Tibeto-Burman expansions: high-altitude adaptation and Paleolithic legacy on the Tibetan Plateau

Humans have been living at extreme altitudes for a very long time. However, only a very small percentage of the planet’s population inhabit such places. Today, the largest communities of high-altitude dwellers reside on the Tibetan Plateau. These mountainous people are speakers of Tibeto-Burman languages which came to be spoken as a result of relatively recent population movements, expansions and language developments. This article will go through the genetic landscape of the Tibetan Plateau, how Tibeto-Burman speakers expanded into and across the Plateau, and why and how some Tibeto-Burman populations came to be characterized by unique adaptations and archaic ancestry.

Qi et al. (2013) put forth solid evidence of Upper Paleolithic colonization of the Tibetan Plateau and gave us a good idea of what the process looked like. The Upper Paleolithic inhabitants of the Tibetan Plateau are quite relevant when discussing the emergence of the Tibeto-Burman populations that settled the Plateau. While the bulk of the autosomal DNA of modern Tibetans is made up by DNA from Neolithic Yellow River immigrants, Tibetans and populations that are closely related to them still carry a significant amount of DNA from these Paleolithic highland-foragers who inhabited the Tibetan Plateau before the arrival of the Yellow River agro-pastoralists.

The Yangshao culture, a likely birthplace of Sino-Tibetan languages

Tibeto-Burman languages are a language group within the Sino-Tibetan family. While the other branch of the ST language family, the Sinitic languages, has many more speakers than Tibeto-Burman languages, the TB language branch has a very significant internal diversity. In fact, the internal diversity of the TB languages can be compared to that of Indo-European languages.

Sagart et al. (2019) used dated language phylogeny to provide an estimation for the formation of the Sino-Tibetan language family and assign it to one or more material cultures. The study concluded that the ST languages most likely have their origins in the late Cishan culture and the early Yangshao culture, both which are associated with the early East Asian dispersal of what proved to be an extremely efficient substinence strategy, namely millet farming. Driven by the significant increase in population size that took place in the Yangshao culture, its people migrated in many directions. This increase in population size likely triggered the expansion into the Tibetan Plateau. All of this is strongly supported by archaeology and linguistics and, more recently, also by genetics.

Zhang et al. (2017) supports earlier data for the Tibeto-Burman Y-DNA expansion path and the linguistic data with an estimation of the time for the divergence event between Tibetans and the Han Chinese, which they pin down to between 15,000-9000 years ago. This would again support what earlier data suggested, which is that ST languages have their urheimat in early Yellow River Neolithic cultures, whose populations later split up, went their separate paths and had their languages develop independently of each other, with other influences and local substrates from the regions they expanded into.

Paternal lineages of ancient and modern Tibeto-Burmans

As is often the case with expansions of speakers of a language group, the Tibeto-Burmans sprung from a “core group” that spread in multiple directions and assimilated and/or outcompeted the people they encountered on their way. As they expanded, their autosomal ancestry and Y-DNA haplogroups was spread. Before we delve further into the Tibeto-Burman expansions, it is important that we are aware of the most important Y-DNA haplogroups involved in the expansions. The main Y-DNA haplogroups of Tibeto-Burmans are:

  • O1-CTS1642 (branches O-CTS5308, O- Z25929)
  • D-M174 (branches D1a2a1-PH116, D1a1a1a2-Z31591, D1a2a-P47)

While haplogroup D-M174 is very old, the subclades of D-M174 that Tibeto-Burmans belong to all have a fairly recent TMRCA (time to most recent common ancestor). Here, we can observe a pattern that is quite common in archaogenetics. A very old Paleolithic Y-DNA lineage experiences a long-term bottleneck, dwindles in frequency to existing only in a very small population (often a small hunter-gatherer population), until it is picked up by an expanding population larger in size, often an agricultural or pastoralist population. The formerly bottlenecked haplogroup “rides the wave” of this expansion, either through becoming part of the elite and gaining more access to reproduction, or purely by chance. By the end of the expansion, the formerly rare and old haplogroup is now common and widespread, but has a recent TMRCA, making a Y-DNA haplogroup both young and old, in a way. This is exactly what happened in the case of D1-PH116, D1-Z31591 and D1-P47 which are the Tibeto-Burman subclades of D-M174. Together these subclades of D-M174 have a 44% frequency among Sherpa males from Nepal and Tibet, and a 52.84% frequency among Tibetan males (Bhandari et al. 2015).

As for the Neolithic population that fuelled the expansion during which D-M174 was picked up from East Asian highland foragers, they are represented paternally by two branches of O1α1c1-CTS1642, namely O-Z25929 and O-CTS5308, both found at high frequencies in modern Tibeto-Burman populations. There is something of a divide in distribution of haplogroups when it comes to Tibeto-Burman O1-CTS1642, with O-CTS5308 mainly being found at high frequencies among Tibetans, Sherpas, Riang and Dai peoples, while O-Z25929 is somewhat more widespread, being found at high frequencies among the Burmese, Han, Kinh, Naxi as well as Tibetans. Tibeto-Burman branches of O1-CTS1642 have a frequency of 27% among Sherpa males, and 33.13% among Tibetans.

The Maijayao culture and subsequent expansions of Tibeto-Burmans

While the Sino-Tibetan languages may have their origin in the Yellow River Neolithic Yangshao culture, from which its descendant cultures diverged and split into Tibeto-Burman and Sinitic, it is probably not until the Maijayao culture that we can confidently identify the immediate ancestors of the Proto-Tibeto-Burmans. This culture, in turn, gave rise to the Bronze Age Qijia culture. The descendants of the Qijia culture would later go on to influence and found several succeeding cultures, one of which were the Siwa culture. The later three can all be associated with Tibeto-Burmans in one way or another.

Studies like Hung (2011) have shown that the formation of the Majiayao culture was, in many ways, a result of interactions between local hunter-gatherers and farmers from the western branch of the Yangshao culture. It is fully possible that in the Maijayao culture, we may essentially be looking at Proto-Tibeto-Burmans, or at least their immediate predecessors. In Majiayao, we have one branch of the Yangshao culture extending all the way to the edges of the Tibetan Plateau. It was likely there that Yellow River-related farmers encountered East Asian highland foragers and mixed with them. An admixture event which in turn, brings us to a very important part of early Tibeto-Burman population dynamics – Paleolithic ancestry.

The most obvious sign of Paleolithic genetic legacy in some Tibeto-Burman populations is the very high frequency of haplogroup D-M174 mentioned earlier in this article. Among Tibetan males, it reaches a frequency of over 50%. This is quite remarkable, and in fact makes Tibetans one of the populations in the world with the highest frequency of Y-DNA haplogroup D, along with the Japanese and the Andamanese Islanders. Furthermore, some subgroups of these populations have even higher frequencies, such as the Ainu people of Japan and the Tripuri people of Tripura in India, the latter which is a Tibeto-Burman population.

It is quite likely that most of the D-M174 lineages of the Tibeto-Burmans were picked up during the aforementioned interaction between farmer-pastoralists and foragers, and in order for the TB branches of D-M174 to have undergone the significant growth in frequency they did, haplogroup D-M174 must have been present at a very early stage in the early TB population. If we assume that this assimilation of D-M174 into the otherwise Neolithic Yellow River-derived population (in which subclades of haplogroup O1a-F5 would have been the dominant paternal marker) happened at the foothills of the Tibetan Plateau, then we have a very good candidate for a founder population that expanded into the Plateau and beyond. It is in all likelihood in the Maijayao culture that we see the emergence of this unique population, a proto-Tibeto-Burman group characterized by a mix of Yellow River Neolithic-related ancestry and East Asian highland forager-related ancestry.

Interestingly, Tibeto-Burman subclades of O1α1c1-CTS1642 have a TMRCA (time to most recent common ancestor) that is almost exactly as old as the formerly mentioned Maijayao culture.

It is worth mentioning that Paleolithic contribution into Tibeto-Burmans was not entirely male-driven, either. MtDNA haplogroups such as M16 and M62 most likely got into the early TB gene pool from the same population as the Tibeto-Burman subclades of Y-DNA haplogroup D-M174 entered it from.

Furthermore, Paleolithic admixture was decisive in determining the outcome of Tibeto-Burman movement into the Tibetan Plateau in more ways than one. Modern populations on the Tibetan Plateau are genetically adapted to high altitudes, exemplified by adaptive alleles associated with oxygen efficiency and increased nitric oxide production, among other adaptations. It is very unlikely that the Neolithic people migrating from the middle Yellow River Basin had the physical adaptations required in order to survive – and thrive, in the harsh high-altitude environment of the Tibetan Plateau. This, of course, raises the question of where, when and how the linguistic and genetic forefathers of the Tibeto-Burmans became so well adapted to such environments. Recent studies such as Wang et al. (2018) have shown that they developed these traits due to long-term admixture with people descended from the Paleolithic inhabitants of the Tibetan Plateau. As an example, in the present day, the village of Tuiwa in Tibet is the second highest village by elevation in the entire world. Its inhabitants may owe their suitability for life in such a place mainly to the aforementioned admixture event and selection that took place between Yellow River immigrants and local hunter-gatherers of areas in and near the Tibetan Plateau.

This long-term admixture between Yellow River Neolithic-related groups and Paleolithic remnants was clearly mutually beneficial. The former received extremely useful high-altitude genetic adaptations, while the latter groups were taught plenty of useful skills such as agropastoralist substinence strategies and more advanced tool making. We will delve further into the details of Tibetan high-altitude genetic adaptations later in this article.

Let us now move on to the Yellow River Neolithic-related part of Tibeto-Burman Y-DNA haplogroups. If we look at the phylogeny of Oa-F5 in general, it becomes rather obvious that this lineage was present at what was most likely moderate to high frequencies in the Neolithic Yangshao culture. From there, significant diversification occurred and a high amount of branches subsequently developed. Many of them would go on to become the founding paternal lineages in Proto-Sinitic-speaking cultures, but a few others took a different path of expansion. These other divergent groups, many of whom carried Y-DNA haplogroups such as O1ac1b-CTS5308 and O1a1c1a-Z25929, would play a highly important role in the dispersal of Tibeto-Burman languages as well as agriculture-facilitated permanent human occupation of the Tibetan Plateau. Interestingly, O-CTS5308 was found in an ancient DNA sample from the 2400 years old Nepalese sample with the label Chokhopani-C1 from Jeong et al. (2016). This consolidates the path of expansion that linguistics and archaeology already implied for this paternal lineage.

While it is easy to assume that the dispersal of these languages happened in just one massive sweep as was the case for many language expansions, DNA suggests that the case of the Tibeto-Burman expansions is not that simple. Rather, we are looking at a minimum of two major expansions from two founder populations with different local substrates. This, at least, is what a study by Wang et al. (2018) concluded, based on the presence andabsence of some subclades of O1-CTS1642 (again, a sublineage of Oa-F5) in various Tibeto-Burman populations. For example, Y-DNA haplogroup O1a1c1a-Z25929 has a strong presence among Tibeto-Burman males in Burma, Hunan and Yunnan in China, as well as in parts of Northeast India. However, it is present only at low frequencies in some other Tibeto-Burman populations, which indicates that while it is to some degree a pan-TB lineage, it is characteristic only of one of multiple TB expansions. If we get back to the other major O1-CTS1642 subclade among Tibeto-Burmans, O-CTS5308, we can see that it is also pan-TB, but still mainly confined to some TB populations, suggesting a highland expansion route. O-CTS5308 is found at significant frequencies among Tibetans, Sherpas (who descend from Tibetans, which we will get to later in this article), as well as the Dai people in the Yunnan province of China.

Clearly, what we are looking at here, are two populations that almost certainly expanded out of the same cultural network but underwent individual founder effects in terms of Y-DNA haplogroups, and some of those lineages were picked up locally and/or before the expansions reached their “final destination”. In mountaineous areas, many cases of periodic isolation could probably be found, which would result in all kinds of Y-DNA founder effects, further explaining minor differences and general variation in modern Tibeto-Burman Y-DNA distribution. Featured below is an image of approximate proposed migration paths for Tibeto-Burman populations, from Wang et al. (2018) which clearly shows that O-Z25929 took a southwestern route of expansion while O-CTS5308 initially took a more western/northwestern path of expansion:

Figure 3, from Wang et al. (2018)

The Sherpa, where do they come from?

The Sherpa people, native to regions of what is now Nepal and China, as well as the Himalaya mountains and parts of Tibet, have been the subjects of many genetic studies due to their notable feats of performance in high-altitude environments. These mountain-dwelling people speak Sherpa, a language which is closely related to Tibetan.

Until relatively recently, the genetic origins of the Sherpa people were still poorly understood and a topic of debate. Some early genetic studies speculated, without much evidence, that it was Tibetans who descended from Sherpas, as a mix of Sherpas and the Han. However, we now know that is not the case. Rather, we now have strong evidence suggesting that Tibetans and Sherpas share recent common ancestors and have their origins in the same Tibeto-Burman expansion. This is not only strengthened by the close autosomal similarity and resemblance in Y-DNA haplogroup composition, but also by the fact that mtDNA haplogroups that are quite specific to the modern Sherpa population display only a very minor and recent divergence from the mtDNA of modern Tibetans. The minor differences in autosomal admixture between the two populations are mainly explained by an increased presence of South Asian admixture in Sherpas, and more East and Central Asian-related ancestry in Tibetans. In terms of genetic distance, the differences are not overly significant, and Tibetans and Sherpas share much of the same genetic drift and even the same genetic high-altitude adaptations. If we use a tool like G25 to see how Sherpas and Tibetans plot on a PCA relative to other East Asian populations, what we get is the result below:

Unsurprisingly, Tibetan and Sherpan populations demonstrate a strong affinity to each other. For further clarity, besides samples from modern East Asian populations, I have added ancient samples from the Amur River basin, Yellow River, as well as Jōmon samples from Japan.

High-altitude adaptations: from archaics into humans and animals alike

Inhabitants of the Tibetan Plateau are well known for their ability to handle life at high altitudes. Studies have shown that the adaptations to these harsh circumstances came to be through a series of complex events of selection, and that their origin lies with the highland forager populations that contributed a signficant amount of ancestry to modern inhabitants of the Tibetan Plateau.

For example, adaptations in the EPAS1 and EGLN1 genes which codes for proteins involved in the sensing of oxygen levels have been identified in Tibetan and Sherpan populations. These adaptations are believed to help the body utilize oxygen in a more efficient manner, partially through the regulation of hemoglobin production, which is an incredibly useful advantage to have when finding yourself in a high-altitude environment and dealing with low oxygen levels. With such a high degree of usefulness, it is no wonder that the mutation near EPAS1 is found at such a high frequency in, for example, Tibetans (a frequency of almost 90%). What we are seeing here are mutations originally present in the East Asian highland hunter-gatherer populations that were assimilated by the expanding lowland East Asian Neolithic population and most likely ended up being selected for at a high intensity, which probably made these traits even more common in the emerging Tibeto-Burman populations of the Plateau than they had been before. For comparison, the same adaptive alleles in or near the genes EPAS1 and EGLN1 are present only at an estimated 9% frequency among the Han Chinese, strongly suggesting that these adaptations are not particularly useful for, and thus were not selected for, in the lowland populations of East Asia.

Many, if not all of the adaptive hemoglobin traits present among Tibetans are also present among Sherpas, and so are the adaptive alleles associated with an increased production of nitric oxide (NO). Inhabitants of the Tibetan Plateau tend to have these adaptive alleles, and in some studies they have been noted to have an NO production many times higher than low altitude dwellers. Some of these alleles have been associated not only with increased NO production in general, but with increased blood flow to the forearms in particular. This, of course, is a hugely beneficial adaptation to have for mountain climbers. In ancient times – and modern, having such a trait could easily make the difference between life and death.

Interestingly, Huerta-Sanchéz et al. (2014) associates the alleles associated with high-altitude adaptation in Tibetan populations with Denisovan-like DNA. Furthermore, the importance of an archaic human introgression into the East Asian highlander population was elaborated on in Xinjung Zhang et al. (2021). This study largely corroborated that the Tibetan and Sherpa EPAS1 haplotypes in all likelihood have their deep origins in an introgression of Denisovan-like DNA into the gene pool of Paleolithic foragers of the Tibetan Plateau and in nearby regions. It should be kept in mind, however, that the actual percentage of Denisovan-like DNA among Tibetans and Sherpas is very small. These populations have far less Denisovan-related ancestry than, for example, modern Melanesians. Additionally, there appears to have been two independent admixture events between Denisovans and East Asian populations. One of them is shared with populations in Oceania and South Asia. The other one, however, is unique to East Asians. The introgression of Denisovan-like DNA that originally introduced the adaptations in EPAS1 is estimated to have occurred around 48, 000 years ago. So, what we can observe here is a truly fascinating case of archaic human legacy entering the gene pool of Paleolithic highland foragers, who in turn mixed with a Yellow River Neolithic population and selected even further for these adaptive alleles, eventually resulting in populations that are extremely well adapted to high-altitude environments.

Just like the humans of the Tibetan Plateau became genetically adapted to the region’s difficult circumstances, so did the animals accompanying them. The best example of this is no doubt the Tibetan Mastiff, a large and beautiful dog breed found in the Himalayan mountain ranges. This breed is mainly used as a herding and watch dog, and has been known to have a tremendous tolerance for low oxygen environments. A high-altitude adapter, much like its masters.

Fascinatingly, studies like Ming-Shan Wang et al. (2020) and Signore et al. (2019) found that the Tibetan Mastiff has gone through selection for the same adaptive alleles that allow for a more efficient oxygen utilization in humans of the Tibetan Plateau. Not only that, but much like humans, they ultimately received their genetic high-altitude adaptations from an archaic species. In the case of Tibetan Mastiffs, it was from admixture with an unknown wolf-like canid. It is hard to determine the exact nature of this archaic ghost population, but it is safe to say that these must have been some very tough beasts, incredibly well adapted to high altitudes. Tibetan and Himalayan wolves derive roughly 39% of their total DNA from this unidentified ancient wolf-like popoulation, and admixture between them and Tibetan Mastiffs introduced these beneficial adaptations into the genome of Tibetan Mastiffs. This process is remarkably similar to how modern Tibetans and Sherpas became so well adapted to high altitudes. It shows how Paleolithic ancestry was able to persist in the region due to suitability for such an environment, a suitability that they may very well have owed to even older ancestry, inherited from an archaic source.

Of course, Himalayan canines are not the only animals in the region adapted to high altitudes. Yaks in the Himalayas also have their own genetic adaptations to such environments, partially due to changes in internal organ size and function compared to lowland cattle, and due to having similar hemoglobin-related mutations as the humans and canines in the region have. As mentioned earlier, Yaks played an important role in Tibeto-Burman settlement of the Tibetan Plateau.

Summary

Modern Tibeto-Burman speakers in the Tibetan Plateau and in the Himalayan region descend from populations that arrived there during a relatively recent expansion.

Through archaic admixture, the East Asian highland hunter-gatherers became physiologically adapted to high-altitude environments. When they encountered the expanding Yellow River Neolithic-derived farmers at the edges of the Tibetan Plateau, the two populations mingled for a long period of time and the result of this long-term admixture was a population that was well-suited for settlement of a region as demanding as the ones they would go on to permanently inhabit.

In the Tibetan and Sherpa populations, Y-DNA lineages belong to fairly young branches of older haplogroups corresponding perfectly to the expansion of Tibeto-Burman populations into the Tibetan Plateau and the Himalayan region. Similarly, most common Tibeto-Burman paternal haplogroups show clear signs of having undergone founder effects during relatively rapid expansions. So, while the high frequency of haplogroup D-M174 in the Tibetan Plateau today may at first glance appear to be a sign of unbroken Paleolithic continuity, it does in fact represent a resurgence of a bottlenecked lineage that exploded in frequency during the TB expansions into the region and is now represented by very young sublineages. The high frequency of haplogroups O-CTS5308 and Tibeto-Burman subclades of D-M174 in modern populations of the Tibetan Plateau and the Himalayan region serves as a clear display of the fact that this population mastered their ecological niche, adapted successfully and thrived. As a result of that, the population rapidly increased in size and range of distribution.

References:

Jeong, Choongwon et al (2016): Long-term genetic stability and a high-altitude East Asian origin for the peoples of the high valleys of the Himalayan arc https://www.pnas.org/content/113/27/7485

Hung, Ling-yu (2011): Pottery Production, Mortuary Practice, and Social Complexity in the Majiayao Culture, NW China (ca. 5300-4000 BP) https://openscholarship.wustl.edu/etd/589/

Zhang et al. (2017): Differentiated demographic histories and local adaptations between Sherpas and Tibetans https://genomebiology.biomedcentral.com/articles/10.1186/s13059-017-1242-y

Lu et al. (2016): Ancestral Origins and Genetic History of Tibetan Highlanders https://pubmed.ncbi.nlm.nih.gov/27569548/

Jianxin Guo et al. (2021): Genomic insights into Neolithic farming-related migrations in the junction of east and southeast Asia https://onlinelibrary.wiley.com/doi/full/10.1002/ajpa.24434

Qi et al. (2013): Genetic evidence of paleolithic colonization and neolithic expansion of modern humans on the tibetan plateau https://pubmed.ncbi.nlm.nih.gov/23682168/

Jeong, Choongwon et al. (2014): Admixture facilitates genetic adaptations to high altitude in Tibet https://www.nature.com/articles/ncomms4281

Bhandari et al. (2015): Genetic evidence of a recent Tibetan ancestry to Sherpas in the Himalayan region https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4633682/

Zhang et al. (2021): The history and evolution of the Denisovan-EPAS1 haplotype in Tibetans https://www.pnas.org/content/118/22/e2020803118

Zhang et al. (2020): Dated phylogeny suggests early Neolithic origin of Sino-Tibetan languages https://www.nature.com/articles/s41598-020-77404-4

Mengge, Wang et al. (2021): Genomic history and forensic characteristics of Sherpa highlanders on the Tibetan Plateau inferred from high-resolution genome-wide InDels and SNPs https://www.biorxiv.org/content/10.1101/2021.06.23.449553v1

Peiqi Zhang et al. (2021): Denisovans and Homo sapiens on the Tibetan Plateau: dispersals and adaptations https://www.cell.com/trends/ecology-evolution/fulltext/S0169-5347(21)00307-4

Sagart et al. (2019): Dated language phylogenies shed light on the ancestry of Sino-Tibetan https://www.pnas.org/content/116/21/10317

A. H. Dani, V. M. Masson (ed.): History of civilizations of Central Asia. Volume 1. The dawn of civilization: earliest times to 700 B. C. http://archiv.ub.uni-heidelberg.de/propylaeumdok/4096/

Chen et al. (2014): Agriculture facilitated permanent human occupation of the Tibetan Plateau after 3600 B.P https://pubmed.ncbi.nlm.nih.gov/25593179/

Cuiying Li et al. (2018): Investigation of the differences between the Tibetan and Han populations in the hemoglobin-oxygen affinity of red blood cells and in the adaptation to high-altitude environments https://pubmed.ncbi.nlm.nih.gov/29130390/

Beall et al. (1998): Hemoglobin Concentration of High-Altitude Tibetans
and Bolivian Aymara
https://pubmed.ncbi.nlm.nih.gov/9696153/

Ming-Shan Wang et al. (2020): Ancient Hybridization with an Unknown Population Facilitated High-Altitude Adaptation of Canids https://academic.oup.com/mbe/article/37/9/2616/5834723

Signore et al. (2019): Adaptive Changes in Hemoglobin Function in High-Altitude Tibetan Canids Were Derived via Gene Conversion and Introgression https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6759075/

Gayden et al. (2007): The Himalayas as a Directional Barrier to Gene Flow https://www.sciencedirect.com/science/article/pii/S0002929707609446

Ling-Xiang Wang et al. (2018): Reconstruction of Y-chromosome phylogeny reveals two neolithic expansions of Tibeto-Burman populations https://link.springer.com/article/10.1007/s00438-018-1461-2

© Genomic Atlas 2022

Content Protection by DMCA.com

Leave a Reply