Early Pleistocene enamel proteome sequences from Dmanisi resolve Stephanorhinus phylogeny (original) (raw)

Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny

Nature

Ancient DNA (aDNA) sequencing has enabled unprecedented reconstruction of speciation, 55 migration, and admixture events for extinct taxa 1 . Outside the permafrost, however, irreversible 56 aDNA post-mortem degradation 2 has so far limited aDNA recovery within the ~0.5 million years (Ma) 57 time range 3 . Tandem mass spectrometry (MS)-based collagen type I (COL1) sequencing provides 58 direct access to older biomolecular information 4 , though with limited phylogenetic use. In the 59 absence of molecular evidence, the speciation of several Early and Middle Pleistocene extinct 60 species remain contentious. In this study, we address the phylogenetic relationships of the Eurasian 61

Middle Pleistocene protein sequences from the rhinoceros genus Stephanorhinus and the phylogeny of extant and extinct Middle/Late Pleistocene Rhinocerotidae

Background: Ancient protein sequences are increasingly used to elucidate the phylogenetic relationships between extinct and extant mammalian taxa. Here, we apply these recent developments to Middle Pleistocene bone specimens of the rhinoceros genus Stephanorhinus. No biomolecular sequence data is currently available for this genus, leaving phylogenetic hypotheses on its evolutionary relationships to extant and extinct rhinoceroses untested. Furthermore, recent phylogenies based on Rhinocerotidae (partial or complete) mitochondrial DNA sequences differ in the placement of the Sumatran rhinoceros (Dicerorhinus sumatrensis). Therefore, studies utilising ancient protein sequences from Middle Pleistocene contexts have the potential to provide further insights into the phylogenetic relationships between extant and extinct species, including Stephanorhinus and Dicerorhinus. Methods: ZooMS screening (zooarchaeology by mass spectrometry) was performed on several Late and Middle Pleistocene specimens from the genus Stephanorhinus, subsequently followed by liquid chromatography-tandem mass spectrometry (LC-MS/MS) to obtain ancient protein sequences from a Middle Pleistocene Stephanorhinus specimen. We performed parallel analysis on a Late Pleistocene woolly rhinoceros specimen and extant species of rhinoceroses, resulting in the availability of protein sequence data for five extant species and two extinct genera. Phylogenetic analysis additionally included all extant Perissodactyla genera (Equus, Tapirus), and was conducted using Bayesian (MrBayes) and maximum-likelihood (RAxML) methods. Results: Various ancient proteins were identified in both the Middle and Late Pleistocene rhinoceros samples. Protein degradation and proteome complexity are consistent with an endogenous origin of the identified proteins. Phylogenetic analysis of informative proteins resolved the Perissodactyla phylogeny in agreement

Ancient DNA analysis reveals woolly rhino evolutionary relationships

Molecular Phylogenetics and Evolution, 2003

With ancient DNA technology, DNA sequences have been added to the list of characters available to infer the phyletic position of extinct species in evolutionary trees. We have sequenced the entire 12S rRNA and partial cytochrome b (cyt b) genes of one 60-70,000-year-old sample, and partial 12S rRNA and cyt b sequences of two 40-45,000-year-old samples of the extinct woolly rhinoceros (Coelodonta antiquitatis). Based on these two mitochondrial markers, phylogenetic analyses show that C. antiquitatis is most closely related to one of the three extant Asian rhinoceros species, Dicerorhinus sumatrensis. Calculations based on a molecular clock suggest that the lineage leading to C. antiquitatis and D. sumatrensis diverged in the Oligocene, 21-26 MYA. Both results agree with morphological models deduced from palaeontological data. Nuclear inserts of mitochondrial DNA were identified in the ancient specimens. These data should encourage the use of nuclear DNA in future ancient DNA studies. It also further establishes that the degraded nature of ancient DNA does not completely protect ancient DNA studies based on mitochondrial data from the problems associated with nuclear inserts.

Late Pleistocene paleoecology and phylogeography of woolly rhinoceroses

Quaternary Science Reviews, 2021

The woolly rhinoceros (Coelodonta antiquitatis) was a cold-adapted herbivore, widely distributed from western Europe to northeast Siberia during the Late Pleistocene. Previous studies have associated the extinction of the species~14,000 calendar years before present to climatic and vegetational changes, suggesting the later survival of populations in northeast Siberia may have related to the later persistence of open vegetation in the region. Here, we analyzed carbon (d 13 C) and nitrogen (d 15 N) stable isotopes and mitochondrial DNA sequences to elucidate the evolutionary ecology of the species. Our dataset comprised 286 woolly rhinoceros isotopic records, including 192 unpublished records, from across the species range, dating from >58,600 to 12,135 14 C years before present (equivalent to 14,040 calendar years ago). Crucially, we present the first 71 isotopic records available to date of the 15,000 years preceding woolly rhinoceros extinction. The data revealed ecological flexibility and geographic variation in woolly rhinoceros stable isotope compositions across time. In northeast Siberia, we detected stability in d 15 N through time, which could reflect long-term environmental stability, and may have enabled the later survival of the species in the region. To further investigate the paleoecology of woolly rhinoceroses, we compared their isotopic compositions with other contemporary herbivores. Our findings suggested isotopic similarities between woolly rhinoceros and both musk ox (Ovibos moschatus) and saiga (Saiga tatarica), albeit at varying points in time, and possible niche partitioning between woolly rhinoceros and both horse (Equus spp.) and woolly mammoth (Mammuthus primigenius). To provide phylogeographic context to the isotopic data, we compiled and analyzed the 61 published mitochondrial control region sequences. The genetic data showed a lack of geographic structuring; we found three haplogroups with overlapping distributions, all of which showed a signal of expansion during the Last Glacial Maximum. Furthermore, our genetic findings support the notion that environmental stability in Siberia influenced the paleoecology of woolly rhinoceroses in the region. Our study highlights the utility of combining stable isotopic records with ancient DNA to advance our knowledge of the evolutionary ecology of past populations and extinct species.

Late Pleistocene palaeoecology and phylogeography of woolly rhinoceroses

2021

The woolly rhinoceros (Coelodonta antiquitatis) was a cold-adapted herbivore, widely distributed from western Europe to north-east Siberia during the Late Pleistocene. Previous studies associate the extinction of the species ~14,000 years before present to climatic and vegetational changes, and suggest that later survival of populations in north-east Siberia may relate to the later persistence of open vegetation in that region. Here, we analyzed carbon (δ13C) and nitrogen (δ15N) stable isotopes and mitochondrial DNA sequences to elucidate the evolutionary ecology of the species. Our dataset comprised 286 woolly rhinoceros isotopic records, including 192 unpublished records, from across the species range, dating from >58,600 14C years to ~14,000 years before present. Crucially, we present the first 71 isotopic records available to date of the 15,000 years preceding woolly rhinoceros extinction. The data reveal ecological flexibility and geographical variation in woolly rhinoceros ...

Ancient DNA shows high faunal diversity in the Lesser Caucasus during the Late Pleistocene

Quaternary Science Reviews, 2019

In this study, we explore the Late Pleistocene (LP) vertebrate fauna diversity in southeastern Lesser Caucasus based on morphological and genetic identification of fossil bones from Karin Tak cave. For the first time in this under-studied region, we used a bulk bone metabarcoding genetic approach to complement traditional morphology-based taxonomic identification hampered by highly fragmented fossil bones. Excellent ancient DNA (aDNA) preservation allowed for a successful species identification of many bone remains and improved paleoenvironmental interpretations for the region. The identification of fossil bones revealed a high diversity of animal taxa inhabiting the region between ca. > 42,000 and 25,683-24,803 calibrated years before present (cal. BP). The reconstructed taxonomic assemblage comprises 29 taxa, including 11 mammalian and three avian families currently inhabiting the region, together with a few taxa that are regionally extinct today. Despite limited temporal resolution, the taxonomic assemblage identified points to faunal continuity in the study region during the LP. This suggests that the transition between warm and humid Marine Isotope Stage (MIS) 3 and cold and arid MIS 2 did not cause a dramatic change in the faunal makeup of the region.

Reassessing the phylogeny of Quaternary Eurasian Rhinocerotidae

The phylogenetic relationships within Eurasian Quaternary rhinoceroses is reassessed for the first time by means of Bayesian analysis. The results show Stephanorhinus as a monophyletic clade, with Pliorhinus as a sister taxon and Coelodonta as their closest relative. A new scenario on the origin, evolution and paleobiogeography of Quaternary rhinoceroses is therefore provided. Stephanorhinus originated in the Mediterranean Basin, dispersing towards Eastern Eurasia during the Early Pleistocene and leading to S. kirchbergensis. S. hemitoechus probably originated in Europe.

Extinct species identification from Upper Pleistocene bone fragments not identifiable from their osteomorphological studies by proteomics analysis

2020

The ancient preserved molecules offer the opportunity to gain a better knowledge on the biological past. In recent years, bones proteomics has become an attractive method to study the animal biological origin, extinct species and species evolution as an alternative to DNA analysis which is limited by DNA amplification present in ancient samples and its contamination. However, the development of a proteomic workflow remains a challenge. The analysis of fossils must consume a low quantity of material to avoid damaging the samples. Another difficulty is the absence of genomic data for most of the extinct species. In this study, a proteomic methodology was applied to mammalian bones of 130,000 years old from the earlier Upper Pleistocene site of Scladina Cave (Belgium). Starting from 5 milligram samples, our results show a large majority of detected peptides matching collagen I alpha 1 and alpha 2 proteins with a sequence coverage up to 60%. Using sequence homology with modern sequences...

Genotyping of Capreolus pygargus Fossil DNA from Denisova Cave Reveals Phylogenetic Relationships between Ancient and Modern Populations

PLoS ONE, 2011

Background: The extant roe deer (Capreolus Gray, 1821) includes two species: the European roe deer (C. capreolus) and the Siberian roe deer (C. pygargus) that are distinguished by morphological and karyotypical differences. The Siberian roe deer occupies a vast area of Asia and is considerably less studied than the European roe deer. Modern systematics of the Siberian roe deer remain controversial with 4 morphological subspecies. Roe deer fossilized bones are quite abundant in Denisova cave (Altai Mountains, South Siberia), where dozens of both extant and extinct mammalian species from modern Holocene to Middle Pleistocene have been retrieved. Methodology/Principal Findings: We analyzed a 629 bp fragment of the mitochondrial control region from ancient bones of 10 Holocene and four Pleistocene Siberian roe deer from Denisova cave as well as 37 modern specimen belonging to populations from Altai, Tian Shan (Kyrgyzstan), Yakutia, Novosibirsk region and the Russian Far East. Genealogical reconstructions indicated that most Holocene haplotypes were probably ancestral for modern roe deer populations of Western Siberia and Tian Shan. One of the Pleistocene haplotypes was possibly ancestral for modern Yakutian populations, and two extinct Pleistocene haplotypes were close to modern roe deer from Tian Shan and Yakutia. Most modern geographical populations (except for West Siberian Plains) are heterogeneous and there is some tentative evidence for structure. However, we did not find any distinct phylogenetic signal characterizing particular subspecies in either modern or ancient samples. Conclusion/Significance: Analysis of mitochondrial DNA from both ancient and modern samples of Siberian roe deer shed new light on understanding the evolutionary history of roe deer. Our data indicate that during the last 50,000 years multiple replacements of populations of the Siberian roe deer took place in the Altai Mountains correlating with climatic changes. The Siberian roe deer represent a complex and heterogeneous species with high migration rates and without evident subspecies structure. Low genetic diversity of the West Siberian Plain population indicates a recent bottleneck or founder effect.