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Animal movement on short and long time scales and the effect on genetic diversity in cold-adapted species
Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Department of Bioinformatics and Genetics.
2016 (English)Doctoral 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.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2016. , 45 p.
National Category
Zoology
Research subject
Systematic Zoology
Identifiers
URN: urn:nbn:se:su:diva-129132ISBN: 978-91-7649-421-9 (print)OAI: oai:DiVA.org:su-129132DiVA: diva2:920686
Public defence
2016-06-10, Vivi Täckholmsalen, NPQ-huset, Svante Arrhenius väg 20, Stockholm, 13:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 1: Manuscript. Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2016-05-18 Created: 2016-04-15 Last updated: 2017-05-18Bibliographically approved
List of papers
1. Run to the hills: gene flow among mountain areas leads to low genetic differentiation in the Norwegian lemming
Open this publication in new window or tab >>Run to the hills: gene flow among mountain areas leads to low genetic differentiation in the Norwegian lemming
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2017 (English)In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 121, no 1, 1-14 p.Article in journal (Refereed) Published
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.

Keyword
Microsatellites, DNA, Lemmus, migration, dispersal
National Category
Zoology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-140622 (URN)10.1093/biolinnean/blw020 (DOI)000400957700001 ()
Available from: 2017-03-13 Created: 2017-03-13 Last updated: 2017-06-26Bibliographically approved
2. On the origin of the Norwegian lemming
Open this publication in new window or tab >>On the origin of the Norwegian lemming
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2014 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 23, no 8, 2060-2071 p.Article in journal (Refereed) Published
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.

Keyword
speciation, extinction, ancient DNA, colonization, Pleistocene, Lemmus
National Category
Biochemistry and Molecular Biology Developmental Biology Zoology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-103287 (URN)10.1111/mec.12698 (DOI)000333858200014 ()
Note

AuthorCount:10;

Available from: 2014-05-19 Created: 2014-05-12 Last updated: 2017-12-05Bibliographically approved
3. Range shifts or extinction? Ancient DNA and distribution modelling reveal past and future responses to climate warming in cold-adapted birds
Open this publication in new window or tab >>Range shifts or extinction? Ancient DNA and distribution modelling reveal past and future responses to climate warming in cold-adapted birds
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2017 (English)In: Global Change Biology, ISSN 1354-1013, E-ISSN 1365-2486, Vol. 23, no 4, 1425-1435 p.Article in journal (Refereed) Published
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.

Keyword
approximate Bayesian computation, climate change, colonization, extinction, Lagopus, palaeogenetics, phylogeography, Pleistocene, species distribution modelling
National Category
Biological Sciences Earth and Related Environmental Sciences
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-141195 (URN)10.1111/gcb.13522 (DOI)000396836800006 ()27762483 (PubMedID)
Available from: 2017-04-28 Created: 2017-04-28 Last updated: 2017-05-18Bibliographically approved
4. Non-receding hare lines: genetic continuity since the Late Pleistocene in European mountain hares (Lepus timidus)
Open this publication in new window or tab >>Non-receding hare lines: genetic continuity since the Late Pleistocene in European mountain hares (Lepus timidus)
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(English)Manuscript (preprint) (Other academic)
National Category
Zoology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-129136 (URN)
Available from: 2016-04-15 Created: 2016-04-15 Last updated: 2016-05-09Bibliographically approved

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