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      Genetic rescue of an endangered domestic animal through outcrossing with closely related breeds: A case study of the Norwegian Lundehund

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          Abstract

          Genetic rescue, outcrossing with individuals from a related population, is used to augment genetic diversity in populations threatened by severe inbreeding and extinction. The endangered Norwegian Lundehund dog underwent at least two severe bottlenecks in the 1940s and 1960s that each left only five inbred dogs, and the approximately 1500 dogs remaining world-wide today appear to descend from only two individuals. The Lundehund has a high prevalence of a gastrointestinal disease, to which all remaining dogs may be predisposed. Outcrossing is currently performed with three Nordic Spitz breeds: Norwegian Buhund, Icelandic Sheepdog, and Norrbottenspets. Examination of single nucleotide polymorphism (SNP) genotypes based on 165K loci in 48 dogs from the four breeds revealed substantially lower genetic diversity for the Lundehund (H E 0.035) than for other breeds (H E 0.209–0.284). Analyses of genetic structure with > 15K linkage disequilibrium-pruned SNPs showed four distinct genetic clusters. Pairwise F ST values between Lundehund and the candidate breeds were highest for Icelandic Sheepdog, followed by Buhund and Norrbottenspets. We assessed the presence of outlier loci among candidate breeds and examined flanking genome regions (1 megabase) for genes under possible selection to identify potential adaptive differences among breeds; outliers were observed in flanking regions of genes associated with key functions including the immune system, metabolism, cognition and physical development. We suggest crossbreeding with multiple breeds as the best strategy to increase genetic diversity for the Lundehund and to reduce the incidence of health problems. For this project, the three candidate breeds were first selected based on phenotypes and then subjected to genetic investigation. Because phenotypes are often paramount for domestic breed owners, such a strategy could provide a helpful approach for genetic rescue and restoration of other domestic populations at risk, by ensuring the involvement of owners, breeders and managers at the start of the project.

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          Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management.

          As populations become increasingly fragmented, managers are often faced with the dilemma that intentional hybridization might save a population from inbreeding depression but it might also induce outbreeding depression. While empirical evidence for inbreeding depression is vastly greater than that for outbreeding depression, the available data suggest that risks of outbreeding, particularly in the second generation, are on par with the risks of inbreeding. Predicting the relative risks in any particular situation is complicated by variation among taxa, characters being measured, level of divergence between hybridizing populations, mating history, environmental conditions and the potential for inbreeding and outbreeding effects to be occurring simultaneously. Further work on consequences of interpopulation hybridization is sorely needed with particular emphasis on the taxonomic scope, the duration of fitness problems and the joint effects of inbreeding and outbreeding. Meanwhile, managers can minimize the risks of both inbreeding and outbreeding by using intentional hybridization only for populations clearly suffering from inbreeding depression, maximizing the genetic and adaptive similarity between populations, and testing the effects of hybridization for at least two generations whenever possible.
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            Genetic rescue to the rescue.

            Genetic rescue can increase the fitness of small, imperiled populations via immigration. A suite of studies from the past decade highlights the value of genetic rescue in increasing population fitness. Nonetheless, genetic rescue has not been widely applied to conserve many of the threatened populations that it could benefit. In this review, we highlight recent studies of genetic rescue and place it in the larger context of theoretical and empirical developments in evolutionary and conservation biology. We also propose directions to help shape future research on genetic rescue. Genetic rescue is a tool that can stem biodiversity loss more than has been appreciated, provides population resilience, and will become increasingly useful if integrated with molecular advances in population genomics.
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              Revealing cryptic spatial patterns in genetic variability by a new multivariate method.

              Increasing attention is being devoted to taking landscape information into account in genetic studies. Among landscape variables, space is often considered as one of the most important. To reveal spatial patterns, a statistical method should be spatially explicit, that is, it should directly take spatial information into account as a component of the adjusted model or of the optimized criterion. In this paper we propose a new spatially explicit multivariate method, spatial principal component analysis (sPCA), to investigate the spatial pattern of genetic variability using allelic frequency data of individuals or populations. This analysis does not require data to meet Hardy-Weinberg expectations or linkage equilibrium to exist between loci. The sPCA yields scores summarizing both the genetic variability and the spatial structure among individuals (or populations). Global structures (patches, clines and intermediates) are disentangled from local ones (strong genetic differences between neighbors) and from random noise. Two statistical tests are proposed to detect the existence of both types of patterns. As an illustration, the results of principal component analysis (PCA) and sPCA are compared using simulated datasets and real georeferenced microsatellite data of Scandinavian brown bear individuals (Ursus arctos). sPCA performed better than PCA to reveal spatial genetic patterns. The proposed methodology is implemented in the adegenet package of the free software R.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                1 June 2017
                2017
                : 12
                : 6
                : e0177429
                Affiliations
                [1 ]Section of Biology and Environmental Science, Department of Chemistry and Bioscience, Aalborg University, Aalborg Øst, Denmark
                [2 ]Research Programs Unit, Molecular Neurology and Department of Veterinary Biosciences, University of Helsinki, and Folkhälsan Research Center, Helsinki, Finland
                [3 ]Department of Biosciences, University of Helsinki, Helsinki, Finland
                [4 ]Icelandic Genetic Resource Center, Hvanneyri, Borganes, Iceland
                [5 ]Nordic Genetic Resource Center, Ås, Norway
                [6 ]Norwegian Lundehund Club, Tangen, Trondheim, Norway
                [7 ]Centre for Biodiversity Dynamics, Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway
                [8 ]Department of Biosciences, Section for Genetics, Ecology and Evolution, Aarhus University, Aarhus C, Denmark
                [9 ]Queen Maud University College of Early Childhood Education, Trondheim, Norway
                [10 ]Aalborg Zoo, Aalborg, Denmark
                University of Florence, ITALY
                Author notes

                Competing Interests: HL owns stocks from Genoscoper Ltd that provides canine DNA diagnostics services, but the company has not been involved in any part of this study. There are no patents, products in development or marketed products to declare. This does not alter our adherence to all the PLOS ONE policies on sharing data and materials.

                • Conceptualization: TNK CP AVS.

                • Formal analysis: AVS ES HL TM.

                • Funding acquisition: TNK HJ HL CP.

                • Project administration: TNK CP.

                • Resources: BKB CM ISE KJ HJ.

                • Writing – original draft: AVS.

                • Writing – review & editing: AVS ES BKB PB ISE KJ HJ TNK CM TM HL CP.

                Author information
                http://orcid.org/0000-0002-5169-6736
                Article
                PONE-D-16-48367
                10.1371/journal.pone.0177429
                5453418
                28570553
                06b2984c-9488-44aa-90b2-8a90ec9567c2
                © 2017 Stronen et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 7 December 2016
                : 27 April 2017
                Page count
                Figures: 5, Tables: 3, Pages: 18
                Funding
                Funded by: The Norwegian Genetic Resource Center
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100008393, Teknologi og Produktion, Det Frie Forskningsråd;
                Award ID: 1337-00007
                Award Recipient :
                Funded by: Det Frie Forskningsråd (DK)
                Award ID: 21-01- 0526
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004836, Det Frie Forskningsråd;
                Award ID: 21-03-0125
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004836, Det Frie Forskningsråd;
                Award ID: 95095995
                Award Recipient :
                Funded by: Aalborg Zoo Conservation Foundation
                Award Recipient :
                Funded by: the Jane and Aatos Erkko Foundation
                Award Recipient :
                Funded by: the Jenny and Antti Wihuri Foundation
                Award Recipient :
                Funded by: the Academy of Finland
                Award Recipient :
                Funded by: Biocentrum Helsinki
                Award Recipient :
                Funded by: The Research Council of Norway
                Award ID: 221956
                Award Recipient :
                AVS received funding from the Danish Natural Science Research Council (postdoctoral grant 1337-00007). The study was partly supported by the Danish Natural Science Research Council grant number: #21-01- 0526, #21-03-0125 and 95095995, and the Aalborg Zoo Conservation Foundation (AZCF) for CP, the Jane and Aatos Erkko Foundation (HL), the Jenny and Antti Wihuri Foundation (ES), the Academy of Finland (HL), and Biocentrum Helsinki (HL). HJ was supported by grant number 221956 from the Research Council of Norway. A portion of the SNP analyses was financed by the Norwegian Genetic Resource Center.
                Categories
                Research Article
                Biology and Life Sciences
                Evolutionary Biology
                Population Genetics
                Genetic Polymorphism
                Biology and Life Sciences
                Genetics
                Population Genetics
                Genetic Polymorphism
                Biology and Life Sciences
                Population Biology
                Population Genetics
                Genetic Polymorphism
                Biology and Life Sciences
                Evolutionary Biology
                Population Genetics
                Biology and Life Sciences
                Genetics
                Population Genetics
                Biology and Life Sciences
                Population Biology
                Population Genetics
                Biology and Life Sciences
                Conservation Biology
                Conservation Genetics
                Ecology and Environmental Sciences
                Conservation Science
                Conservation Biology
                Conservation Genetics
                Biology and Life Sciences
                Genetics
                Conservation Genetics
                People and Places
                Population Groupings
                Ethnicities
                Norwegian People
                Biology and Life Sciences
                Genetics
                Genetic Loci
                Biology and Life Sciences
                Cell Biology
                Chromosome Biology
                Chromosomes
                Biology and Life Sciences
                Organisms
                Animals
                Animal Types
                Pets and Companion Animals
                Biology and Life Sciences
                Zoology
                Animal Types
                Pets and Companion Animals
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Dogs
                Custom metadata
                Data on individual and breeds included in this study, as well as their genomic SNP profiles, are available in the Dryad Digital Repository at: http://dx.doi.org/10.5061/dryad.5gm12.

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