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  • 1. Dalén, Love
    et al.
    Kempe Lagerholm, Vendela
    Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Sweden; University of St Andrews, UK.
    Nylander, Johan A. A.
    Barton, Nick
    Bochenski, Zbigniew M.
    Tomek, Teresa
    Rudling, David
    Ericson, Per G. P.
    Irestedt, Martin
    Stewart, John R.
    Identifying Bird Remains Using Ancient DNA Barcoding2017In: Genes, ISSN 2073-4425, E-ISSN 2073-4425, Vol. 8, no 6, article id 169Article in journal (Refereed)
    Abstract [en]

    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.

  • 2.
    Kempe Lagerholm, Vendela
    Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Department of Bioinformatics and Genetics.
    Animal movement on short and long time scales and the effect on genetic diversity in cold-adapted species2016Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    The genetic diversity in modern species is strongly affected by contemporary gene flow between populations, which in turn is governed by individual dispersal capacities and barriers in the landscape. However, current patterns of variation have also been shaped by movement over longer time-scales, such as the successive shifts in species distributions that have occurred during past climate changes. This thesis is focused on cold-adapted species, and one parameter that has greatly influenced their current genetic diversity is how they coped with climate warming at the last glacial/interglacial transition, ca 11.7 thousand years ago. I examined this in three different small herbivore taxa; true lemmings (Lemmus), ptarmigan (Lagopus) and hares (Lepus), whose modern distributions stretch from the exposed tundra to the subarctic moorlands and taiga. In the first paper, I investigated contemporary genetic structure in the cyclic Norwegian lemming (Lemmus lemmus) and proposed that mass movements during peak years act as pulses of gene flow between mountain areas, which homogenise the gene pool over surprisingly vast geographic distances. However, when I used ancient DNA to analyse the lemmings’ ability for long-term directional movement, I found that the Ice Age populations that inhabited the former midlatitude European tundra-steppe appear to have been incapable of shifting their distribution northwards following post-glacial climate warming. Instead, the results suggest that the endemic Norwegian lemming descends from an isolated population that survived the last glacial maximum in situ in a restricted ice free refugium. In contrast to the glacial lemmings, as well the majority of previously studied mammals, the ptarmigan (L. lagopus and L. muta) and hare (L. timidus) analyses revealed a long-term genetic continuity in Europe, where the midlatitude populations were able to keep pace with the rapidly changing climate at the last glacial/interglacial transition, enabling them to shift their ranges to northern and high-alpine regions. These different outcomes might be explained by ptarmigans’ flight capability that allows a less restricted dispersal across fragmented landscapes, and that the generalist nature of mountain hares makes them less vulnerable to habitat alterations. Species distribution modelling, however, indicated that continued climate warming will make some isolated regions unsuitable in the future, thereby forcing populations to adapt the new environmental conditions in order to avoid local extinctions.

  • 3.
    Lagerholm, Vendela K.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Sweden; University of St Andrews, UK.
    Norén, Karin
    Stockholm University, Faculty of Science, Department of Zoology. University of California Davis, USA.
    Ehrich, Dorothee
    Ims, Rolf A.
    Killengreen, Siw T.
    Abramson, Natalia I.
    Niemaa, Jukka
    Angerbjörn, Anders
    Stockholm University, Faculty of Science, Department of Zoology.
    Henttonen, Heikki
    Dalén, Love
    Run to the hills: gene flow among mountain areas leads to low genetic differentiation in the Norwegian lemming2017In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 121, no 1, p. 1-14Article in journal (Refereed)
    Abstract [en]

    The endemic Norwegian lemming (Lemmus lemmus) is an icon for cyclic species, famous since the Middle Ages for its enormous population outbreaks and mass movements. Although the drivers behind this cyclicity have been intensively investigated, virtually nothing is known about the extent to which long-distance dispersal during population peaks actually lead to gene flow among mountain tundra areas. In this article, we use nine microsatellite markers to address this question and analyse range-wide genetic diversity and differentiation between Fennoscandian sub-regions. The results revealed a high genetic variation with a surprisingly weak population structure, comparable to that of much larger mammals. The differentiation was mainly characterized as a genetic cline across the species' entire distribution, and results from spatial autocorrelation analyses suggested that gene flow occurs with sufficiently high frequency to create a genetic patch size of 100 km. Further, we found that for the equivalent distances, the southern sub-regions were genetically more similar to each other than those in the north, which indicates that the prolonged periods of interrupted lemming cyclicity recorded in the northern parts of Fennoscandia have led to increased isolation and population differentiation. In summary, we propose that mass movements during peak years act as pulses of gene flow between mountain tundra areas, and that these help to maintain genetic variation and counteract differentiation over vast geographic distances.

  • 4.
    Lagerholm, Vendela K.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Sweden.
    Sandoval-Castellanos, Edson
    Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Sweden.
    Ehrich, Dorothee
    Abramson, Natalia I.
    Nadachowski, Adam
    Kalthoff, Daniela C.
    Germonpre, Mietje
    Angerbjörn, Anders
    Stockholm University, Faculty of Science, Department of Zoology.
    Stewart, John R.
    Dalén, Love
    On the origin of the Norwegian lemming2014In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 23, no 8, p. 2060-2071Article in journal (Refereed)
    Abstract [en]

    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.

  • 5.
    Lagerholm, Vendela K.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Sweden.
    Sandoval-Castellanos, Edson
    Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Sweden; Universidad Nacional Autónoma de México, México.
    Vaniscotte, Amelie
    Potapova, Olga R.
    Tomek, Teresa
    Bochenski, Zbigniew M.
    Shepherd, Paul
    Barton, Nick
    Van Dyck, Marie-Claire
    Miller, Rebecca
    Höglund, Jacob
    Yoccoz, Nigel G.
    Dalén, Love
    Stewart, John R.
    Range shifts or extinction? Ancient DNA and distribution modelling reveal past and future responses to climate warming in cold-adapted birds2017In: Global Change Biology, ISSN 1354-1013, E-ISSN 1365-2486, Vol. 23, no 4, p. 1425-1435Article in journal (Refereed)
    Abstract [en]

    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.

  • 6. Smith, Steve
    et al.
    Sandoval-Castellanos, Edson
    Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Sweden; Universidad Nacional Autónoma de México, México.
    Lagerholm, Vendela K.
    Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Sweden.
    Napierala, Hannes
    Sablin, Mikhail
    Von Seth, Johanna
    Fladerer, Florian A.
    Germonpre, Mietje
    Wojtal, Piotr
    Miller, Rebecca
    Stewart, John R.
    Dalén, Love
    Nonreceding hare lines: genetic continuity since the Late Pleistocene in European mountain hares (Lepus timidus)2017In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 120, no 4, p. 891-908Article in journal (Refereed)
    Abstract [en]

    Throughout time, climate changes have caused substantial rearrangements of habitats which have alternately promoted and disfavoured different types of taxa. At first glance, the mountain hare (Lepus timidus) shows the typical hallmarks of a cold-adapted species that has retreated to refugia since the onset of the current Holocene interglacial. In contrary to expectations, however, the species has a high contemporary genetic diversity with no clear differentiation between geographically isolated populations. In order to clarify the phylogeographic history of European mountain hares, we here analysed ancient DNA from the glacial populations that inhabited the previous midlatitude European tundra region. Our results reveal that the Ice Age hares had similar levels of genetic variation and lack of geographic structure as observed today, and the ancient samples were intermingled with modern individuals throughout the reconstructed evolutionary tree. This suggests a temporal genetic continuity in Europe, where the mountain hares were able to keep pace with the rapid changes at the last glacial/ interglacial transition and successfully track their shifting habitat to northern and alpine regions. Further, the temporal demographic analyses showed that the species' population size in Europe appears to have been tightly linked with palaeoclimatic fluctuations, with increases and declines occurring during periods of global cooling and warming, respectively. Taken together, our results suggest that neither habitat shifts nor demographic fluctuations have had any substantial impact on the genetic diversity of European mountain hares. This remarkable resilience, which contrasts to a majority of previously investigated cold-adapted species, is likely due to its generalist nature that makes it less vulnerable to environmental changes.

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