Inferring phylogenetic structure, taxa hybridization, and divergence times within rock voles of subgenus Aschizomys (Cricetidae: Alticola) using quaddRAD sequencing and a cytb dataset.

The subgenus Aschizomys belongs to the genus Alticola (Central Asian mountain vole) and consists of two species: Alticola macrotis and Alticola lemminus. Phylogenetic relationships within the subgenus Aschizomys remain obscure due to limited sampling, an insufficient number of molecular markers used in phylogenetic studies, and paraphyly observed on mitochondrial trees. In this work, to infer reliable phylogenetic relationships and evaluate putative scenarios of ancient hybridization within the subgenus, we applied double-digest restriction site-associated DNA paired-end (quaddRAD) sequencing to 20 DNA samples (20 individuals), including five species of the genus Alticola, and dated the divergence of cytochrome b (cytb) lineages within Aschizomys using a "second calibration" approach. We showed monophyly of the two species on the basis of thousands of nuclear loci and demonstrated traces of introgression also in the nuclear genome. Observed paraphyly in cytb could be explained by an introgression event rather than incomplete lineage sorting. This explanation was confirmed by an analysis of the cytb divergence time. Overall, our results support the hypothesis of extensive migration of the Aschizomys species during the Late Pleistocene, with this migration leading to population divergence and introgression. We expect our article to become a starting point for a series of rigorous studies on the population history of the genus Alticola as a whole.

In Search of the Elusive North: Evolutionary History of the Arctic Fox (Vulpes lagopus) in the Palearctic from the Late Pleistocene to the Recent Inferred from Mitogenomic Data.

Despite the high level of interest, the population history of arctic foxes during the Late Pleistocene and Holocene remains poorly understood. Here we aimed to fill gaps in the demographic and colonization history of the arctic fox by analyzing new ancient DNA data from fossil specimens aged from 50 to 1 thousand years from the Northern and Polar Urals, historic DNA from museum specimens from the Novaya Zemlya Archipelago and the Taymyr Peninsula and supplementing these data by previously published sequences of recent and extinct arctic foxes from other regions. This dataset was used for reconstruction of a time-calibrated phylogeny and a temporal haplotype network covering four time intervals: Late Pleistocene (ranging from 30 to 13 thousand years bp), Holocene (ranging from 4 to 1 thousand years bp), historical (approximately 150 years), and modern. Our results revealed that Late Pleistocene specimens showed no genetic similarity to either modern or historical specimens, thus supporting the earlier hypothesis on local extinction rather than habitat tracking.

Population dynamics and demographic history of Eurasian collared lemmings.

BACKGROUND: Ancient DNA studies suggest that Late Pleistocene climatic changes had a significant effect on population dynamics in Arctic species. The Eurasian collared lemming (Dicrostonyx torquatus) is a keystone species in the Arctic ecosystem. Earlier studies have indicated that past climatic fluctuations were important drivers of past population dynamics in this species. RESULTS: Here, we analysed 59 ancient and 54 modern mitogenomes from across Eurasia, along with one modern nuclear genome. Our results suggest population growth and genetic diversification during the early Late Pleistocene, implying that collared lemmings may have experienced a genetic bottleneck during the warm Eemian interglacial. Furthermore, we find multiple temporally structured mitogenome clades during the Late Pleistocene, consistent with earlier results suggesting a dynamic late glacial population history. Finally, we identify a population in northeastern Siberia that maintained genetic diversity and a constant population size at the end of the Pleistocene, suggesting suitable conditions for collared lemmings in this region during the increasing temperatures associated with the onset of the Holocene. CONCLUSIONS: This study highlights an influence of past warming, in particular the Eemian interglacial, on the evolutionary history of the collared lemming, along with spatiotemporal population structuring throughout the Late Pleistocene.

A mitochondrial genome phylogeny of voles and lemmings (Rodentia: Arvicolinae): Evolutionary and taxonomic implications.

Arvicolinae is one of the most impressive placental radiations with over 150 extant and numerous extinct species that emerged since the Miocene in the Northern Hemisphere. The phylogeny of Arvicolinae has been studied intensively for several decades using morphological and genetic methods. Here, we sequenced 30 new mitochondrial genomes to better understand the evolutionary relationships among the major tribes and genera within the subfamily. The phylogenetic and molecular dating analyses based on 11,391 bp concatenated alignment of protein-coding mitochondrial genes confirmed the monophyly of the subfamily. While Bayesian analysis provided a high resolution across the entire tree, Maximum Likelihood tree reconstruction showed weak support for the ordering of divergence and interrelationships of tribal level taxa within the most ancient radiation. Both the interrelationships among tribes Lagurini, Ellobiusini and Arvicolini, comprising the largest radiation and the position of the genus Dinaromys within it also remained unresolved. For the first time complex relationships between genus level taxa within the species-rich tribe Arvicolini received full resolution. Particularly Lemmiscus was robustly placed as sister to the snow voles Chionomys in the tribe Arvicolini in contrast with a long-held belief of its affinity with Lagurini. Molecular dating of the origin of Arvicolinae and early divergences obtained from the mitogenome data were consistent with fossil records. The mtDNA estimates for putative ancestors of the most genera within Arvicolini appeared to be much older than it was previously proposed in paleontological studies.

Searching for signatures of positive selection in cytochrome b gene associated with subterranean lifestyle in fast-evolving arvicolines (Arvicolinae, Cricetidae, Rodentia).

BACKGROUND: Mitochondrial genes encode proteins involved in oxidative phosphorylation. Variations in lifestyle and ecological niche can be directly reflected in metabolic performance. Subterranean rodents represent a good model for testing hypotheses on adaptive evolution driven by important ecological shifts. Voles and lemmings of the subfamily Arvicolinae (Rodentia: Cricetidae) provide a good example for studies of adaptive radiation. This is the youngest group within the order Rodentia showing the fastest rates of diversification, including the transition to the subterranean lifestyle in several phylogenetically independent lineages. RESULTS: We evaluated the signatures of selection in the mitochondrial cytochrome b (cytB) gene in 62 Arvicolinae species characterized by either subterranean or surface-dwelling lifestyle by assessing amino acid sequence variation, exploring the functional consequences of the observed variation in the tertiary protein structure, and estimating selection pressure. Our analysis revealed that: (1) three of the convergent amino acid substitutions were found among phylogenetically distant subterranean species and (2) these substitutions may have an influence on the protein complex structure, (3) cytB showed an increased ω and evidence of relaxed selection in subterranean lineages, relative to non-subterranean, and (4) eight protein domains possess increased nonsynonymous substitutions ratio in subterranean species. CONCLUSIONS: Our study provides insights into the adaptive evolution of the cytochrome b gene in the Arvicolinae subfamily and its potential implications in the molecular mechanism of adaptation. We present a framework for future characterizations of the impact of specific mutations on the function, physiology, and interactions of the mtDNA-encoded proteins involved in oxidative phosphorylation.

Phylogenetic relationships and taxonomic position of genus Hyperacrius (Rodentia: Arvicolinae) from Kashmir based on evidences from analysis of mitochondrial genome and study of skull morphology.

In this article, we present the nearly complete mitochondrial genome of the Subalpine Kashmir vole Hyperacrius fertilis (Arvicolinae, Cricetidae, Rodentia), assembled using data from Illumina next-generation sequencing (NGS) of the DNA from a century-old museum specimen. De novo assembly consisted of 16,341 bp and included all mitogenome protein-coding genes as well as 12S and 16S RNAs, tRNAs and D-loop. Using the alignment of protein-coding genes of 14 previously published Arvicolini tribe mitogenomes, seven Clethrionomyini mitogenomes, and also Ondatra and Dicrostonyx outgroups, we conducted phylogenetic reconstructions based on a dataset of 13 protein-coding genes (PCGs) under maximum likelihood and Bayesian inference. Phylogenetic analyses robustly supported the phylogenetic position of this species within the tribe Arvicolini. Among the Arvicolini, Hyperacrius represents one of the early-diverged lineages. This result of phylogenetic analysis altered the conventional view on phylogenetic relatedness between Hyperacrius and Alticola and prompted the revision of morphological characters underlying the former assumption. Morphological analysis performed here confirmed molecular data and provided additional evidence for taxonomic replacement of the genus Hyperacrius from the tribe Clethrionomyini to the tribe Arvicolini.

The complete mitochondrial genomes of three Ellobius mole vole species (Rodentia: Arvicolinae).

The subterranean voles of the genus Ellobius are species of subfamily Arvicolinae well adapted to underground life. In this paper, we report the assemblies of complete mitochondrial genomes for three mole voles from genus Ellobius - northern mole vole Ellobius talpinus (16,376 bp), transcaucasian mole vole E. lutescens (16,540 bp), and southern mole vole E. fuscocapillus (16,388 bp). Each of three mitogenomes encode for 12S and 16S rRNAs, 22 tRNAs, 13 protein-coding genes, and D-loop in the characteristic arrangement of subfamily Arvicolinae (Rodentia: Cricetidae). This study verifies the evolutionary status of subgenera Bramus and Ellobius within the genus Ellobius at the molecular level. The mitochondrial genome would be a significant supplement for the Ellobius genetic background. The three Ellobius species formed a monophyletic group with the high bootstrap value (100%) in all examinations.

Evolutionary history of mountain voles of the subgenus Aschizomys (Cricetidae, Rodentia), inferred from mitochondrial and nuclear markers.

In this study, we present an assessment of the evolutionary history and phylogenetic relationships of Asian mountain voles of the subgenus Aschizomys, genus Alticola, based on extensive sampling and phylogenetic analyses of data from mitochondrial and nuclear markers. Two species of this subgenus are widespread in the mountain areas of north-eastern Asia. However, both their distribution and taxonomic borders remained questionable for more than 100 years. Our study showed discordance in the phylogenetic patterns between nuclear and mtDNA markers. We found that mtDNA in A. lemminus is paraphyletic relative to A. macrotis, but nuclear markers demonstrated reciprocal monophyly. According to species distribution modeling, ranges of A. macrotis and A. lemminus experienced a secondary contact during the Last Glacial Maximum (approximately 22 kyr BP), and thus a hybridization event seems plausible during that period. Species tree analyses recovered a sister group relationship between the two species of the Aschizomys subgenus, with an estimated divergence date of around 0.8 Ma. Our results provided good support for currently recognized subspecies within both A. macrotis and A. lemminus based on mitochondrial and nuclear datasets. A new, yet undescribed form, supposedly of a subspecific status within A. lemminus, was found in the Bureinskiy Range in the Khabarovsk area. This finding expands the current species distribution range further to the southeast.

The complete mitochondrial genome of the common pine vole Terricola subterraneus (Arvicolinae, Rodentia).

In this paper, we report the complete mitochondrial genome of the common pine vole Microtus (Terricola) subterraneus, which was sequenced for the first time using Illumina next-generation sequencing (NGS) technology. The total length of the mitogenome was 16,398 bp and contained 12S, 16S rRNAs, 22 tRNAs, 13 protein-coding genes, and a 883 bp D-loop in the characteristic arrangement of subfamily Arvicolinae, Rodentia. Overall base composition of the complete mitochondrial DNA is A (33.0%), C (26.5%), G (13.4%), and T (27.0%), respectively. Phylogenetic analysis of mitochondrial genomes showed a classic taxon pattern, identified using individual phylogenetic markers.

Synchronous genetic turnovers across Western Eurasia in Late Pleistocene collared lemmings.

Recent palaeogenetic studies indicate a highly dynamic history in collared lemmings (Dicrostonyx spp.), with several demographical changes linked to climatic fluctuations that took place during the last glaciation. At the western range margin of D. torquatus, these changes were characterized by a series of local extinctions and recolonizations. However, it is unclear whether this pattern represents a local phenomenon, possibly driven by ecological edge effects, or a global phenomenon that took place across large geographical scales. To address this, we explored the palaeogenetic history of the collared lemming using a next-generation sequencing approach for pooled mitochondrial DNA amplicons. Sequences were obtained from over 300 fossil remains sampled across Eurasia and two sites in North America. We identified five mitochondrial lineages of D. torquatus that succeeded each other through time across Europe and western Russia, indicating a history of repeated population extinctions and recolonizations, most likely from eastern Russia, during the last 50 000 years. The observation of repeated extinctions across such a vast geographical range indicates large-scale changes in the steppe-tundra environment in western Eurasia during the last glaciation. All Holocene samples, from across the species' entire range, belonged to only one of the five mitochondrial lineages. Thus, extant D. torquatus populations only harbour a small fraction of the total genetic diversity that existed across different stages of the Late Pleistocene. In North American samples, haplotypes belonging to both D. groenlandicus and D. richardsoni were recovered from a Late Pleistocene site in south-western Canada. This suggests that D. groenlandicus had a more southern and D. richardsoni a more northern glacial distribution than previously thought. This study provides significant insights into the population dynamics of a small mammal at a large geographical scale and reveals a rather complex demographical history, which could have had bottom-up effects in the Late Pleistocene steppe-tundra ecosystem.

Evolutionary Genomics and Conservation of the Endangered Przewalski's Horse.

Przewalski's horses (PHs, Equus ferus ssp. przewalskii) were discovered in the Asian steppes in the 1870s and represent the last remaining true wild horses. PHs became extinct in the wild in the 1960s but survived in captivity, thanks to major conservation efforts. The current population is still endangered, with just 2,109 individuals, one-quarter of which are in Chinese and Mongolian reintroduction reserves [1]. These horses descend from a founding population of 12 wild-caught PHs and possibly up to four domesticated individuals [2-4]. With a stocky build, an erect mane, and stripped and short legs, they are phenotypically and behaviorally distinct from domesticated horses (DHs, Equus caballus). Here, we sequenced the complete genomes of 11 PHs, representing all founding lineages, and five historical specimens dated to 1878-1929 CE, including the Holotype. These were compared to the hitherto-most-extensive genome dataset characterized for horses, comprising 21 new genomes. We found that loci showing the most genetic differentiation with DHs were enriched in genes involved in metabolism, cardiac disorders, muscle contraction, reproduction, behavior, and signaling pathways. We also show that DH and PH populations split ∼45,000 years ago and have remained connected by gene-flow thereafter. Finally, we monitor the genomic impact of ∼110 years of captivity, revealing reduced heterozygosity, increased inbreeding, and variable introgression of domestic alleles, ranging from non-detectable to as much as 31.1%. This, together with the identification of ancestry informative markers and corrections to the International Studbook, establishes a framework for evaluating the persistence of genetic variation in future reintroduced populations.

On the origin of the Norwegian lemming.

The Pleistocene glacial cycles resulted in significant changes in species distributions, and it has been discussed whether this caused increased rates of population divergence and speciation. One species that is likely to have evolved during the Pleistocene is the Norwegian lemming (Lemmus lemmus). However, the origin of this species, both in terms of when and from what ancestral taxon it evolved, has been difficult to ascertain. Here, we use ancient DNA recovered from lemming remains from a series of Late Pleistocene and Holocene sites to explore the species' evolutionary history. The results revealed considerable genetic differentiation between glacial and contemporary samples. Moreover, the analyses provided strong support for a divergence time prior to the Last Glacial Maximum (LGM), therefore likely ruling out a postglacial colonization of Scandinavia. Consequently, it appears that the Norwegian lemming evolved from a small population that survived the LGM in an ice-free Scandinavian refugium.