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Conservation Genetics of the Saimaa Ringed Seal

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Conservation Genetics of the Saimaa Ringed Seal dissertations Mi a Va ltonen Conservation genetics of | Mia 159 | No Valtonen | the Saimaa ringed seal – insights into the history of a critically endangered population A critically endangered subspecies of the ringed seal has remained Mi a Va ltonen isolated in Lake Saimaa in Finland Conservation genetics the of Saimaa ringed seal since the last glacial period, i.e., for nearly 10,000 years. The small Conservation genetics of population of ~300 seals is currently threatened by anthropogenic the Saimaa ringed seal factors, such as high by-catch mortality and climate change. This – insights into the history of a critically thesis examines changes in genetic endangered population diversity and population structure of the Saimaa ringed seal, and provides new information for conservation. Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences No 159 isbn 978-952-61-1582-5 (printed) issnl 1798-5668 issn 1798-5668 isbn 978-952-61-1583-2 (pdf) issnl 1798-5668 issn 1798-5676 MIA VALTONEN Conservation genetics of the Saimaa ringed seal – insights into the history of a critically endangered population Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences No 159 Academic Dissertation To be presented by permission of the Faculty of Science and Forestry for public examination in the Auditorium N100 in Natura Building at the University of Eastern Finland, Joensuu, on October, 31, 2014, at 12 noon Department of Biology Grano Joensuu, 2014 Editors: Prof. Pertti Pasanen, Prof. Pekka Kilpeläinen, Prof. Kai Peiponen, Prof. Matti Vornanen Cover photo: Mervi Kunnasranta Distribution: Eastern Finland University Library / Sales of publications [email protected] www.uef.fi/kirjasto ISBN: 978‐952‐61‐1582‐5 (printed) ISSNL: 1798‐5668 ISSN: 1798‐5668 ISBN: 978‐952‐61‐1583‐2 (PDF) ISSNL: 1798‐5668 ISSN: 1798‐5676 Author’s address: University of Eastern Finland Department of Biology P.O. Box 111 80101 JOENSUU FINLAND email: [email protected] Supervisors: Associate Professor Tommi Nyman, Ph.D. University of Eastern Finland Department of Biology P.O. Box 111 80101 JOENSUU FINLAND email: [email protected] Senior Researcher Mervi Kunnasranta, Ph.D. University of Eastern Finland Department of Biology P.O. Box 111 80101 JOENSUU FINLAND email: [email protected] Docent Minna Ruokonen, Ph.D. University of Oulu Department of Biology P.O. Box 3000 90014 OULU FINLAND Docent Jukka Palo, Ph.D. University of Helsinki Hjelt Institute, Department of Forensic Medicine P.O. Box 40 00014 HELSINKI FINLAND email: [email protected] Professor Jouni Aspi, Ph.D. University of Oulu Department of Biology P.O. Box 3000 90014 OULU FINLAND email: [email protected] Reviewers: Professor David Coltman, Ph.D University of Alberta Department of Biological Sciences EDMONTON, ALBERTA T6G 2E9 CANADA email: [email protected] Senior Researcher Liselotte Andersen, Ph.D University of Aarhus Department of Bioscience Grenåvej 14 8410 RØNDE DENMARK email: [email protected] Opponent: Professor Craig Primmer, Ph.D University of Turku Department of Biology 20014 TURKU FINLAND email: [email protected] ABSTRACT Small and isolated populations lose genetic diversity, the raw material of evolution, more rapidly than do large populations, which may make them more vulnerable to demographic and environmental stochasticity. Fragmentation of an already small population may further increase its extinction risk by intensifying such effects in the even smaller subpopulations. The Saimaa ringed seal (Phoca hispida saimensis) represents an ideal study system for investigating the genetic and demographic effects of long isolation, small population size, and spatial subdivision. This critically endangered subspecies of c. 300 seals inhabits the highly fragmented Lake Saimaa in southeastern Finland. The population has remained completely isolated for c. 9,500 years and is currently threatened by anthropogenic factors, such as high by‐catch mortality and climate change. This thesis examines spatial and temporal variation in genetic diversity of the Saimaa ringed seal. For this, tissue samples collected from seal carcasses (N = 212) in 1980– 2008 and placentas (N = 66) collected from birth‐lair sites during 2000–2011 were examined for mtDNA and microsatellite variation. A new method of non‐invasive genetic sampling was developed, demonstrating the utility of placentas for reliable DNA genotyping. The diversity of the Saimaa population was contrasted with the levels found in populations sharing the same ancestry, Baltic (P. h. botnica; N = 21) and Ladoga (P. h. ladogensis; N = 16) ringed seals. The results show that genetic diversity of the Saimaa ringed seal is extremely low, with observed microsatellite heterozygosity for this subspecies (HE = 0.36) being the lowest recorded within the order Pinnipedia. Effective population sizes estimated for the total population and regional subpopulations were also very low (NE = 5–113), suggesting that the population is too small to maintain its current diversity in the long term. Although coalescent simulations indicated that most of the original diversity was lost during the long isolation, we observed a decrease in diversity also during the past decades, which suggests ongoing diversity loss in the population. Moreover, Bayesian clustering analyses revealed significant differentiation among the breeding areas. The fine‐scaled structuring of the Saimaa population is surprising, because in marine ringed seals only weak differentiation has been detected even among subpopulations located thousands of kilometres apart. In the Saimaa ringed seal, the population structure is most likely induced by the small subpopulation sizes and fragmented lacustrine habitat, but also by behavioural patterns of the seals. Overall gene flow within the lake is limited, as females are philopatric and, although males appear to be more prone to disperse, gene flow mediated by males is insufficient for counteracting the effects of genetic drift. The findings of the present study indicate that genetic diversity of the Saimaa ringed seal will inevitably continue to decrease unless its population size can be increased substantially. Additionally, the observed fine‐scaled structuring of the population raises concerns about the viability of subpopulations. Therefore, as rapid population growth is improbable in this slowly reproducing species, short‐term conservation efforts (e.g., translocations of adult seals) should focus on facilitating gene flow among breeding areas. Universal Decimal Classification: 574.3, 575.113.2, 575.17, 575.22, 599.745.3 CAB Thesaurus: seals; Phoca hispida; effective population size; gene flow; genetic diversity; genetics; monitoring; placenta; mitochondrial DNA; microsatellites; heterozygosity; genotypes; population structure; spatial variation; temporal variation Yleinen suomalainen asiasanasto: hylkeet; norppa; saimaannorppa; populaatiot; koko; rakenne; vaihtelu; genetiikka; geenit; geneettinen monimuotoisuus; genotyyppi; seuranta; näytteenotto; istukka; mitokondrio‐ DNA; mikrosatelliitit Preface There are so many people that I wish to thank for their help, encouragement and support during this long journey. First of all, I wish to acknowledge my numerous supervisors located in different parts of the country, from whom each I learned so much. I want to thank Tommi Nyman for providing me the opportunity to study Saimaa ringed seal genetics and all his help during the preparation of this thesis. Your high standards taught me what it requires to make proper science. I am grateful to Mervi Kunnasranta, whose idea this PhD project originally was. You taught me how important it is to translate my results into common sense – what do they mean and what is their real‐ world relevance, if any. I also wish to express my gratitude to Jukka Palo, whose PhD work provided the basis for this study. Your enthusiasm for the subject has been extremely inspiring and your endless support invaluable along the sometimes not so smooth road. I also want to acknowledge Minna Ruokonen, who patiently guided my first steps into the field of population genetics. Sadly, she passed away two years ago. Jouni Aspi replaced Minna as my supervisor. I deeply appreciate that you shared your broad experience with me, your expert advice and never‐failing encouragement. I thank my co‐authors for their help with several issues: Hanna Buuri for her contribution to the placental lab work, Matti Heino for his huge effort in genotyping placentas and help in data analyses, and Tuomo Kokkonen, who tragically perished recently, for seamless co‐operation, especially in organising the field‐collection of placentas. I am grateful to Markku Viljanen for his help with the funding issues, Heikki Hyvärinen for his helpful comments, and Gernot Segelbacher for his major help and support during the final meters of the thesis. I sincerely thank David Coltman and Liselotte Andersen for their thorough reviews of this thesis. Further, I am grateful to Jukka Jernvall and Petri Auvinen for providing me the opportunity to continue and expand my research on the Saimaa ringed seal genetics. There are a number of sponsors which made this research possible: the Maj and Tor Nessling Foundation, Saimaa Ringed Seal Genome Project, Raija and Ossi Tuuliainen Foundation, Kuopio Naturalists’ Society, Nestori Foundation, Finnish Foundation for Nature
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