Turns Out, Early Humans Not the Cause of Woolly Rhinoceros Extinction

Paleogenomics (the use of genetic analysis of DNA contained in ancient remains) has developed rapidly since Svante Pääbo first showed that DNA could be extracted in sufficient quantity and of sufficient quality to be useful in making evolutionary comparisons between, inter alia, modern Homo sapiens sapiens and Homo sapiens neanderthalis. See Krings, Stone, Schmitz, Krainitzki, Stoneking, and Pääbo, "Neandertal DNA sequences and the origin of modern humans," Cell. 90(1): 19–30 (1997). Since then, ancient DNA (both genomic, gDNA, and mitochondrial, mtDNA) have been used to establish relationships, geographic localization, and patterns of extinction. One such pattern involves the wooly rhinoceros (Coelodonta antiquitatis) whose extinction was believed to have arisen at the predacious hand of human beings.

But in a recent paper, an international team of scientists* found this not to be the case. The paper, entitled "Pre-extinction Demographic Stability and Genomic Signatures of Adaptation in the Wooly Rhinoceros," Current Biology (2020), presented evidence that this is not the case. Wooly rhinoceros populations in northern Siberia went extinct about 14,000 years ago. The species were "widely distributed" in northern Eurasia in late Pleistocene (2.58 million to 11,700 years ago). These researchers determined the sequence of one sample of genome gDNA (from an ~18,500 year old specimen) and 14 mtDNA samples ranging in age from more than 50,000 years ago to about 14,000 years ago. These authors identified more than 28 million single nucleotide polymorphisms (SNPs) in the gDNA sample, having an average heterozygosity of 1.7 sites per 1000 basepairs, which is higher than what has been reported for the mammoth genome (1.25 heterozygous sites/1000bp), the Sumatran rhinoceros Dicerorhinus sumatrensis (their closest living relative) (1.3 heterozygous sites/1000bp), or the Northern or Southern White rhinoceros (1.1 and 0.9 heterozygous sites/1000bp, respectively). Runs of homozygosity (ROH) analysis was also consistent with relatively low levels of inbreeding, "on par with non-African human populations," although higher than that detected in the mainland mammoth from this period.

A closer sequence comparison between the gDNA from the wooly rhinoceros and the Sumatran rhinoceros of 19,556 coding genes showed 1,524 genes with non-synonymous mutations, consisting of 1,386 missense mutations and 138 with loss-of-function or non-sense mutations. These genes were associated with "cellular component organization or biogenesis, cellular process, localization, reproduction, biological regulation, response to stimulus, developmental processes, and metabolic processes." Not detected were such mutations in genes relating to fat deposition or circadian rhythm changes, which was different from the patterns found inter alia in wooly mammoth. There were 89 genes in both wooly mammoth and wooly rhinoceros that showed non-synonymous mutations, including Transient Receptor Potential subfamily A (involved in adaptation to cold tolerance), and a member of potassium channel subfamily K analogous to TWIK-Related Arachidonic Acid-Stimulated Potassium Channel Protein involved in cold perception. Finally, a more in-depth assessment of the amino acid sequence changes these mutations caused (and their expected effects on encoded protein structure) showed 284 variants of the 17,888 genes analyzed having maximal change in protein structure, and 83 of these were in olfactory receptor genes.

Shown below (in panel A) are the regions where the sample were obtained. The importance of this Siberian region during interglacial periods in the Pleistocene is reflected in the putative origination of extant wolf species** in northeastern Siberia, highly divergent mtDNA lineages in horse, bison, and collared lemming populations, and admixing of human populations in the region prior to colonialization of North America (see "Genetic Research Continues to Reveal Ancestry Relationships in Early Human Migrations").

Population genetic studies based on comparative mtDNA sequencing revealed a pattern of the development of two clades having the geographic distribution shown in panel B:

Panel B shows the phylogenetic relationship between the 14 specimens; the two main branches diverged ~205,000 years ago, with the Wangel Island branch diverging about 154,00 years ago (consistent with its island location). The structure of the interrelationships between the various related groups consistent with isolation during interglacial periods. The diversification in each branch estimated to have arisen between 86,000 and 22,000 years ago.

Population genetic analysis via mtDNA showed a stable population without evidence on inbreeding or reduction in genetic heterogeneity that would have been indicative of being driven to extinction through, for example, human hunting. Indeed, the population remained stable until about 4,500 years before the extinction event after an initial increase in population. The effective population size increased gradually (i.e., there was no evidence of a population explosion) beginning at around 1 million years ago, reaching a peak of around 21,000 animals about 152,000 years ago during the Marine Isotope Stage 6 (MIS6) glaciation. Thereafter, population size decreased 10-fold fold from 152,000 to 29,700 years ago, experiencing a minimum size at about 33,000 years ago. The population then experienced a rapid expansion resulting in a stable population size until 4,500 prior to the extinction event. These population dynamics are not shared by the wooly mammoth during this period. This suggests that the wooly rhinoceros was particularly well-adapted to the climate during this period, and thus relatively more susceptible to population decline as a consequence of population changes with climate warming. Overall, the authors' assessment was that this population pattern was more indicative of changes in climate, i.e., warming during the interglacial period with changes in local flora used by these animals as a food source.

The authors conclude that:

[O]ur analyses of nuclear and mitochondrial genomic diversity in the woolly rhinoceros provide no evidence for a decline in population size preceding the samples analyzed here, nor any indication of elevated inbreeding typical of small populations. While we cannot exclude the role of humans in woolly rhinoceros' extinction, our results imply that the arrival of anatomically modern humans in northeastern Siberia was not correlated with a demographic decline in the woolly rhinoceros.

The paper concludes with these thoughts:

Taken together, these findings highlight the utility of genomic data in unraveling previously unknown evolutionary processes in extinct species and illustrate the need to investigate demographic trajectories in other megafauna to develop a better understanding of the timing and rate of demographic change during the Late Quaternary.

* Edana Lord, Nicolas Dussex, Marcin Kierczak, David Díez-del-Molino, Oliver A. Ryder David W.G. Stanton, M. Thomas P. Gilbert, Fátima Sánchez-Barreiro ,Guojie Zhang, Mikkel-Eske Willerslev, Albert Protopopov, Fedor Shidlovskiy, Sergey Fedorov, Hervé Bocherens, Senthilvel K.S.S. Nathan, Benoit Goossens, Johannes van der Plicht, Yvonne L. Chan, Stefan Prost, Olga Potapova, Irina Kirillova, Adrian M. Lister, Peter D. Heintzman, Joshua D. Kapp, Beth Shapiro, Sergey Vartanyan, Anders Götherström, and Love Dalén

** In an uncanny coincidence, CNN reported today that a "perfectly preserved" wolf pup, dating from ~14,000 years ago, was found to have wooly rhino meat in his stomach, thus providing another suspect for their extinction. See CNN report.

Image of Reconstruction of Wooly Rhinoceros - Coelodonta antiquitatis, from Late Pleistocene of Europe and Asia by ДиБгд, from the Wikimedia Commons under the Creative Commons Attribution-Share Alike 4.0 International license.