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Large carnivore population turnover and ecological change during the Late Quaternary
Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History (NRM).
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The cave lion (Panthera spelaea), the grey wolf (Canis lupus) and the brown bear (Ursus arctos) all shared an intercontinental distribution across the northern hemisphere during most of the Late Quaternary, and experienced repeated events of climate change. The cave lion went extinct at the end of the Pleistocene and although the wolf and the bear have survived until present day, recent human persecution has caused demographic bottlenecks and local extinctions. In this thesis, mitochondrial and nuclear DNA was analyzed from ancient and modern samples in order to study spatiotemporal changes in genetic diversity in the three species. Mitochondrial sequences analyzed from 48 radiocarbon dated cave lion remains revealed two haplogroups, of which the more genetically diverse seemingly disappeared around 41,000 years BP. Serial coalescent simulations on the data supported a population bottleneck in Beringia between roughly 47-18,000 years BP. Its long duration prevents a specific causal factor to be singled out, but the early onset and overlapping declines of other large mammals in the region suggests that major environmental changes greatly impacted the fauna of Beringia during this time. Using a similar genetic marker, a set of 126 modern wolves and two Siberian wolf remains of Late Pleistocene age were analyzed. The sequences yielded from the latter samples pertained to a basal haplogroup, which contained all Late Pleistocene wolves from previous studies. As data from both modern and ancient wolves were combined, a pattern of decreasing genetic diversity was identified around the Pleistocene-Holocene transition. This decrease was further tested by serial coalescent simulations, which supported a bottleneck in northern North America around this time. Further analyses were applied to one of the ancient wolf remains from Siberia, producing a draft genome sequence and a complete mitochondrial genome. Given the radiocarbon date of the Siberian wolf, a slower mutation rate could be inferred, which pushed back the split between the lineages leading to modern wolves and dogs to at least 27,000 years BP. The Siberian wolf was positioned close to the split but basal to these lineages. A global comparison with modern dogs indicated a closer genetic affiliation between the Siberian wolf and some arctic breeds. For the brown bear, phylogeographic changes in Europe were studied over the last 50,000 years, using radiocarbon dating and mitochondrial sequences. When concatenated and compared with published data, the mtDNA revealed a turnover event just before the LGM, while the dating confirmed a presence of brown bears at relatively high latitudes during this period. Marked shifts in population size were also inferred. Furthermore, data of stable isotope levels confirmed a dietary shift to increasing herbivory around the LGM. Finally, a recent anthropogenic bottleneck among Scandinavian brown bears was studied. While no change in genetic structure could be detected, mitochondrial and microsatellite markers showed a decline in genetic diversity, especially pronounced in the southern subpopulation. ABC simulations supported a bottleneck taking place across all of Scandinavia. Taken together, this thesis have identified and elucidated several impacts on genetic diversity in the past populations of large carnivores. The use of different genetic markers has enabled comparisons with published data, but also revealed their comparatively different benefits and limitations. Overall, the presented studies compose a synthesis of past population dynamics in large carnivores, uniquely revealed by ancient DNA.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2016.
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
URN: urn:nbn:se:su:diva-127845ISBN: 978-91-7649-380-9 (print)OAI: oai:DiVA.org:su-127845DiVA: diva2:911571
Public defence
2016-04-29, De Geersalen, Geovetenskapens hus, Svante Arrhenius väg 14, 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 2: Manuscript. Paper 4: Manuscript.

Available from: 2016-04-06 Created: 2016-03-13 Last updated: 2017-02-17Bibliographically approved
List of papers
1. Population demography and genetic diversity in the Pleistocene cave lion
Open this publication in new window or tab >>Population demography and genetic diversity in the Pleistocene cave lion
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2015 (English)In: Open Quaternary, ISSN 2055-298X, Vol. 1, no 1, 4Article in journal (Refereed) Published
Abstract [en]

With a range that covered most of northern Eurasia and parts of North America, the cave lion (Panthera spelaea) was one of the most widespread carnivores of the Late Pleistocene. Earlier ancient DNA analyses have shown that it is distinct from modern lions, and have suggested a demographic decline in Beringia during marine isotope stage 3 (MIS 3). Here, we further investigate the Late Pleistocene population dynamics in more detail by combining a powerful algorithm that couples MCMC with coalescent simulations under an approximate Bayesian computation framework. We use an ancient DNA dataset of previously published (n = 34) and new radiocarbon dated specimens (n = 14). Phylogenetic and network analyses based on the mitochondrial control region and the ATP8 gene identified two major haplogroups, one of which appears to vanish around 41,000 cal a BP. The approximate Bayesian computation analysis suggested a decline in effective population size (Ne) in Beringia of at least a 2-fold magnitude that began approximately 47,000 cal a BP, followed by an increase in Ne, most likely around 18,000 cal a BP. The cave lion went through a demographic bottleneck during MIS 3, which may have lasted for several tens of thousands of years, and only recovered shortly before the species' extinction. Several other large mammal species display similar declines in genetic diversity in Beringia during MIS 3, suggesting that major environmental changes might have affected megafaunal populations during this time period.

Keyword
Panthera spelaea, Beringia, bottleneck, Quaternary, haplogroup, Megafauna
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-127825 (URN)10.5334/oq.aa (DOI)
Available from: 2016-03-11 Created: 2016-03-11 Last updated: 2016-03-14Bibliographically approved
2. From the past to the present: Wolf phylogeography and demographic history based on the mitochondrial control region
Open this publication in new window or tab >>From the past to the present: Wolf phylogeography and demographic history based on the mitochondrial control region
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(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-127829 (URN)
Available from: 2016-03-11 Created: 2016-03-11 Last updated: 2016-03-14Bibliographically approved
3. Ancient Wolf Genome Reveals an Early Divergence of Domestic Dog Ancestors and Admixture into High-Latitude Breeds
Open this publication in new window or tab >>Ancient Wolf Genome Reveals an Early Divergence of Domestic Dog Ancestors and Admixture into High-Latitude Breeds
2015 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 25, no 11, 1515-1519 p.Article in journal (Refereed) Published
Abstract [en]

The origin of domestic dogs is poorly understood [1-15], with suggested evidence of dog-like features in fossils that predate the Last Glacial Maximum [6, 9, 10, 14, 16] conflicting with genetic estimates of a more recent divergence between dogs and worldwide wolf populations [13, 15, 17-19]. Here, we present a draft genome sequence from a 35,000 year-old wolf from the Taimyr Peninsula in northern Siberia. We find that this individual belonged to a population that diverged from the common ancestor of present-day wolves and dogs very close in time to the appearance of the domestic dog lineage. We use the directly dated ancient wolf genome to recalibrate the molecular timescale of wolves and dogs and find that the mutation rate is substantially slower than assumed by most previous studies, suggesting that the ancestors of dogs were separated from present-day wolves before the Last Glacial Maximum. We also find evidence of introgression from the archaic Taimyr wolf lineage into present-day dog breeds from northeast Siberia and Greenland, contributing between 1.4% and 27.3% of their ancestry. This demonstrates that the ancestry of present-day dogs is derived from multiple regional wolf populations.

National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-119054 (URN)10.1016/j.cub.2015.04.019 (DOI)000355556600028 ()
Available from: 2015-08-17 Created: 2015-07-27 Last updated: 2017-12-04Bibliographically approved
4. Genetic revolutions and northern survival during the last glacial maximum in European brown bears
Open this publication in new window or tab >>Genetic revolutions and northern survival during the last glacial maximum in European brown bears
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(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-127831 (URN)
Available from: 2016-03-11 Created: 2016-03-11 Last updated: 2016-03-14Bibliographically approved
5. Consequences of a demographic bottleneck on geneticstructure and variation in the Scandinavian brown bear
Open this publication in new window or tab >>Consequences of a demographic bottleneck on geneticstructure and variation in the Scandinavian brown bear
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2015 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 24, no 13, 3441-3454 p.Article in journal (Refereed) Published
Abstract [en]

The Scandinavian brown bear went through a major decline in population size approximately 100years ago, due to intense hunting. After being protected, the population subsequently recovered and today numbers in the thousands. The genetic diversity in the contemporary population has been investigated in considerable detail, and it has been shown that the population consists of several subpopulations that display relatively high levels of genetic variation. However, previous studies have been unable to resolve the degree to which the demographic bottleneck impacted the contemporary genetic structure and diversity. In this study, we used mitochondrial and microsatellite DNA markers from pre- and postbottleneck Scandinavian brown bear samples to investigate the effect of the bottleneck. Simulation and multivariate analysis suggested the same genetic structure for the historical and modern samples, which are clustered into three subpopulations in southern, central and northern Scandinavia. However, the southern subpopulation appears to have gone through a marked change in allele frequencies. When comparing the mitochondrial DNA diversity in the whole population, we found a major decline in haplotype numbers across the bottleneck. However, the loss of autosomal genetic diversity was less pronounced, although a significant decline in allelic richness was observed in the southern subpopulation. Approximate Bayesian computations provided clear support for a decline in effective population size during the bottleneck, in both the southern and northern subpopulations. These results have implications for the future management of the Scandinavian brown bear because they indicate a recent loss in genetic diversity and also that the current genetic structure may have been caused by historical ecological processes rather than recent anthropogenic persecution.

Keyword
bottleneck, decline, microsatellites, mtDNA, Ursus arctos
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-119131 (URN)10.1111/mec.13239 (DOI)000356973100018 ()
Available from: 2015-07-31 Created: 2015-07-29 Last updated: 2017-12-04Bibliographically approved

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