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Genetic Structure and Gene Flow in a Continuously Distributed Large Terrestrial Carnivore - the Brown Bear (Ursus Arctos) in Northern Europe

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Genetic Structure and Gene Flow in a Continuously Distributed Large Terrestrial Carnivore - the Brown Bear (Ursus Arctos) in Northern Europe Norwegian University of Life Sciences Faculty of Environmental Science and Technology Department of Ecology and Natural Resource Management Philosophiae Doctor (PhD) Thesis 2015:72 Genetic structure and gene flow in a continuously distributed large terrestrial carnivore - the brown bear (Ursus arctos) in Northern Europe Genetisk struktur og genflyt i et kontinuerlig distribuert stort rovdyr - den nordeuropeiske brunbjørn (Ursus arctos) Julia Schregel Genetic structure and gene flow in a continuously distributed large terrestrial carnivore - the brown bear (Ursus arctos) in Northern Europe Genetisk struktur og genflyt i et kontinuerlig distribuert stort rovdyr - den nordeuropeiske brunbjørn (Ursus arctos) Philosophiae Doctor (PhD) Thesis Julia Schregel Department of Ecology and Natural Resource Management Faculty of Environmental Science and Technology Norwegian University of Life Sciences Ås 2015 Thesis number 2015:72 ISSN 1894-6402 ISBN 978-82-575-1309-2 PhD supervisors Dr Snorre B. Hagen1 Dr Hans Geir Eiken1 Professor Jon E. Swenson2 1Norwegian Institute of Bioeconomy (NIBIO), Section of Biotechnology and Molecular Genetics, Frederik A. Dahls vei 20, N-1430 Ås, Norway 2NMBU, Department of Ecology and Natural Resource Management P.O.Box 5003, N-1432 Ås, Norway PhD evaluation committee Professor Ettore Randi University of Bologna Instituto Superiore per la protezione e la Ricerca Ambientale (ISPRA) Via Cà Fornacetta 9 I-40064 Ozzano dell'Emilia (BO), Italy Dr Øystein Flagstad Norwegian Institute for Nature Research (NINA) P.O.Box 5685 Sluppen N-7485 Trondheim, Norway Committee coordinator Dr Katrine Eldegard NMBU, Department of Ecology and Natural Resource Management P.O.Box 5003N-1432 Ås, Norway ii Table of contents Summary ................................................................................................................................... v Sammendrag ........................................................................................................................... vii List of papers ........................................................................................................................... ix Introduction .............................................................................................................................. 1 Objectives and their rational ................................................................................................... 5 How reliable are the microsatellite markers used to identify individuals and to study the genetic structure of brown bear populations? (Paper I) .................................................... 5 What is the genetic structure, connectivity, and diversity of the recovering Northern European brown bear population? (Paper II, III, IV, V) ........................................................ 5 What is the structure, diversity, and distribution of male brown bear lineages across the Northern European distribution zone? (Paper III) .................................................................. 6 What is the importance of male gene flow in the Northern European brown bear? (Paper III, IV, V) .................................................................................................................... 7 Do genetic analyses reflect the observed male-biased dispersal and female philopatry in the brown bear? (Paper III, IV, V) ..................................................................................... 8 What influence do scale and isolation by distance have on the result of the population genetic analysis? (Paper IV, V) .............................................................................................. 9 Material and Methods .............................................................................................................. 9 Study area ............................................................................................................................... 9 Study populations ................................................................................................................... 9 Sampling ............................................................................................................................... 10 DNA extraction and amplification ....................................................................................... 10 Testing for reliability of microsatellite markers ................................................................... 12 Statistical methods ................................................................................................................ 12 Results and Discussion ........................................................................................................... 16 How reliable are the microsatellite markers used to identify individuals and to study the genetic structure of brown bear populations? ................................................................. 16 What is the genetic structure, connectivity and diversity of the recovering Northern European brown bear population? ........................................................................................ 17 What is the structure, diversity and distribution of male brown bear lineages across the Northern European distribution zone? .................................................................................. 24 What is the importance of male gene flow in the Northern European brown bear? ............ 25 Do genetic analyses reflect the observed male-biased dispersal and female philopatry in the brown bear? ................................................................................................................ 27 What influence do scale and isolation-by-distance have on the results of population genetic analyses? .................................................................................................................. 29 Management implications and future perspective .............................................................. 31 Acknowledgements ................................................................................................................. 33 References ............................................................................................................................... 37 Papers I-V have separate page numbers iii iv Summary The aim of this thesis was to investigate large scale population structure and gene flow in the Northern European brown bear (Ursus arctos). Brown bears were reduced in numbers to near extinction during recent centuries due to human persecution, but have gradually recovered after protective measures were initiated. In this context, our goal was also to provide knowledge that will be of aid for current and future management. For this, we analyzed samples obtained at high spatial density from across the Northern European distribution zone in the course of regional and national monitoring schemes during 2005-2012, which allowed statistical analysis on various spatial scales. Sample material consisted of feces and hairs sampled in the field as well as tissue samples of bears shot legally. For the genetic analysis, we employed autosomal microsatellite markers (short-tandem repeats, STRs) and male specific Y chromosomal markers (STRs and single-nucleotide polymorphisms, SNPs). We used individual-based population genetic approaches (Bayesian assignment algorithms) to unveil population structure, F-statistics to estimate genetic differentiation, and spatial autocorrelation to assess fine-scale population structure. Population size (Nc), effective population size (Ne) and the ratio between these measures may have a practical value in wildlife conservation, and we investigated the temporal stability of these measures in a focal bear group in the Pasvik Valley between Norway, Finland and Russia. We also performed clustering and cluster placement analyses to identify the number of genetic clusters across Sweden and Norway and assess their spatial arrangement. Furthermore, we used the new DResD approach to i) identify the location of gene flow barriers and corridors and ii) determine the importance of limited dispersal distance as the structuring mechanism. This was done by correcting pairwise measures of genetic distance for isolation by distance (IBD). Initially, we validated 12 STR markers and established an analysis protocol that minimizes risks for genotyping errors and produces highly reliable genetic data valuable for increasing possibility for comparing genetic data in international brown bear studies. Next, we determined the average brown bear populations size (Nc) in the Pasvik Valley during 2005- 2010 to be between 40 and 45 individuals. Also we found a high Ne/Nc ratio, indicating gene flow from other populations. In the same study, a large scale analysis of population structure based on 477 individuals from the Pasvik Valley and three other regions (Karelia in Finland and Russia, Västerbotten in Sweden and Troms in Norway), revealed four distinct genetic clusters with low migration rates between the regions and indications of limited gene flow v towards the west. Using Y chromosomal markers on 443 males from Sweden, Norway, Finland and Northwestern Russia, we studied the importance male gene flow in the recovering Northern European brown bear. We found clear differences in distribution of Y-lineages across the study area depending on the amount of gene flow from the outside during the recovery process between the eastern and the western parts of Northern Europe. In the eastern parts
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