Revealed for the first time! How do cattle quickly adapt to the extreme environment of the Qinghai-Tibet Plateau?

Produced by: Science Popularization China

author:

Chen Ningbo, Lü Yang, Lei Chuchao (Northwest Agriculture and Forestry University)

Zhang Zhengwei, Lv Hongliang (Sichuan University)

Shungang Chen (Institute of Tibetan Plateau Research, Chinese Academy of Sciences)

Producer: China Science Expo

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The Qinghai-Tibet Plateau is known as the "Roof of the World". With an average altitude of over 4,000 meters, it is also considered the world's third pole. Despite the harsh environment of low temperature, low oxygen and strong ultraviolet rays on the Qinghai-Tibet Plateau, many lives still thrive on this land.

Tibetans living on the Qinghai-Tibet Plateau mainly engage in grazing, and have long raised large domestic animals such as yaks, horses, goats and cattle. Domestic cattle include two subspecies: common cattle (Bos taurus taurus) and zebu cattle (B. t. indicus). Domestic cattle are called yellow cattle in China, which refers to the general term for domestic cattle other than yaks and buffaloes.

In my country, cattle breed resources are very rich. In the National Livestock and Poultry Genetic Resources - Cattle, there are currently 57 local cattle breeds. There are many cattle breeds in the Qinghai-Tibet Plateau, including the Apai Gyatsa cattle, Tibetan cattle, Shigatse humpback cattle and Zhangmu cattle in the Tibet Autonomous Region; Diqing cattle in Yunnan Province, Ganzi cattle in Sichuan Province and Qaidam cattle in Qinghai Province. Due to the complex terrain of the Qinghai-Tibet Plateau, cattle that migrated to the hinterland of the plateau have never migrated to other places on a large scale, thus retaining their original characteristics.

Archaeological and ancient DNA evidence shows that cattle were one of the earliest domesticated animals to enter the Qinghai-Tibet Plateau. They are also the most primitive cattle germplasm resources in China and even in the world. After thousands of years of natural and artificial selection, Qinghai-Tibet Plateau cattle have unique characteristics such as small size, late maturity and adaptation to the plateau climate.

In such an extreme environment, when and where did cattle enter the Qinghai-Tibet Plateau? How did they quickly adapt to the plateau environment? These questions have aroused great interest among scientific researchers.

Yellow cattle on the Qinghai-Tibet Plateau

(Photo credit: Photo taken by Chen Ningbo from Northwest Agriculture and Forestry University)

Origin of Scalpers

Ancient DNA evidence shows that domestic cattle domesticated in the Fertile Crescent of West Asia had entered East Asia at least 3,900 years ago. After entering East Asia, their bloodline also changed. We call them East Asian common cattle, represented by the yellow cattle unearthed from the Shimao site in northern Shaanxi 3,900 years ago.

Genomic evidence also supports that the Shimao cattle are the ancestors of modern Tibetan Plateau cattle and Northeast Asian domestic cattle, such as the Yanbian cattle in Northeast China, Japanese Wagyu and Korean Hanbok.

Domestic cattle groups represented by the Shimao yellow cattle continued to spread after entering China. They spread eastward to China's northeast region, and then entered the Korean Peninsula and Japan; westward to the edge of the Qinghai-Tibet Plateau, and gradually spread to the entire Qinghai-Tibet Plateau region in the following thousands of years. Archaeological and genetic evidence further supports that yellow cattle spread to the Bangga area in the southern hinterland of the Qinghai-Tibet Plateau at least 2,500 years ago.

Yellow cattle raised by herders on the Qinghai-Tibet Plateau

(Photo credit: Photo taken by Chen Ningbo from Northwest Agriculture and Forestry University)

How do cattle adapt to the plateau climate?

Compared with the 10,000-year domestication history of domestic cattle, the Tibetan Plateau cattle may only have a history of 3,000 to 4,000 years. How did the cattle quickly adapt to the plateau environment in such a short period of time? To answer this question, we collected samples from 8 cattle populations on the Tibetan Plateau, a total of 89 cattle, for genome sequencing and analysis.

The collected cattle samples came from the main grazing areas in the northeastern, central and southern regions of the Qinghai-Tibet Plateau, with an altitude between 3,400 and 4,300 meters. We then analyzed the genomic information of other domestic cattle around the world and found that the Qinghai-Tibet Plateau cattle have rich genetic diversity.

Consistent with the geographical distribution of the eight Tibetan Plateau cattle populations, their ancestral lineage composition also showed a continuous change from East Asian common cattle to South Asian zebu cattle.

In the following 3,000 years of reproduction, through the natural selection of the living environment on generations of cattle, the favorable cattle individuals that survived through the mechanism of survival of the fittest were highly adaptable to the environment of the Qinghai-Tibet Plateau. These individuals underwent some slight changes in their genome sequences. So how did these changes occur?

By comparing the genome sequence of cattle from low altitude areas with that of cattle from low altitude areas, we found HMGA2 and NCAPG genes that affect body size in the Qinghai-Tibet Plateau cattle genome. There are two gene mutations with very high frequency in the Qinghai-Tibet Plateau cattle, and these two mutations are almost absent in cattle from low altitude areas, which may be the reason for the smaller body size of Qinghai-Tibet Plateau cattle.

We also found that the DUOXA2 gene involved in energy metabolism also has a high-frequency mutation. This mutation is related to the body energy metabolism of plateau cattle, which can better adapt to the extreme plateau environment by regulating energy metabolism. Therefore, we speculate that these mutations may be the "key code" for the Qinghai-Tibet Plateau cattle to adapt to the plateau environment through natural selection.

However, in just over 3,000 years, it is far from enough to adapt to this extreme environment through natural selection. In order to better adapt to the extreme environment of the Qinghai-Tibet Plateau, the Qinghai-Tibet Plateau cattle chose to "intermarry" with yaks.

Intermarriage

Yaks are known as the "boats of the plateau" and have been the dominant livestock in the pastoral areas of the Qinghai-Tibet Plateau since ancient times. Yaks can make full use of the forage resources of alpine grasslands, have strong adaptability to local ecological and environmental conditions, are resistant to rough feed, and can live freely in harsh environmental conditions such as thin air, cold weather, and short grass growing season.

Yaks and cattle can crossbreed, and their offspring, yaks, are also of great significance to human settlement in extreme high-altitude environments. Yaks, cattle and yaks are not only the main force for plowing and transportation in plateau agriculture, but also have a lot of treasures. Agricultural products such as beef, ghee and yogurt are important food resources. Tents woven with yak hair can withstand the wind, snow and cold, and cow dung is an indispensable main fuel for every family.

So when did the intermarriage between yaks and cattle first begin? Archaeological discoveries at the Bangga site in the southern Qinghai-Tibet Plateau provide us with important clues. The Bangga site is 3,750 meters above sea level, and its early remains date back 2,000 to 3,000 years. It is one of the few high-altitude prehistoric sites in Tibet that has been systematically excavated. Animal archaeological research at the Bangga site found that the Bangga ancestors used both yaks and cattle, and most of the cattle died at an age of more than four years old, which is similar to the use and management of domestic cattle by modern herders on the Qinghai-Tibet Plateau.

Through the chronology and ancient DNA analysis of five cattle bones from the Bangga site, we found that as early as 2,500 years ago, cattle had arrived in Bangga with the migration of our ancestors. At that time, the Bangga ancestors had already begun to experiment with the "intermarriage" of yaks and cattle. So far, this intentional "intermarriage" event has lasted for at least 2,500 years, or even longer, which requires more archaeological evidence in the future.

So what "excellent genes" did the yellow cattle on the Qinghai-Tibet Plateau obtain from the yaks through "intermarriage"? Our further research found that the yellow cattle in different altitudes of the Qinghai-Tibet Plateau have many "excellent genes" of yaks. For example: functional genes related to hypoxia response (EGLN1), cold adaptation (LPR11), DNA damage repair (LATS1) and ultraviolet resistance (GNPAT). These favorable genes have more or less influenced the yellow cattle migrating to the Qinghai-Tibet Plateau through "intermarriage". Coupled with the "teachings and examples" of their ancestors, their offspring are becoming more and more adaptable.

We also found that non-coding region mutations with yak ancestry can change the original "gene expression balance". Once this gene expression balance is changed, the genes that affect high-altitude adaptation will "actively express", so the offspring of cattle after "intermarriage" have stronger adaptability. The "intermarriage" between yaks and cattle is also another "key code" to enhance the ability of cattle on the Qinghai-Tibet Plateau to cope with the plateau environment.

Bangga Archaeological Site

(Photo source: Provided by Professor Lv Hongliang's team from the Archaeological Science Center of Sichuan University)

The hybrid offspring of cattle and yaks - yak

(Photo credit: Photo taken by Chen Ningbo from Northwest Agriculture and Forestry University)

All kinds of cattle are distributed in China. In addition to the cattle, yaks and their hybrid offspring, the yak, which still live on the Qinghai-Tibet Plateau today, are there other cattle that have lived on this vast plateau in the long river of history? What stories do they have with cattle and yaks?

Driven by curiosity, we collected three ancient cattle bones from an archaeological site called Tawendaliha in the northeast of the Qinghai-Tibet Plateau, hoping to find clues and answers. Because these cattle bones have been baptized by nearly three thousand years, we can no longer determine from their morphology what kind of cattle they came from.

Therefore, we once again used ancient DNA technology, hoping to extract the remaining ancient DNA fragments from these cattle bones and use a method similar to "paternity testing" to solve the mystery of their identity.

We successfully obtained the genetic information of these three ancient cattle bones by extracting ancient DNA, amplifying it, and sequencing the genome. By analyzing these ancient genetic information, we found that their mothers were yellow cattle and East Asian aurochs, respectively.

Aurochs, as the name suggests, is a primitive, undomesticated cattle that once lived throughout Eurasia and northern Africa. The ancestors of modern domestic cattle came from the common aurochs in West Asia and the tumoured aurochs in South Asia. Unfortunately, the aurochs became extinct in 1627.

Aurochs refers to a species of aurochs that live in East Asia. So far, no traces of them have been found on the Qinghai-Tibet Plateau. The 3,400-year-old aurochs specimen we found at the Tawintarika site proves that aurochs may have lived freely on the Qinghai-Tibet Plateau for hundreds of years after the arrival of domesticated cattle.

Morphological identification of animal skeletal remains

(Photo credit: Photo taken by Chen Shungang from the Institute of Tibetan Plateau Research, Chinese Academy of Sciences)

Since cattle and East Asian aurochs once met on the Qinghai-Tibet Plateau more than 3,000 years ago, did they also have "close contact" with each other like cattle and yaks? With this question in mind, we further carried out nuclear genome analysis.

Surprisingly, we found that the mitochondria of one sample belonged to the East Asian aurochs, but the nuclear genome was similar to that of the yellow cattle. After further analysis of its ancestral lineage, we found that this individual had 84% of the yellow cattle ancestry and 16% of the East Asian aurochs ancestry, confirming its unique identity as a "hybrid".

At this point, genetics and ancient DNA research have helped us realize that not only did cattle intermarry with yaks, but cattle also intermarried with East Asian aurochs. Even more impressive is that we have also detected yak and East Asian aurochs bloodlines in Bangga cattle, which is the best example of aurochs-cattle-yak "hybridization".

Extracting ancient DNA from samples in an ultra-clean laboratory

(Photo courtesy of Han Xu from the Institute of Tibetan Plateau Research, Chinese Academy of Sciences)

We have collaborated with the Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Archaeological Science Center, Sichuan University, Washington University in St. Louis, China University of Geosciences (Wuhan), Yazhou Bay National Laboratory, Lanzhou University, Jilin Agricultural University, Kunming Institute of Zoology, Chinese Academy of Sciences, and other institutions to publish a series of research on Tibetan Plateau cattle, yaks, yaks, and East Asian aurochs in Nature Communications, Science Advances, and Science Bulletin. This series of research has enriched our understanding of the prehistoric cattle resources on the Qinghai-Tibet Plateau and also helped us understand the "intermarriage" between cattle.

If we want to further explore the mysteries of the evolution of cattle on the Qinghai-Tibet Plateau in the future, we can uncover the mystery of domestic cattle on the Qinghai-Tibet Plateau by further in-depth research on the genomes of modern and ancient samples.

(Note: Latin parts in the text should be italicized)

References:

[1] Ningbo Chen, Xiaoting Xia, Quratulain Hanif, et al. Global genetic diversity, introgression and evolutionary adaptation of indicine cattle revealed by whole genome sequencing. Nature Communications. 2023, 14, 7803.

[2] Ningbo Chen, Zhengwei Zhang, Jiawen Ho, et al. Evidence for early domestic yak, taurine cattle, and their hybrids on the Tibetan Plateau. Science Advances. 2023, 9, eadi6857.

[3] Ningbo Chen, Yudong, Qiuming Chen, et al. Whole-genome resequencing reveals world-wide ancestry and adaptive introgression events of domesticated cattle in East Asia. Nature Communications. 2018, 9, 2337.

[4] Shungang Chen, Lele Ren, Yu Gao, et al. Evidence of hybridization of cattle and aurochs on the Tibetan Plateau ~3750 years ago. Science Bulletin, 2024.

[5] Yang Lyu, Fuwen Wang, Haijian Cheng, et al. Recent selection and introgression facilitated high-altitude adaptation in cattle. Science Bulletin, 2024.