Evolution and extinction of the giant rhinoceros Elasmotherium sibiricum sheds light on late Quaternary megafaunal extinctions

Abstract

Understanding extinction events requires an unbiased record of the chronology and ecology of victims and survivors. The rhinoceros Elasmotherium sibiricum, known as the 'Siberian unicorn', was believed to have gone extinct around 200 ka, well before the Late Quaternary megafaunal extinction event. However, no absolute dating, genetic analysis, or quantitative ecological assessment of this species has been undertaken. Here we show, by AMS radiocarbon dating of 23 individuals, including cross-validation by compound specific analysis, that E. sibiricum survived in Eastern Europe and Central Asia until at least 39 ka BP, corroborating a wave of megafaunal turnover prior to the Last Glacial Maximum in Eurasia, in addition to the better-known Late-glacial event. Stable isotope data indicate a dry steppe niche for E. sibiricum and, together with morphology, a highly specialised diet that likely contributed to its extinction. We further demonstrate, with DNA sequence data, a very deep phylogenetic split between the subfamilies Elasmotheriinae and Rhinocerotinae that includes all the living rhinos, settling a debate based on fossil evidence and confirming that the two lineages had diverged by the Eocene. As the last surviving member of the Elasmotheriinae, the demise of the 'Siberian unicorn' marked the extinction of this subfamily. The rhinoceros family (Rhinocerotidae) was formerly much more diverse than it is today, with some 250 named species 1 of which only five survive. During the Miocene (ca. 23-5 Ma), rhinos were a dominant part of the large mammal fauna in Africa, Eurasia, and North America. Phylogenetic analysis of fossil species has resolved two main lineages: the Rhinocerotinae, which includes all living species and the recently-extinct woolly rhinoceros (Coelodonta antiquitatis), and the extinct Elasmotheriinae 2. Based on morphological diagnoses of early remains, the two subfamilies are thought to have diverged very early in rhinoceros evolution, by at latest 35 Ma 2,3. The Elasmotheriinae subsequently gave rise to some 20 genera, of which only Elasmotherium survived the Miocene, with E. sibiricum its last surviving member, although some authors have separated Elasmotherium from other members of the group and place it within Rhinocerotinae 4,5. A spectacular megafaunal species of Eurasia, at ca. 3.5 tonnes, E. sibiricum was the largest Quaternary rhinoceros. E. sibiricum was also remarkable in its anatomy: relatively slender limbs indicating adaptation for running, despite its mass 6 ; absence of incisors and canines; and-uniquely among rhinos-continuously-growing cheek-teeth with distinctive, highly convoluted enamel plates. The presence of a massive single horn in Elasmotherium has been inferred from the bony protuberance on the frontal bone of the skull which implies a horn base much larger than in any other rhino, living or extinct; hence the informal name 'Siberian unicorn' (Fig. 1). The known geographical ranges of both E. sibiricum and related (in some cases possibly synonymous) Elasmotherium species ...

The origin of Rhinocerotoidea and phylogeny of Ceratomorpha (Mammalia, Perissodactyla)

“…8). Both estimates are earlier than current fossil evidence, but the former estimate is close to the divergence time between Rhinocerotoidea and Tapiroidea (57.5 Mya) based on recent molecular analysis 3 . Similarly, the divergences time of different groups within Lophialetidae, Tapiroidea, and Rhinocerotoidea (s.s.) are in the early Eocene, and the divergence between Deperetellidae and Rhinocerotoidea (s.s.) occurred 54.6 Mya (Fig.…”

“…The new rhinocerotoid taxa Y. magna, as well as reassigned Minchenoletes, from the early Eocene Bumbanian is nearly contemporary with early Eocene tapiroids, suggesting that the divergence between rhinocerotoids and tapiroids occurred no later than the early Eocene (52)(53)(54)(55)(56). The divergence time between Rhinocerotoidea and Tapiroidea in the early early Eocene based on fossil evidence here falls between the~51 Mya and~57.5 Mya estimates from molecular data 2,3 . Furthermore, forstercooperiid Gobioceras, rhinocerotoid Triplopus?…”

“…oth morphological and molecular studies support the idea that Rhinocerotoidea and Tapiroidea form a monophyletic group Ceratomorpha [1][2][3] . The ceratomorphs have abundant, diverse fossil records in the Cenozoic; however, extant ceratomorphs are reduced to five genera and on the brink of extinction.…”

Utilizing field collected insects for next generation sequencing: Effects of sampling, storage, and DNA extraction methods

“…Tremendous biological insight can be gained from specimens which may have degraded DNA due to environmental or storage conditions including road-killed specimens (Rusterholz, Ursenbacher, Coray, Weibel, & Baur, 2015;Say, Devillard, Léger, Pontier, & Ruette, 2012), shed substances including feces, feathers, or fur (Alda et al, 2013;Hans et al, 2015;Waits & Paetkau, 2005), as well as museum and herbarium specimens (Beck & Semple, 2015;Gilbert, Moore, Melchior, & Worobey, 2007;Sproul & Maddison, 2017). Recent work on ancient specimens has revealed great potential for NGS with very limited amounts of highly degraded DNA (Heintzman et al, 2015;Knapp & Hofreiter, 2010;Kosintsev et al, 2018), although most ancient studies focus on large vertebrate taxa (but see Heintzman, Elias, Moore, Paszkiewicz, & Barnes, 2014). Thus, there is a need for better understanding more taxonomically diverse groups, like insects, which represent an estimated 40% of the world's non-microbial biodiversity (Scheffers, Joppa, Pimm, & Laurance, 2012), but have limited markerbased resources and typically need to be dried and pinned before expert identification is possible (Wheeler & Miller, 2017), possibly leading to greater DNA degradation than in other taxa.…”

Palaeogenomics of the Hydrocarbon Producing Microalga Botryococcus braunii

“…The purification and analysis of ancient DNA (aDNA) from preserved materials has recently transformed our understanding of the phylogenies and migration patterns of extinct megafauna 22–24 and humans 25,26 . Microfossils are much more common in sediment cores and widely used as proxies of environmental change but have not yet been subject to targeted genomic analysis.…”