The origin and evolution of woolly rhinoceros in the view of ancient DNA

Woolly rhinoceros is one of the most popular species of the Ice Age, which has been attracting great interests from both the scientific community and the public. In recent years, technical advances in ancient DNA have provided powerful tools for exploring the evolution of this extinct star species.

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Ancient mitogenomes reveal a high maternal genetic diversity of Pleistocene woolly rhinoceros in Northern China - BMC Ecology and Evolution

Background Woolly rhinoceros (Coelodonta antiquitatis) is a typical indicator of cold-stage climate that was widely distributed in Northern Hemisphere during the Middle-Late Pleistocene. Although a plethora of fossils have been excavated from Northern China, their phylogenetic status, intraspecific diversity and phylogeographical structure are still vague. Results In the present study, we generated four mitogenomes from Late Pleistocene woolly rhinoceros in Northern China and compared them with published data. Bayesian and network analyses indicate that the analyzed individuals contain at least four maternal haplogroups, and Chinese samples fall in three of them. One of our samples belongs to a previously unidentified early diverging clade (haplogroup D), which separated from other woolly rhinoceros around 0.57 Ma (95% CI: 0.76–0.41 Ma). The timing of this clade’s origin coincides with the first occurrence of woolly rhinoceros, which are thought to have evolved in Europe. Our other three samples cluster in haplogroup C, previously only identified from one specimen from Wrangel Island (ND030) and initially considered to be an isolated clade. Herein, our findings suggest that ND030 is likely descended from a northward dispersal of the individuals carrying haplogroup C from Northern China. Additionally, Chinese woolly rhinoceros specimens exhibit higher nucleotide diversity than those from Siberia. Conclusion Our findings highlight Northern China as a possible refugium and a key evolution center of the Pleistocene woolly rhinoceros.

The rhino family once evolved into at least 100 species, inhabited from Africa across Eurasia to America, while only five critically endangered species surviving at present. Among the extinct rhino species, woolly rhinoceros (Coelodonta antiquitatis) is the most well-known one, which became extinct at the end of the Late Pleistocene. Woolly rhinoceros is an advanced species of the genus Coelodonta. The earliest representative of this genus, Coelodonta thibetana (~3.7 million years ago, Ma), originated in Qing-Tibetan Plateau, Southwestern China, then gradually evolved into different cold-adapt forms in Northern China since the start of Ice Age. Woolly rhinoceros is generally suggested as a typical indicator taxa of cold environments, and once widely distributed in Northern Eurasia during the Late Pleistocene. Unlike mammoth, it failed to cross the Bering Land Bridge from Eurasia into North America.

Figure 1. Parts of unearthed woolly rhinoceros remains from Ulanmulun Paleolithic site, Inner Mongolia, Northern China. Credit: Lei Bao

Northern China is famous for “Mammuthus-Coelodonta faunas” during the Late Pleistocene, and abundant woolly rhinoceros fossil materials have been excavated from the Late Pleistocene strata in this region. Given the early members of the genus Coelodonta originated in Northern China and numerous woolly rhinoceros remains excavated in this region, Northern China holds a crucial importance in the evolutionary history of this genus. Paleontologists carried out a series of exploration on fossil materials of Coelodonta in terms of morphological analyses, and previously proposed that Chinese woolly rhinoceros possibly descended from its Siberian relatives.

Figure 2. Qinggang County, Heilongjiang Province——one of the most important fossil localities of “Mammuthus-Coelodonta faunas” in China. Credit: Bo Xiao

In recent years, the rapid development of ancient DNA technologies, especially the metagenomic technology, have greatly increased the length of obtained sequences, making it possible to retrieve whole genomes from fossil materials. Until present, the outcomes of paleogenomic studies have fundamentally changed our understanding of the evolutionary history of many extinct/extant species. Especially, woolly mammoth, as one of the iconic members of “Mammuthus-Coelodonta faunas”, has become a model species for ancient DNA study due to its widespread distribution in Northern Hemisphere, while woolly rhinoceroses has received far less attention in the molecular level.

Our team has been dedicated to DNA studies of Chinese Pleistocene-Holocene vertebrates over the past two decades, trying to explore the evolutionary history of the analyzed populations. We have focused on members of “Mammuthus-Coelodonta faunas” from Northern China, such as woolly mammoth, straight-tusked elephant, steppe bison, Ovodov horse, Przewalski׳s horse, red deer, roe deer, tiger, and cave hyenas as well. Molecular studies suggested several ancient Chinese populations showed close relationship to their Siberian relatives. With regards to woolly rhinoceros, where did the Chinese woolly rhinoceros come from? What is the exact phylogenetic status of the Chinese woolly rhinoceros from a genetic perspective? How about the genetic diversity level of Chinese individuals? To figure out problem solving possibilities, we carried out ancient DNA study on Chinese woolly rhinoceros individuals at about ten years ago. Unfortunately, only several fragment sequences were obtained from the analyzed samples at that time. However, the initial results and context of our previous ancient DNA studies on other Pleistocene mammals greatly sparked our interest in studying the genetic evolution of woolly rhinoceros.

Figure 3. Salawusu, Inner Mongolia, Northern China——with a high proportion of woolly rhinoceros fossils from the Late Pleistocene strata in this region. Credit: Taogetongqimuge

With help of our collaborators, we collected Late Pleistocene woolly rhinoceros remains from seven locations distributed in Northern China. We reconstructed the maternal phylogenetic trees based on the newly obtained mitochondrial genomes and previous published data using Bayesian and network analyses. Surprisingly, we found three Chinese samples cluster with one Wrangel Island sample and form a distinct maternal clade that previously proposed as an isolated lineage. Another surprise comes from the appearance of the oldest mitochondrial lineage of woolly rhinoceroses in Inner Mongolia, China. Moreover, the Late Pleistocene woolly rhinoceros individuals in Northern China have relatively high maternal genetic diversity compared with their Siberian relatives.

Figure 4. Xinbarhu Left Banner, Inner Mongolia, Northern China——the known habitat of the basal woolly rhinoceros lineage. Credit: Longmei Bao

In summary, our new genetic data not only indicates the surprising result that Northern China could be an important evolutionary center for woolly rhinoceroses during the Pleistocene, but also suggests that this famous extinct rhino possibly originated in this region rather than in Europe that derived from fossil records. Although our preliminary study has only uncovered the tip of the iceberg on the evolutionary history of this rhino species, our findings herein highlight that ancient DNA sequences from Chinese individuals are very important for revealing the full picture of the evolution of woolly rhinoceros, which will also have the enlightenment significance for exploring the evolutionary history of the other members of “Mammuthus-Coelodonta faunas” under the influence of global climate and environmental changes in Quaternary.

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