final destination of migration that remained isolated for tens of thousands of years it can yield important insights into human expansion and diversification. Michael Gross reports.
Analysing the first human genomes, researchers in the countries that could afford to fund this enormous effort showed a pronounced bias to their own kind. Men of European descent dominated the first few dozens, and it took an embarrassing amount of time before the first woman, the first African, and the first Chinese person were sequenced. Considering that our entire species has its roots in Africa, and this part of the world hosts most of our genetic diversity and many of our biomedical challenges, the initial neglect of this continent was particularly counterproductive (Curr. Biol. (2011) 21, R481–R484). Coverage of human ethnicities has improved since then, but the genomics of the indigenous population of Australia and Papua New Guinea (PNG) has lagged behind. The first genome of an Australian Aboriginal person was only published in 2011. Even the draft genomes of the Neanderthal were revealed earlier, in May 2010. Now that research is catching up and has finally unveiled around 100 genomes from Australia and PNG, the first analyses show how valuable these are. Australia and PNG were accessible by short sea crossings at lower sea levels during the glacial maxima, but became isolated afterwards, setting a clearly defined and, until the onset of colonial times, almost undisturbed endpoint to the migration that began in Africa. Thus, understanding the genomes of native Australians not only explains their history, but also provides valuable insights into how our species spread around the globe. The long trek One of the most controversially debated questions regarding the expansion of our species out of Africa is whether it can be described as the consequence of one root migration which then branched
out or whether separate emigrations at different times led to the settling of different parts of the world. In 2011, when Eske Willerslev, then at Copenhagen University, Denmark, and colleagues published the first genome of an Australian Aborigines person, based on a historic lock of hair given to the Cambridge anthropologist and ethnologist Alfred Haddon by an Aboriginal trader at a train station in 1923, they concluded that differences between Australian natives and Eurasians required separate emigration events as an explanation. This result, however, was obtained without taking into account the admixture of the ancient race of the Denisovans, represented by the genome obtained from a single finger bone found in the Denisova cave in Siberia in 2008. The shared ancestors of Denisovans
and Neanderthals separated from those of modern humans around 400,000 years ago. Willerslev, who now holds a position at Cambridge University, UK, as well as at Copenhagen, and colleagues, in close collaboration with Aborigines and PNG communities, have now begun to fill in these white patches in world genomics with high-quality sequences of 83 Aboriginal Australians and 25 Papuans (Nature (2016) 538, 207–214). Comparing these genomes, representative of most but not all indigenous populations in Australia and PNG, with known genomes from other continents, Willerslev and colleagues arrive at a migration scenario that is markedly different from the one glimpsed from the first Aboriginal genome in 2011. As always, the model comes with large error bars regarding the dates, but the most likely course of events looks like this: all non-African populations of present-day humans go back to a single wave of emigration from Africa. The genetic bottleneck presumably caused by the small size of the migrating population can be dated to 72,000 years ago, although the common ancestors that all non-Africans share with WestAfrican Yoruba lived much earlier, around 127,000 years ago.
True colours: Since modern humans expanded into the Australian continent some 40,000 years ago, they developed a rich landscape of cultural and linguistic diversity — until the arrival of the colonialists who failed to appreciate their ancient civilisation. (Photo: © Wayne Quilliam Photography/Yothu Yindu Foundation.)
Current Biology 26, R1119–R1136, November 7, 2016 R1119
Current Biology
Magazine
Music making: Papua New Guinea was connected to Australia at the time when humans arrived, but soon became separated and thus its population went its separate genetic, cultural, and linguistic ways. (Photo: Anselmo Lastra, Flickr.)
Before splitting and going their separate ways, the migrants encountered Neanderthals, who were already present in Eurasia more than 200,000 years before our time, and interbred with them to a limited extent, meaning that all non-African humans today have a small but significant Neanderthal signature in their genomes which amounts to between 1 and 4% of the genomic material. The ancestors of Australians and Papuans split from the Eurasians and future Native Americans around 58,000 years ago. They went through another noticeable bottleneck soon after the split (50,000 years ago) and then, around 44,000 years ago, encountered Denisovans, another archaic hominin species, who contributed around 2% of the genomic DNA of Australo-Papuans, but none in any other present-day population. They colonised the ancient continent Sahul, comprising today’s Australia, PNG, and Tasmania, along with areas now covered by the shallow waters between these. This continent was separated from the Sunda landmass, of which today only islands survive, by a deep but narrow trench which ancient migrants must have crossed with canoes or floats. With rising sea levels, the isolation of Australia from Eurasia became more difficult to overcome, R1120
while PNG and Tasmania were separated from the Australian mainland. Around 37,000 years ago, the Papuans split from the lineage of the Australian Aborigines whose genomes were studied. While these represent a geographic spread covering most of the habitable surface of Australia, they are all speakers of languages belonging to the major language family of Pama-Nyungan, so some other, less widespread linguistic groups are not yet accounted for. Archaeological evidence suggests that humans conquered the Australian continent over 40,000 years ago, leaving researchers with open questions as to why the Papuan split happened so much later. Further genomes of other Australian population groups may help to clarify this issue. Within today’s Australia, a major split emerged between northeastern and southwestern groups, which is welldocumented both in linguistic analyses and in the genomes. The diversification of the languages occurred much later than the genetic split, which in turn can be traced back to challenging climate conditions. Climate drivers and barriers All of the evolution of our species from the ancestors we share with
Current Biology 26, R1119–R1136, November 7, 2016
great apes has happened within a general icehouse period, marked by the presence of a permanent ice cap at the South Pole, which has been present since the beginning of the Oligocene, some 34 million years ago. Climate fluctuations within that icehouse framework happened on a timescale relevant for human evolution and expansion, creating dangers and opportunities through changes both in sea levels and the habitability of large areas of land. In parallel with the progress of genomics, climate modelling has also been able to improve the level of detail it can provide on the impact of climate on past human populations. SubSaharan Africa is now separated from Europe and Asia by deserts that early modern humans would have found impossible to pass through. However, these arid conditions have varied over time, as even the Sahara has seen episodes with wetter conditions and abundant vegetation. Climate modelling predicts that, in the timeframe relevant to the spread of our species out of Africa, there have been three significant windows of opportunity, when relatively mild and humid weather conditions made the Arabian Peninsula passable. These conditions are attributed to a variation in the Earth’s orbital precession, which recurs at intervals of around 21,000 years. In a recent study modelling the interactions of climate and migration, Axel Timmermann and Tobias Friedrich from the University of Hawaii at Manoa, USA, locate these windows at 106–94, 89–73, and 45–29 thousand years ago (Nature (2016) 538, 92–95). Further migrations around the world were also shaped by climate variations and their effects on land and sea. The expansion into the Americas from Siberia, which Willerslev and colleagues have also investigated in previous genome studies, was only possible for a short time, when low sea levels and benign climate conditions in the Beringia area created the opportunity that led to the peopling of the entire double continent. Similarly, the expansion into Sahul across the Sunda strait depended on low sea levels narrowing the sea passages to be made. Rising sea levels later separated Papua New Guinea and Tasmania from the Australian continent.
Current Biology
Magazine
Desert barrier: At the time when they first settled in Australia, humans could spread throughout the continent. At the time of the last glacial maximum, large parts of the interior became deserts, splitting the inhabitants into several regional populations that lost genetic contact with each other. (Photo: outreachr.com, Flickr.)
After arrival in today’s Australia, humans were able to disperse across the continent, but during the last glacial maximum, which peaked around 19,000 years ago, the increasingly arid climate in the continent’s interior made large areas impassable and thus separated populations which went on to develop separate cultures and languages. Language families European colonialists failed to appreciate the wealth of native languages present in the new worlds they conquered and actively sought to eradicate them. Only in recent decades was the ensuing decline of linguistic diversity recognised as a tragic loss for humanity. In Australia, in particular, language diversification over tens of thousands of years on a continent largely cut off from the rest of the world has occurred in a unique test-tube situation that might provide valuable insights into the evolution of languages in our species more generally. Linguists studying the embers of what once was a rich cultural tapestry have produced family trees of language groups (Bowern, C. and Atkinson, Q. (2012). Language 88, 817–845) that can now be checked against the genome data. The first analyses reported by Willerslev’s group suggest that the genetic data are in good agreement with what is known about the largest language family, the Pama-Nyungan languages, which only branched out within the last 6,000 years. The data suggest that genetic division preceded the diversification of the languages. The family consists of the Pama languages in the northeast of the
continent and the Nyungan languages in the southwest and comprises around 300 known languages, many of which are on the brink of extinction. Other language families found in the far north of the continent, in Arnhem Land and the Gulf of Carpentaria, are yet awaiting genomic analyses, which might also help to clarify their evolution, an issue that has so far been subject to debate. Adapting to your new home In analysing the Australian genomes, Willerslev and colleagues also looked out for specific adaptation to life in the particular climate conditions. They discovered strong selection for two genes associated with survival in the desert, one associated with the thyroid system and the response to cold nights in the desert, and the other with serum urate levels and the response to dehydration. Elsewhere, other genetic variants have facilitated the spread of our species around the world, and genomic studies are uncovering more and more of these, as Sarah Tishkoff from the University of Pennsylvania at Philadelphia, USA, and colleagues report in a recent review (Science (2016) 354, 54–59). Apart from the obvious skin colour variations, specific adaptations have been described for high altitude, for arctic environments, for arsenic-rich environments, as well as for resistance to trypanosomes and malaria, and for certain diets. Sharing a common story When scientists from the western world approach native populations in order to study their genomes, this can create
an ethically fraught situation, which could easily lead to suspicion of a new kind of exploitation. In the 1990s, the Human Genome Diversity Project was heavily criticised by Native American and Australian Aborigines groups on the basis of such fears. Willerslev, however, who has previously worked with native American and Inuit groups, takes pride in his good contacts with the subjects of his studies and has always succeeded in convincing them that their interests will also be taken into account. In the Australian paper, Aboriginal scientists contributed as co-authors. Beyond the author credits, there are also benefits for the Aborigines communities in that the study underlines their belief in the ancient nature of their civilisation. Moreover, in the long-running disputes over demands to repatriate human remains taken from Australia, the genomes provide a tool for campaigners to identify to which part of the continent the remains belong. Colleen Wall, an Aboriginal coauthor of the paper told ABC News: “This information, coupled with the technology now used to assist in identifying where our human remains come from exactly, is exciting. It means that all our old people who are still in collecting institutions across the world may be able to come home and be on their own specific country, not in a museum somewhere in Australia. Placing them as close to country as possible will settle them down.” Thus, the genomes may mean different things to different people, but everybody wins. More generally, the Australian work, together with other genome studies, two of which appeared simultaneously (Nature (2016) 538, 201–206; 238–242), may help all of humanity to gain a deeper understanding of our shared global history and relatedness. Whereas the superficial differences have long fuelled prejudice and racism, scientists now have increasingly sophisticated versions of our family tree to prove in detail that all humans are family in the sense that they share a common ancestry, complete with migration background. Michael Gross is a science writer based at Oxford. He can be contacted via his web page at www.michaelgross.co.uk
Current Biology 26, R1119–R1136, November 7, 2016 R1121
Magazine Feature
Out of Africa, into Australia Genomics combined with climate modelling and linguistic analysis provides rapidly improving scenarios of how, when, and why modern humans expanded out of Africa and swiftly conquered the world. Australia has long been neglected by genome research, but in its unique situation as a final destination of migration that remained isolated for tens of thousands of years it can yield important insights into human expansion and diversification. Michael Gross reports.
Analysing the first human genomes, researchers in the countries that could afford to fund this enormous effort showed a pronounced bias to their own kind. Men of European descent dominated the first few dozens, and it took an embarrassing amount of time before the first woman, the first African, and the first Chinese person were sequenced. Considering that our entire species has its roots in Africa, and this part of the world hosts most of our genetic diversity and many of our biomedical challenges, the initial neglect of this continent was particularly counterproductive (Curr. Biol. (2011) 21, R481–R484). Coverage of human ethnicities has improved since then, but the genomics of the indigenous population of Australia and Papua New Guinea (PNG) has lagged behind. The first genome of an Australian Aboriginal person was only published in 2011. Even the draft genomes of the Neanderthal were revealed earlier, in May 2010. Now that research is catching up and has finally unveiled around 100 genomes from Australia and PNG, the first analyses show how valuable these are. Australia and PNG were accessible by short sea crossings at lower sea levels during the glacial maxima, but became isolated afterwards, setting a clearly defined and, until the onset of colonial times, almost undisturbed endpoint to the migration that began in Africa. Thus, understanding the genomes of native Australians not only explains their history, but also provides valuable insights into how our species spread around the globe. The long trek One of the most controversially debated questions regarding the expansion of our species out of Africa is whether it can be described as the consequence of one root migration which then branched
out or whether separate emigrations at different times led to the settling of different parts of the world. In 2011, when Eske Willerslev, then at Copenhagen University, Denmark, and colleagues published the first genome of an Australian Aborigines person, based on a historic lock of hair given to the Cambridge anthropologist and ethnologist Alfred Haddon by an Aboriginal trader at a train station in 1923, they concluded that differences between Australian natives and Eurasians required separate emigration events as an explanation. This result, however, was obtained without taking into account the admixture of the ancient race of the Denisovans, represented by the genome obtained from a single finger bone found in the Denisova cave in Siberia in 2008. The shared ancestors of Denisovans
and Neanderthals separated from those of modern humans around 400,000 years ago. Willerslev, who now holds a position at Cambridge University, UK, as well as at Copenhagen, and colleagues, in close collaboration with Aborigines and PNG communities, have now begun to fill in these white patches in world genomics with high-quality sequences of 83 Aboriginal Australians and 25 Papuans (Nature (2016) 538, 207–214). Comparing these genomes, representative of most but not all indigenous populations in Australia and PNG, with known genomes from other continents, Willerslev and colleagues arrive at a migration scenario that is markedly different from the one glimpsed from the first Aboriginal genome in 2011. As always, the model comes with large error bars regarding the dates, but the most likely course of events looks like this: all non-African populations of present-day humans go back to a single wave of emigration from Africa. The genetic bottleneck presumably caused by the small size of the migrating population can be dated to 72,000 years ago, although the common ancestors that all non-Africans share with WestAfrican Yoruba lived much earlier, around 127,000 years ago.
True colours: Since modern humans expanded into the Australian continent some 40,000 years ago, they developed a rich landscape of cultural and linguistic diversity — until the arrival of the colonialists who failed to appreciate their ancient civilisation. (Photo: © Wayne Quilliam Photography/Yothu Yindu Foundation.)
Current Biology 26, R1119–R1136, November 7, 2016 R1119
Current Biology
Magazine
Music making: Papua New Guinea was connected to Australia at the time when humans arrived, but soon became separated and thus its population went its separate genetic, cultural, and linguistic ways. (Photo: Anselmo Lastra, Flickr.)
Before splitting and going their separate ways, the migrants encountered Neanderthals, who were already present in Eurasia more than 200,000 years before our time, and interbred with them to a limited extent, meaning that all non-African humans today have a small but significant Neanderthal signature in their genomes which amounts to between 1 and 4% of the genomic material. The ancestors of Australians and Papuans split from the Eurasians and future Native Americans around 58,000 years ago. They went through another noticeable bottleneck soon after the split (50,000 years ago) and then, around 44,000 years ago, encountered Denisovans, another archaic hominin species, who contributed around 2% of the genomic DNA of Australo-Papuans, but none in any other present-day population. They colonised the ancient continent Sahul, comprising today’s Australia, PNG, and Tasmania, along with areas now covered by the shallow waters between these. This continent was separated from the Sunda landmass, of which today only islands survive, by a deep but narrow trench which ancient migrants must have crossed with canoes or floats. With rising sea levels, the isolation of Australia from Eurasia became more difficult to overcome, R1120
while PNG and Tasmania were separated from the Australian mainland. Around 37,000 years ago, the Papuans split from the lineage of the Australian Aborigines whose genomes were studied. While these represent a geographic spread covering most of the habitable surface of Australia, they are all speakers of languages belonging to the major language family of Pama-Nyungan, so some other, less widespread linguistic groups are not yet accounted for. Archaeological evidence suggests that humans conquered the Australian continent over 40,000 years ago, leaving researchers with open questions as to why the Papuan split happened so much later. Further genomes of other Australian population groups may help to clarify this issue. Within today’s Australia, a major split emerged between northeastern and southwestern groups, which is welldocumented both in linguistic analyses and in the genomes. The diversification of the languages occurred much later than the genetic split, which in turn can be traced back to challenging climate conditions. Climate drivers and barriers All of the evolution of our species from the ancestors we share with
Current Biology 26, R1119–R1136, November 7, 2016
great apes has happened within a general icehouse period, marked by the presence of a permanent ice cap at the South Pole, which has been present since the beginning of the Oligocene, some 34 million years ago. Climate fluctuations within that icehouse framework happened on a timescale relevant for human evolution and expansion, creating dangers and opportunities through changes both in sea levels and the habitability of large areas of land. In parallel with the progress of genomics, climate modelling has also been able to improve the level of detail it can provide on the impact of climate on past human populations. SubSaharan Africa is now separated from Europe and Asia by deserts that early modern humans would have found impossible to pass through. However, these arid conditions have varied over time, as even the Sahara has seen episodes with wetter conditions and abundant vegetation. Climate modelling predicts that, in the timeframe relevant to the spread of our species out of Africa, there have been three significant windows of opportunity, when relatively mild and humid weather conditions made the Arabian Peninsula passable. These conditions are attributed to a variation in the Earth’s orbital precession, which recurs at intervals of around 21,000 years. In a recent study modelling the interactions of climate and migration, Axel Timmermann and Tobias Friedrich from the University of Hawaii at Manoa, USA, locate these windows at 106–94, 89–73, and 45–29 thousand years ago (Nature (2016) 538, 92–95). Further migrations around the world were also shaped by climate variations and their effects on land and sea. The expansion into the Americas from Siberia, which Willerslev and colleagues have also investigated in previous genome studies, was only possible for a short time, when low sea levels and benign climate conditions in the Beringia area created the opportunity that led to the peopling of the entire double continent. Similarly, the expansion into Sahul across the Sunda strait depended on low sea levels narrowing the sea passages to be made. Rising sea levels later separated Papua New Guinea and Tasmania from the Australian continent.
Current Biology
Magazine
Desert barrier: At the time when they first settled in Australia, humans could spread throughout the continent. At the time of the last glacial maximum, large parts of the interior became deserts, splitting the inhabitants into several regional populations that lost genetic contact with each other. (Photo: outreachr.com, Flickr.)
After arrival in today’s Australia, humans were able to disperse across the continent, but during the last glacial maximum, which peaked around 19,000 years ago, the increasingly arid climate in the continent’s interior made large areas impassable and thus separated populations which went on to develop separate cultures and languages. Language families European colonialists failed to appreciate the wealth of native languages present in the new worlds they conquered and actively sought to eradicate them. Only in recent decades was the ensuing decline of linguistic diversity recognised as a tragic loss for humanity. In Australia, in particular, language diversification over tens of thousands of years on a continent largely cut off from the rest of the world has occurred in a unique test-tube situation that might provide valuable insights into the evolution of languages in our species more generally. Linguists studying the embers of what once was a rich cultural tapestry have produced family trees of language groups (Bowern, C. and Atkinson, Q. (2012). Language 88, 817–845) that can now be checked against the genome data. The first analyses reported by Willerslev’s group suggest that the genetic data are in good agreement with what is known about the largest language family, the Pama-Nyungan languages, which only branched out within the last 6,000 years. The data suggest that genetic division preceded the diversification of the languages. The family consists of the Pama languages in the northeast of the
continent and the Nyungan languages in the southwest and comprises around 300 known languages, many of which are on the brink of extinction. Other language families found in the far north of the continent, in Arnhem Land and the Gulf of Carpentaria, are yet awaiting genomic analyses, which might also help to clarify their evolution, an issue that has so far been subject to debate. Adapting to your new home In analysing the Australian genomes, Willerslev and colleagues also looked out for specific adaptation to life in the particular climate conditions. They discovered strong selection for two genes associated with survival in the desert, one associated with the thyroid system and the response to cold nights in the desert, and the other with serum urate levels and the response to dehydration. Elsewhere, other genetic variants have facilitated the spread of our species around the world, and genomic studies are uncovering more and more of these, as Sarah Tishkoff from the University of Pennsylvania at Philadelphia, USA, and colleagues report in a recent review (Science (2016) 354, 54–59). Apart from the obvious skin colour variations, specific adaptations have been described for high altitude, for arctic environments, for arsenic-rich environments, as well as for resistance to trypanosomes and malaria, and for certain diets. Sharing a common story When scientists from the western world approach native populations in order to study their genomes, this can create
an ethically fraught situation, which could easily lead to suspicion of a new kind of exploitation. In the 1990s, the Human Genome Diversity Project was heavily criticised by Native American and Australian Aborigines groups on the basis of such fears. Willerslev, however, who has previously worked with native American and Inuit groups, takes pride in his good contacts with the subjects of his studies and has always succeeded in convincing them that their interests will also be taken into account. In the Australian paper, Aboriginal scientists contributed as co-authors. Beyond the author credits, there are also benefits for the Aborigines communities in that the study underlines their belief in the ancient nature of their civilisation. Moreover, in the long-running disputes over demands to repatriate human remains taken from Australia, the genomes provide a tool for campaigners to identify to which part of the continent the remains belong. Colleen Wall, an Aboriginal coauthor of the paper told ABC News: “This information, coupled with the technology now used to assist in identifying where our human remains come from exactly, is exciting. It means that all our old people who are still in collecting institutions across the world may be able to come home and be on their own specific country, not in a museum somewhere in Australia. Placing them as close to country as possible will settle them down.” Thus, the genomes may mean different things to different people, but everybody wins. More generally, the Australian work, together with other genome studies, two of which appeared simultaneously (Nature (2016) 538, 201–206; 238–242), may help all of humanity to gain a deeper understanding of our shared global history and relatedness. Whereas the superficial differences have long fuelled prejudice and racism, scientists now have increasingly sophisticated versions of our family tree to prove in detail that all humans are family in the sense that they share a common ancestry, complete with migration background. Michael Gross is a science writer based at Oxford. He can be contacted via his web page at www.michaelgross.co.uk
Current Biology 26, R1119–R1136, November 7, 2016 R1121