Ancient DNA of narrow-headed vole reveal common features of the Late Pleistocene population dynamics in cold-adapted small mammals.

The narrow-headed vole, collared lemming and common vole were the most abundant small mammal species across the Eurasian Late Pleistocene steppe-tundra environment. Previous ancient DNA studies of the collared lemming and common vole have revealed dynamic population histories shaped by climatic fluctuations. To investigate the extent to which species with similar adaptations share common evolutionary histories, we generated a dataset comprised the mitochondrial genomes of 139 ancient and 6 modern narrow-headed voles from several sites across Europe and northwestern Asia covering approximately the last 100 thousand years (kyr). We inferred Bayesian time-aware phylogenies using 11 radiocarbon-dated samples to calibrate the molecular clock. Divergence of the main mtDNA lineages across the three species occurred during marine isotope stages (MIS) 7 and MIS 5, suggesting a common response of species adapted to open habitat during interglacials. We identified several time-structured mtDNA lineages in European narrow-headed vole, suggesting lineage turnover. The timing of some of these turnovers was synchronous across the three species, allowing us to identify the main drivers of the Late Pleistocene dynamics of steppe- and cold-adapted species.

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.

Ancient mitochondrial DNA connects house mice in the British Isles to trade across Europe over three millennia.

BACKGROUND: The earliest records in Britain for the western European house mouse (Mus musculus domesticus) date from the Late Bronze Age. The arrival of this commensal species in Britain is thought to be related to human transport and trade with continental Europe. In order to study this arrival, we collected a total of 16 ancient mouse mandibulae from four early British archaeological sites, ranging from the Late Bronze Age to the Roman period. RESULTS: From these, we obtained ancient mitochondrial DNA (mtDNA) house mouse sequences from eight house mice from two of the sites dating from the Late Bronze to Middle Iron Age. We also obtained five ancient mtDNA wood mouse (Apodemus spp.) sequences from all four sites. The ancient house mouse sequences found in this study were from haplogroups E (N = 6) and D (N = 2). Modern British house mouse mtDNA sequences are primarily characterised by haplogroups E and F and, much less commonly, haplogroup D. CONCLUSIONS: The presence of haplogroups D and E in our samples and the dating of the archaeological sites provide evidence of an early house mouse colonisation that may relate to Late Bronze Age/Iron Age trade and/or human expansion. Our results confirm the hypothesis, based on zooarchaeological evidence and modern mtDNA predictions, that house mice, with haplogroups D and E, were established in Britain by the Iron Age and, in the case of haplogroup E, possibly as early as the Late Bronze Age.

Demographic reconstruction from ancient DNA supports rapid extinction of the great auk.

The great auk was once abundant and distributed across the North Atlantic. It is now extinct, having been heavily exploited for its eggs, meat, and feathers. We investigated the impact of human hunting on its demise by integrating genetic data, GPS-based ocean current data, and analyses of population viability. We sequenced complete mitochondrial genomes of 41 individuals from across the species' geographic range and reconstructed population structure and population dynamics throughout the Holocene. Taken together, our data do not provide any evidence that great auks were at risk of extinction prior to the onset of intensive human hunting in the early 16th century. In addition, our population viability analyses reveal that even if the great auk had not been under threat by environmental change, human hunting alone could have been sufficient to cause its extinction. Our results emphasise the vulnerability of even abundant and widespread species to intense and localised exploitation.

Genetic turnovers and northern survival during the last glacial maximum in European brown bears.

The current phylogeographic pattern of European brown bears (Ursus arctos) has commonly been explained by postglacial recolonization out of geographically distinct refugia in southern Europe, a pattern well in accordance with the expansion/contraction model. Studies of ancient DNA from brown bear remains have questioned this pattern, but have failed to explain the glacial distribution of mitochondrial brown bear clades and their subsequent expansion across the European continent. We here present 136 new mitochondrial sequences generated from 346 remains from Europe, ranging in age between the Late Pleistocene and historical times. The genetic data show a high Late Pleistocene diversity across the continent and challenge the strict confinement of bears to traditional southern refugia during the last glacial maximum (LGM). The mitochondrial data further suggest a genetic turnover just before this time, as well as a steep demographic decline starting in the mid-Holocene. Levels of stable nitrogen isotopes from the remains confirm a previously proposed shift toward increasing herbivory around the LGM in Europe. Overall, these results suggest that in addition to climate, anthropogenic impact and inter-specific competition may have had more important effects on the brown bear's ecology, demography, and genetic structure than previously thought.

Investigating the Effect of the Environment on Prey Detection Ability in Humans.

Visual search experiments used in the field of psychology may be applied to investigate the relationship between environments and prey detection rates that could influence hunting behaviours in ancient humans. Two lab-based experiments were designed to examine the effects of differing virtual environments, representing Marine Isotope Stage 3 (MIS3) in Europe, on participants' ability to locate prey. The results show that prey detection performance is highly influenced by vegetation structure, both in terms of the biome type (wooded vs. grassland environments) and the density of the vegetation (trees in wooded and shrubs in grassland environments). However, the density of vegetation has a greater relative effect in grassland than in wooded biomes. Closer examination of the transition between biomes (relative percentages of trees vs. shrubs) at the same vegetative density shows a non-linear relationship between prey detection performance and the relative tree to shrub percentages. Changes in the distribution of biomes occurred throughout the Quaternary. The composition of those biomes will have likely affected hominin hunting behaviours because of their intermediary effects on prey detection performance. This may, therefore, have played a role in the turn-overs of hunter-gatherer hominin populations during MIS3 and at other times in the Quaternary.

An ?Aukward' Tale: A Genetic Approach to Discover the Whereabouts of the Last Great Auks.

One hundred and seventy-three years ago, the last two Great Auks, Pinguinusimpennis, ever reliably seen were killed. Their internal organs can be found in the collections of the Natural History Museum of Denmark, but the location of their skins has remained a mystery. In 1999, Great Auk expert Errol Fuller proposed a list of five potential candidate skins in museums around the world. Here we take a palaeogenomic approach to test which-if any-of Fuller's candidate skins likely belong to either of the two birds. Using mitochondrial genomes from the five candidate birds (housed in museums in Bremen, Brussels, Kiel, Los Angeles, and Oldenburg) and the organs of the last two known individuals, we partially solve the mystery that has been on Great Auk scholars' minds for generations and make new suggestions as to the whereabouts of the still-missing skin from these two birds.

Identifying Bird Remains Using Ancient DNA Barcoding.

Bird remains that are difficult to identify taxonomically using morphological methods, are common in the palaeontological record. Other types of challenging avian material include artefacts and food items from endangered taxa, as well as remains from aircraft strikes. We here present a DNA-based method that enables taxonomic identification of bird remains, even from material where the DNA is heavily degraded. The method is based on the amplification and sequencing of two short variable parts of the 16S region in the mitochondrial genome. To demonstrate the applicability of this approach, we evaluated the method on a set of Holocene and Late Pleistocene postcranial bird bones from several palaeontological and archaeological sites in Europe with good success.

Neandertal and Denisovan DNA from Pleistocene sediments.

Although a rich record of Pleistocene human-associated archaeological assemblages exists, the scarcity of hominin fossils often impedes the understanding of which hominins occupied a site. Using targeted enrichment of mitochondrial DNA, we show that cave sediments represent a rich source of ancient mammalian DNA that often includes traces of hominin DNA, even at sites and in layers where no hominin remains have been discovered. By automation-assisted screening of numerous sediment samples, we detected Neandertal DNA in eight archaeological layers from four caves in Eurasia. In Denisova Cave, we retrieved Denisovan DNA in a Middle Pleistocene layer near the bottom of the stratigraphy. Our work opens the possibility of detecting the presence of hominin groups at sites and in areas where no skeletal remains are found.

Range shifts or extinction? Ancient DNA and distribution modelling reveal past and future responses to climate warming in cold-adapted birds.

Global warming is predicted to cause substantial habitat rearrangements, with the most severe effects expected to occur in high-latitude biomes. However, one major uncertainty is whether species will be able to shift their ranges to keep pace with climate-driven environmental changes. Many recent studies on mammals have shown that past range contractions have been associated with local extinctions rather than survival by habitat tracking. Here, we have used an interdisciplinary approach that combines ancient DNA techniques, coalescent simulations and species distribution modelling, to investigate how two common cold-adapted bird species, willow and rock ptarmigan (Lagopus lagopus and Lagopus muta), respond to long-term climate warming. Contrary to previous findings in mammals, we demonstrate a genetic continuity in Europe over the last 20 millennia. Results from back-casted species distribution models suggest that this continuity may have been facilitated by uninterrupted habitat availability and potentially also the greater dispersal ability of birds. However, our predictions show that in the near future, some isolated regions will have little suitable habitat left, implying a future decrease in local populations at a scale unprecedented since the last glacial maximum.

Palaeoproteomic evidence identifies archaic hominins associated with the Châtelperronian at the Grotte du Renne.

In Western Europe, the Middle to Upper Paleolithic transition is associated with the disappearance of Neandertals and the spread of anatomically modern humans (AMHs). Current chronological, behavioral, and biological models of this transitional period hinge on the Châtelperronian technocomplex. At the site of the Grotte du Renne, Arcy-sur-Cure, morphological Neandertal specimens are not directly dated but are contextually associated with the Châtelperronian, which contains bone points and beads. The association between Neandertals and this "transitional" assemblage has been controversial because of the lack either of a direct hominin radiocarbon date or of molecular confirmation of the Neandertal affiliation. Here we provide further evidence for a Neandertal-Châtelperronian association at the Grotte du Renne through biomolecular and chronological analysis. We identified 28 additional hominin specimens through zooarchaeology by mass spectrometry (ZooMS) screening of morphologically uninformative bone specimens from Châtelperronian layers at the Grotte du Renne. Next, we obtain an ancient hominin bone proteome through liquid chromatography-MS/MS analysis and error-tolerant amino acid sequence analysis. Analysis of this palaeoproteome allows us to provide phylogenetic and physiological information on these ancient hominin specimens. We distinguish Late Pleistocene clades within the genus Homo based on ancient protein evidence through the identification of an archaic-derived amino acid sequence for the collagen type X, alpha-1 (COL10α1) protein. We support this by obtaining ancient mtDNA sequences, which indicate a Neandertal ancestry for these specimens. Direct accelerator mass spectometry radiocarbon dating and Bayesian modeling confirm that the hominin specimens date to the Châtelperronian at the Grotte du Renne.

The colonization history of British water vole (Arvicola amphibius (Linnaeus, 1758)): origins and development of the Celtic fringe.

The terminal Pleistocene and Early Holocene, a period from 15 000 to 18 000 Before Present (BP), was critical in establishing the current Holarctic fauna, with temperate-climate species largely replacing cold-adapted ones at mid-latitudes. However, the timing and nature of this process remain unclear for many taxa, a point that impacts on current and future management strategies. Here, we use an ancient DNA dataset to test more directly postglacial histories of the water vole (Arvicola amphibius, formerly A terrestris), a species that is both a conservation priority and a pest in different parts of its range. We specifically examine colonization of Britain, where a complex genetic structure can be observed today. Although we focus on population history at the limits of the species' range, the inclusion of additional European samples allows insights into European postglacial colonization events and provides a molecular perspective on water vole taxonomy.

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.

Exploring the universal ecological responses to climate change in a univoltine butterfly.

Animals with distinct life stages are often exposed to different temperatures during each stage. Thus, how temperature affects these life stages should be considered for broadly understanding the ecological consequences of climate warming on such species. For example, temperature variation during particular life stages may affect respective change in body size, phenology and geographic range, which have been identified as the "universal" ecological responses to climate change. While each of these responses has been separately documented across a number of species, it is not known whether each response occurs together within a species. The influence of temperature during particular life stages may help explain each of these ecological responses to climate change. Our goal was to determine if monthly temperature variation during particular life stages of a butterfly species can predict respective changes in body size and phenology. We also refer to the literature to assess if temperature variability during the adult stage influences range change over time. Using historical museum collections paired with monthly temperature records, we show that changes in body size and phenology of the univoltine butterfly, Hesperia comma, are partly dependent upon temporal variation in summer temperatures during key stages of their life cycle. June temperatures, which are likely to affect growth rate of the final larval instar, are important for predicting adult body size (for males only; showing a positive relationship with temperature). July temperatures, which are likely to influence the pupal stage, are important for predicting the timing of adult emergence (showing a negative relationship with temperature). Previous studies show that August temperatures, which act on the adult stage, are linked to range change. Our study highlights the importance of considering temperature variation during each life stage over historic time-scales for understanding intraspecific response to climate change. Range edge studies of ectothermic species that have annual life cycles, long time-series occurrence data, and associated temperature records (ideally at monthly resolutions) could be useful model systems for intraspecific tests of the universal ecological responses to climate change and for exploring interactive effects.

The long term response of birds to climate change: new results from a cold stage avifauna in northern England.

The early MIS 3 (55-40 Kyr BP associated with Middle Palaeolithic archaeology) bird remains from Pin Hole, Creswell Crags, Derbyshire, England are analysed in the context of the new dating of the site's stratigraphy. The analysis is restricted to the material from the early MIS 3 level of the cave because the upper fauna is now known to include Holocene material as well as that from the Late Glacial. The results of the analysis confirm the presence of the taxa, possibly unexpected for a Late Pleistocene glacial deposit including records such as Alpine swift, demoiselle crane and long-legged buzzard with southern and/or eastern distributions today. These taxa are accompanied by more expected ones such as willow ptarmigan /red grouse and rock ptarmigan living today in northern and montane areas. Finally, there are temperate taxa normally requiring trees for nesting such as wood pigeon and grey heron. Therefore, the result of the analysis is that the avifauna of early MIS 3 in England included taxa whose ranges today do not overlap making it a non-analogue community similar to the many steppe-tundra mammalian faunas of the time. The inclusion of more temperate and woodland taxa is discussed in the light that parts of northern Europe may have acted as cryptic northern refugia for some such taxa during the last glacial. These records showing former ranges of taxa are considered in the light of modern phylogeographic studies as these often assume former ranges without considering the fossil record of those taxa. In addition to the anomalous combination of taxa during MIS 3 living in Derbyshire, the individuals of a number of the taxa are different in size and shape to members of the species today probably due to the high carrying capacity of the steppe-tundra.

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.

Late-glacial recolonization and phylogeography of European red deer (Cervus elaphus L.).

The Pleistocene was an epoch of extreme climatic and environmental changes. How individual species responded to the repeated cycles of warm and cold stages is a major topic of debate. For the European fauna and flora, an expansion-contraction model has been suggested, whereby temperate species were restricted to southern refugia during glacial times and expanded northwards during interglacials, including the present interglacial (Holocene). Here, we test this model on the red deer (Cervus elaphus) a large and highly mobile herbivore, using both modern and ancient mitochondrial DNA from the entire European range of the species over the last c. 40,000 years. Our results indicate that this species was sensitive to the effects of climate change. Prior to the Last Glacial Maximum (LGM) haplogroups restricted today to South-East Europe and Western Asia reached as far west as the UK. During the LGM, red deer was mainly restricted to southern refugia, in Iberia, the Balkans and possibly in Italy and South-Western Asia. At the end of the LGM, red deer expanded from the Iberian refugium, to Central and Northern Europe, including the UK, Belgium, Scandinavia, Germany, Poland and Belarus. Ancient DNA data cannot rule out refugial survival of red deer in North-West Europe through the LGM. Had such deer survived, though, they were replaced by deer migrating from Iberia at the end of the glacial. The Balkans served as a separate LGM refugium and were probably connected to Western Asia with genetic exchange between the two areas.

Rabbits and hominin survival in Iberia.

High dependence on the hunting and consumption of large mammals by some hominins may have limited their survival once their preferred quarry became scarce or disappeared. Adaptation to smaller residual prey would have been essential after the many large-bodied species decreased in numbers. We focus on the use of a superabundant species, the rabbit, to demonstrate the importance of this taxon in Iberia as fundamental to predators. We show that the use of the rabbit over time has increased, and that there could have been differential consumption by Neanderthals and Anatomically Modern Humans (AMH). Analysis of bone remains from excavations throughout Iberia show that this lagomorph was a crucial part of the diet of AMH but was relatively unutilised during the Mousterian, when Neanderthals were present. We first present changes in mammalian biomass and mean body mass of mammals over 50,000 years, to illustrate the dramatic loss of large mammalian fauna and to show how the rabbit may have contributed a consistently high proportion of the available game biomass throughout that period. Unlike the Italian Peninsula and other parts of Europe, in Iberia the rabbit has provided a food resource of great importance for predators including hominins. We suggest that hunters that could shift focus to rabbits and other smaller residual fauna, once larger-bodied species decreased in numbers, would have been able to persist. From the evidence presented here, we postulate that Neanderthals may have been less capable of prey-shifting and hence use the high-biomass prey resource provided by the rabbit, to the extent AMH did.

Serial population extinctions in a small mammal indicate Late Pleistocene ecosystem instability.

The Late Pleistocene global extinction of many terrestrial mammal species has been a subject of intensive scientific study for over a century, yet the relative contributions of environmental changes and the global expansion of humans remain unresolved. A defining component of these extinctions is a bias toward large species, with the majority of small-mammal taxa apparently surviving into the present. Here, we investigate the population-level history of a key tundra-specialist small mammal, the collared lemming (Dicrostonyx torquatus), to explore whether events during the Late Pleistocene had a discernible effect beyond the large mammal fauna. Using ancient DNA techniques to sample across three sites in North-West Europe, we observe a dramatic reduction in genetic diversity in this species over the last 50,000 y. We further identify a series of extinction-recolonization events, indicating a previously unrecognized instability in Late Pleistocene small-mammal populations, which we link with climatic fluctuations. Our results reveal climate-associated, repeated regional extinctions in a keystone prey species across the Late Pleistocene, a pattern likely to have had an impact on the wider steppe-tundra community, and one that is concordant with environmental change as a major force in structuring Late Pleistocene biodiversity.

Refugia revisited: individualistic responses of species in space and time.

Climate change in the past has led to significant changes in species' distributions. However, how individual species respond to climate change depends largely on their adaptations and environmental tolerances. In the Quaternary, temperate-adapted taxa are in general confined to refugia during glacials while cold-adapted taxa are in refugia during interglacials. In the Northern Hemisphere, evidence appears to be mounting that in addition to traditional southern refugia for temperate species, cryptic refugia existed in the North during glacials. Equivalent cryptic southern refugia, to the south of the more conventional high-latitude polar refugia, exist in montane areas during periods of warm climate, such as the current interglacial. There is also a continental/oceanic longitudinal gradient, which should be included in a more complete consideration of the interaction between species ranges and climates. Overall, it seems clear that there is large variation in both the size of refugia and the duration during which species are confined to them. This has implications for the role of refugia in the evolution of species and their genetic diversity.