Many reintroduction projects for conservation fail, and there are a large number of factors that may contribute to failure. Genetic analysis can be used to help stack the odds of a reintroduction in favour of success, by conducting assessment of source populations to evaluate the possibility of inbreeding and outbreeding depression and by conducting postrelease monitoring. In this study, we use a panel of 306 SNP (single nucleotide polymorphism) markers and 487-489 base pairs of mitochondrial DNA control region sequence data to examine 321 individuals from possible source populations of the Eurasian beaver for a reintroduction to Scotland. We use this information to reassess the phylogenetic history of the Eurasian beavers, to examine the genetic legacy of past reintroductions on the Eurasian landmass and to assess the future power of the genetic markers to conduct ongoing monitoring via parentage analysis and individual identification. We demonstrate the capacity of medium density genetic data (hundreds of SNPs) to provide information suitable for applied conservation and discuss the difficulty of balancing the need for high genetic diversity against phylogenetic best fit when choosing source population(s) for reintroduction.

Conservation Genetics Group Senckenberg Research Institute and Natural History Museum Frankfurt Gelnhausen Germany

Conservation Genetics Unit Institute of Botany Liège Belgium

Department of Community Ecology Helmholtz Centre for Environmental Research UFZ Halle Germany

Department of Zoology Faculty of Science Charles University Prague Czech Republic

Department of Zoology School of Biology and Biotechnology National University of Mongolia Ulaanbaatar Mongolia

Faculty of Natural Sciences Vilnius University Vilnius Lithuania

Martin Luther Universität Halle Wittenberg Institut für Biologie Bereich Zoologie Molekulare Ökologie Hoher Weg 4 Halle Saale Germany

Martin Luther Universität Halle Wittenberg Institut für Biologie Domplatz 4 Halle Saale Germany

Russian Research Institute of Game Management and Fur Farming Russian Academy of Sciences Kirov Russia

Telemark University College Department of Environmental Sciences Telemark Norway

Voronezh State Biosphere Reserve Voronezh Russia

WildGenes Laboratory Royal Zoological Society of Scotland Edinburgh UK

Zobrazit více v PubMed

Albrechtsen A, Nielsen FC, Nielsen R. Ascertainment biases in SNP chips affect measures of population divergence. Molecular Biology and Evolution. 2010;27:2534–2547. PubMed PMC

Allendorf FW, Hohenlohe PA, Luikart G. Genomics and the future of conservation genetics. Nature Reviews Genetics. 2010;11:697–709. PubMed

Babik W, Durka W, Radwan J. Sequence diversity of the MHC DRB gene in the Eurasian beaver (Castor fiber. Molecular Ecology. 2005;14:4249–4257. PubMed

Baird NA, Etter PD, Atwood TS, Currey MC, Shiver MC, Lewis ZA, Selker EU, et al. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE. 2008;3:e3376. PubMed PMC

Balloux F, Amos W, Coulson T. Does heterozygosity estimate inbreeding in real populations? Molecular Ecology. 2004;13:3021–3031. PubMed

Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution. 1999;16:37–48. PubMed

Barton NH, Hewitt GM. Analysis of hybrid zones. Annual Review of Ecology and Systematics. 1985;16:113–148.

Bensch S, Andrén H, Hansson B, Pedersen HC, Sand H, Sejberg D, Liberg O. Selection for heterozygosity gives hope to a wild population of inbred wolves. PLoS ONE. 2006;1:e72. PubMed PMC

Broadhurst LM, Lowe A, Coates DJ, Cunningham SA, McDonald M, Vesk PA, Yates C. Seed supply for broadscale restoration: maximizing evolutionary potential. Evolutionary Applications. 2008;1:587–597. PubMed PMC

Bryant D, Moulton V. Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Molecular Biology and Evolution. 2004;21:255–265. PubMed

Chang ZF, Luo MF, Liu ZJ, Yang JY, Xiang ZF, Li M, Vigilant L. Human influence on the population decline and loss of genetic diversity in a small and isolated population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana. Genetica. 2012;140:105–114. PubMed

Christie MR, Marine ML, French RA, Blouin MS. Genetic adaptation to captivity can occur in a single generation. Proceedings of the National Academy of Sciences of the United States of America. 2012;109:238–242. PubMed PMC

Coles B. Beavers in Britain's Past. Oxford, UK: Oxbow books; 2006.

Collett R. Bæveren i Norge, dens Utbredelsen og Levemaade (1896) Bergens Museums Aarbog. 1897;1:1–139.

Crawford J, Liu Z, Nelson T, Nielsen C, Bloomquist C. Isolation and characterization of microsatellite loci in the beaver (Castor canadensis. Molecular Ecology Resources. 2008;8:616–618. PubMed

Crnokrak P, Roff D. Inbreeding depression in the wild. Heredity. 1999;83:260–270. PubMed

Cullingham CI, Moehrenschlager A. Temporal analysis of genetic structure to assess population dynamics of reintroduced swift foxes. Conservation Biology: The Journal of the Society for Conservation Biology. 2013;27:1389–1398. PubMed

Darwin C. The Effects of Cross and Self Fertilisation in the Vegetable Kingdom. London, UK: John Murray; 1876.

De Barba M, Waits LP, Garton EO, Genovesi P, Randi E, Mustoni A, Groff C. The power of genetic monitoring for studying demography, ecology and genetics of a reintroduced brown bear population. Molecular ecology. 2010;19:3938–3951. PubMed

DeFaveri J, Viitaniemi H, Leder E, Merilä J. Characterizing genic and nongenic molecular markers: comparison of microsatellites and SNPs. Molecular ecology resources. 2013;13:377–392. PubMed

Dehnel A. Wykaz stanowisk bobra (Castor fiber vistulanus Matschie) w dorzeczu górnego i srodkowego Niemna oraz górnej Prypeci w latach 1937-1939. Fragmenta Faunistica Musei Zoologii Polonici. 1948;5:199–224. (in Polish)

Dewas M, Herr J, Schley L, Angst C, Manet B, Landry P, Catusee M. Recovery and status of native and introduced beavers Castor fiber and Castor canadensis in France and neighbouring countries. Mammal Review. 2012;42:144–165.

Durka W, Babik W, Ducroz J-F, Heidecke D, Rosell F, Samjaa R, Saveljev A, et al. Mitochondrial phylogeography of the Eurasian beaver Castor fiber L. Molecular Ecology. 2005;14:3843–3856. PubMed

Dzieciolowski R, Gozdziewski J. The reintroduction of European beaver, Castor fiber, in Poland. A success story. In: Busher PE, Dzieciolowski RM, editors. Beaver Protection, Management, and Utilization in Europe and North America. New York, NY: Kluwer Academic Press; 1999. pp. 31–35.

Edmands S, Feaman HV, Harrison JS, Timmerman CC. Genetic consequences of many generations of hybridization between divergent copepod populations. The Journal of Heredity. 2005;96:114–123. PubMed

El Alqamy H, Senn H, Roberts M-F, McEwing R, Ogden R. Genetic assessment of the Arabian oryx founder population in the Emirate of Abu Dhabi, UAE: an example of evaluating unmanaged captive stocks for reintroduction. Conservation Genetics. 2011;13:79–88.

Ellegren H, Hartman G, Johansson M, Andersson L. Major histocompatibility complex monomorphism and low levels of DNA fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proceedings of the National Academy of Sciences of the United States of America. 1993;90:8150–8153. PubMed PMC

Erickson DL, Fenster CB. Intraspecific hybridization and the recovery of fitness in the native legume Chamaecrista fasciculata. Evolution. 2006;60:225–233. PubMed

Etter PD, Preston JL, Bassham S, Cresko WA, Johnson EA. Local de novo assembly of RAD paired-end contigs using short sequencing reads. PLoS ONE. 2011;6:e18561. PubMed PMC

Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology. 2005;14:2611–2620. PubMed

Ewing SR, Nager RG, Nicoll MAC, Aumjaud A, Jones CG, Keller LF. Inbreeding and loss of genetic variation in a reintroduced population of Mauritius Kestrel. Conservation Biology: The Journal of the Society for Conservation Biology. 2008;22:395–404. PubMed

Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes. 2007;7:574–578. PubMed PMC

Fischer J, Lindenmayer D. An assessment of the published results of animal relocations. Biological Conservation. 2000;96:1–11.

Frahnert S. Ontogenetic changes of cranial proportions in beaver, Castor fiber L., 1758 (Rodentia, Castoridae): taxonomical implications and functional aspects. Bonner Zoologische Beiträge. 2000;49:131–153. (in German)

Frankham R. Conservation genetics. Annual Review of Genetics. 1995;29:305–327. PubMed

Frankham R. Inbreeding in the wild really does matter. Heredity. 2010;104:124. PubMed

Frankham R, Ballou J, Eldridge M, Lacy RC, Ralls K, Dudash MR, Fenster CB. Predicting the probability of outbreeding depression. Conservation Biology. 2011;25:465–475. PubMed

Frankham R, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC, Mendelsohn JR, et al. Implications of different species concepts for conserving biodiversity. Biological Conservation. 2012;153:25–31.

Fraser DJ, Bernatchez L. Adaptive evolutionary conservation: towards a unified. Molecular Ecology. 2001;10:2741–2752. PubMed

Freye H-A. Zur Systematik der Castoridae (Rodentia, Mammalia) Mitteilungen aus dem Zoologischen Museum in Berlin. 1960;36:105–122.

Frosch C, Haase P, Nowak C. First set of microsatellite markers for genetic characterization of the Eurasian beaver (Castor fiber) based on tissue and hair samples. European Journal of Wildlife Research. 2010;57:679–682.

Frosch C, Kraus RHS, Angst C, Allgöwer R, Michaux J, Teubner J, Nowak C. The genetic legacy of multiple beaver reintroductions in Central Europe. PLoS One. 2014 doi: 10.1371/journal.pone.0097619. PubMed DOI PMC

Germano JM, Bishop PJ. Suitability of amphibians and reptiles for translocation. Conservation Biology: The Journal of the Society for Conservation Biology. 2009;23:7–15. PubMed

Godefroid S, Piazza C, Rossi G, Buord S, Stevens A-D, Aguraiuja R, Cowell C, et al. How successful are plant species reintroductions? Biological Conservation. 2011;144:672–682.

Graphodatsky AS, Eremina VR, Orlov VN, Bulatova NSh, Lavrov VL. Numerous chromosome rearrangement in karyotype evolution of the beavers (Castor, Castoridae, Rodentia) of the Old and New World. Zoologicheskii Zhurnal. 1991;70:84–91. (In Russian with English summary)

Grueber CE, Jamieson IG. Quantifying and managing the loss of genetic variation in a free-ranging population of takahe through the use of pedigrees. Conservation Genetics. 2007;9:645–651.

Halley D. Sourcing Eurasian beaver Castor fiber stock for reintroductions in Great Britain and Western Europe. Mammal Review. 2011;41:40–53.

Halley D, Rosell F. The beaver ‘s reconquest of Eurasia : status, population development and management of a conservation success. Mammal Review. 2002;32:153–178.

Halley D, Rosell F. Population and distribution of European beavers (Castor fiber. Lutra. 2003;46:91–101.

Halley D, Rosell F, Saveljev A. Population and distribution of Eurasian beaver (Castor fiber. Baltic Foresty. 2012;18:168–175.

Haussler D, O'Brien SJ, Ryder OA, et al. Genome 10K: a proposal to obtain whole-genome sequence for 10 000 vertebrate species. The Journal of Heredity. 2009;100:659–674. PubMed PMC

Heidecke D. Taxonomical aspects of species conservation exemplified with the Eurasian beaver. Hercynia. 1986;2:146–161. (in German)

Heidecke D, Hörig K-J. Bestands- und Schutzsituation des Elbebibers. Halle and Magdeburg. 1986;23:1–14.

Horn S, Teubner J, Teubner J, Heidecke D. Mitochondrial DNA of beavers (Castor) in Germany. Artenschutzreport. 2010;26:72–78.

Horn S, Durka W, Wolf R, Ermala A, Stubbe A, Stubbe M, Hofreiter M. Mitochondrial genomes reveal slow rates of molecular evolution and the timing of speciation in beavers (Castor), one of the largest rodent species. PLoS ONE. 2011;6:e14622. PubMed PMC

Horn S, Prost S, Stiller M, Makowiecki D, Kuznetsova T, Benecke N, Pucher E, et al. Ancient mitochondrial DNA and the genetic history of Eurasian beaver (Castor fiber) in Europe. Molecular Ecology. 2014;23:1717–1729. PubMed

Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. PubMed

Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution. 2006;23:254–267. PubMed

IUCN. IUCN/SSC Guidelines for Re-Introductions. Gland, Switzerland: IUCN Species Survival Commission; 1998.

IUCN/SSC. Guidelines for Reintroductions and Other Conservation Translocations. Version 1.0. Gland, Switzerland: IUCN Species Survival Commission; 2013. viiii + 57 pp.

Kephart SR. Inbreeding and reintroduction: progeny success in rare Silene populations of varied density. Conservation Genetics. 2004;5:49–61.

Kim Y-K, Hong Y-J, Min M-S, Kim KS, Kim Y-J, Voloshina I, Myslenkov A, et al. Genetic status of Asiatic black bear (Ursus thibetanus) reintroduced into South Korea based on mitochondrial DNA and microsatellite loci analysis. The Journal of heredity. 2011;102:165–174. PubMed

Kitchener AC, Conroy JWH. The history of the Eurasian Beaver Castor fiber in Scotland. Mammal Review. 1997;27:95–108.

Kitchener AC, Lynch JM. A morphometric comparison of the skulls of fossil British and extant European beavers, Castor fiber. Scottish Natural Heritage Review. 2000;127:1–37.

Koelewijn HP, Pérez-Haro M, Jansman HAH, Boerwinkel MC, Bovenschen J, Lammertsma DR, Niewold FJJ, Kuiters AT. The reintroduction of the Eurasian otter (Lutra lutra) into the Netherlands: hidden life revealed by noninvasive genetic monitoring. Conservation Genetics. 2010;11:601–614.

Kogan MI. Foreign Fur Markets. Moscow, Russia: 1933. p. 243. Sovetskaya. (in Russian)

Kraus RHS, van Hooft P, Megens H-J, Tsvey A, Fokin SY, Ydenberg RC, Prins HHT. Global lack of flyway structure in a cosmopolitan bird revealed by a genome wide survey of single nucleotide polymorphisms. Molecular Ecology. 2013;22:41–55. PubMed

Kuehn R, Schwab G, Schröder W, Rottmann O. Differentiation of Castor fiber and Castor canadensis by non-invasive molecular methods. Zoo Biology. 2000;19:511–515. PubMed

Latch EK, Rhodes OE. The effects of gene flow and population isolation on the genetic structure of␣reintroduced wild turkey populations: are genetic signatures of source populations retained? Conservation Genetics. 2006;6:981–997.

Lavrov LS. Species of beavers (Castor) of the Palearctic. Zoologicheskii Zhurnal. 1979;58:88–96. (in Russian with English summary)

Lavrov LS, Hao-Tsuan L. Present conditions and ecological peculiarities of beaver in natural colonies in Asia. Vestnik Leningradskogo Universiteta. 1961;9:72–83.

Lavrov LS, Lavrov VL. Verteilung und Anzahl ursprünglicher and aborigener Biberpopulationen in der UdSSR. Zoologische Abhandlungen Staatliches Museum für Tierkunde Dresden. 1986;41:105–110. Nr.8: (in German)

Lavrov LS, Orlov VN. Karyotypes and taxonomy of modern beavers (Castor, Castoridae, Mammalia) Zoologicheskii Zhurnal. 1973;52:734–743. (In Russian with English summary)

Macdonald DW, Tattersall FH, Brown ED, Balharryt D. Reintroducing the European Beaver to Britain : nostalgic meddling or restoring biodiversity? Mammal Review. 1995;25:161–200.

Marshall TC, Spalton JA. Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Animal Conservation. 2000;3:241–248.

McClelland EK, Naish KA. What is the fitness outcome of crossing unrelated fish populations? A meta-analysis and an evaluation of future research directions. Conservation Genetics. 2006;8:397–416.

McEwing R, Frosch C, Rosell F, Campbell-Palmer R. A DNA assay for rapid discrimination between beaver species as a tool for alien species management. European Journal of Wildlife Research. 2014 doi: 10.1007/s10344-014-0803-6. DOI

Morin PA, Mccarthy M. Highly accurate SNP genotyping from historical and low-quality samples. Molecular Ecology Notes. 2007;7:937–946.

Morin PA, Luikart G, Wayne RK. SNPs in ecology, evolution and conservation. Trends in Ecology and Evolution. 2004;19:208–216.

Moritz C. Applications of mitochondrial DNA analysis in conservation: a critical review. Molecular Ecology. 1994;3:401–411.

Narum SR, Buerkle CA, Davey JW, Miller MR, Hohenlohe PA. Genotyping-by-sequencing in ecological and conservation genomics. Molecular Ecology. 2013;22:2841–2847. PubMed PMC

Nolet BA, Rosell F. Comeback of the beaver Castor fiber: an overview of old and new conservation problems. Biological Conservation. 1998;83:165–173.

Nummi P, Hahtola A. The beaver as an ecosystem engineer facilitates teal breeding. Ecography. 2008;31:519–524.

Nummi P, Pöysä H. Population and community level responses in Anas-species to patch disturbance caused by an ecosystem engineer, the beaver. Ecography. 1997;6:580–584.

Nummi P, Kattainen S, Ulander P, Hahtola A. Bats benefit from beavers: a facilitative link between aquatic and terrestrial food webs. Biodiversity and Conservation. 2011;20:851–859.

Ouborg NJ, Pertoldi C, Loeschcke V, Bijlsma RK, Hedrick PW. Conservation genetics in transition to conservation genomics. Trends in Genetics. 2010;26:177–187. PubMed

Ozer F, Gellerman H, Ashley MV. Genetic impacts of Anacapa deer mice reintroductions following rat eradication. Molecular ecology. 2011;20:3525–3539. PubMed

Paetkau D. Using genetics to identify intraspecific conservation units: a critique of current methods. Conservation Biology. 1999;13:1507–1509.

Patterson N, Price AL, Reich D. Population structure and eigenanalysis. PLoS Genetics. 2006;2:e190. PubMed PMC

Peakall R, Smouse PE. genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes. 2006;6:288–295. PubMed PMC

Pelz-Serrano K, Munguia-Vega A, Piaggio AJ, Neubaum M, Munclinger P, Pártl A, Van Riper C, et al. Development of nine new microsatellite loci for the American beaver, Castor canadensis (Rodentia: Castoridae), and cross-species amplification in the European beaver, Castor fiber. Molecular Ecology Resources. 2009;9:551–554. PubMed

Pemberton J. Measuring inbreeding depression in the wild: the old ways are the best. Trends in Ecology and Evolution. 2004;19:613–615. PubMed

Piertney SB, Stewart W, Lambin X, Telfer S, Aars J, Dallas JF. Phylogeographic structure and postglacial evolutionary history of water voles (Arvicola terrestris) in the United Kingdom. Molecular ecology. 2005;14:1435–1444. PubMed

Pritchard JK. Documentation for Structure Software: Version 2. 3. Chicago, IL: University of Chicago; 2010.

Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–959. PubMed PMC

Ralls K, Ballou J. Extinction: lessons from zoos. In: Schonewald-Cox CM, Chambers SM, MacBryde B, Thomas L, editors. Genetics and Conservation: A Reference for Managing Wild Animal and Plant Populations. Menlo Park, CA: Benjamin Cummings; 1983. pp. 164–184.

Richard PB. Peculiarities on the ecology and management of the Rhodanian Beaver (Castor fiber L.) Zeitschrift fuer Angewandte Zoologie. 1985;72:143–152.

Rosell F, Sun L. Use of anal gland secretion to distinguish the two beaver species Castor canadensis and C. fiber. Wildlife Biology. 1999;5:119–123.

Rosell F, Bozsér O, Collen P, Parker H. Castor fiber and Castor canadensis and their ability to modify ecosystems. Mammal Review. 2005;35:248–276.

Rosell F, Steifetten Ø. Subspecies discrimination in the Scandinavian beaver (Castor fiber): combining behavioral and chemical evidence. Canadian Journal of Zoology. 2004;82:902–909.

Rosell F, Campbell-Palmer R, Parker H. More genetic data are needed before populations are mixed: response to “Sourcing Eurasian beaver Castor fiber stock for reintroductions in Great Britain and Western Europe”. Mammal Review. 2012;42:319–324.

Ruiz-López MJ, Gañan N, Godoy JA, Del Olmo A, Garde J, Espeso G, Vargas A, et al. Heterozygosity-fitness correlations and inbreeding depression in two critically endangered mammals. Conservation Biology: The Journal of the Society for Conservation Biology. 2012;26:1121–1129. PubMed

Saveljev AP, Munclinger P, Albrechtova A. 2011. p. 418. Revision of an origin and “purity” of aboriginal beavers of Russia and Belarus with use new genetic data. Theriofauna of Russia and adjacent territories. Abst. Intern. Congress. Moscow (in Russian)

Schwab G. Biber und Bibermanagement in Bayern. Natur and Land. 2013;3:18–21.

Seddon PJ, Armstrong DP, Maloney RF. Developing the science of reintroduction biology. Conservation Biology. 2007;21:303–312. PubMed

Senn HV, Pemberton JM. Variable extent of hybridization between invasive sika (Cervus nippon) and native red deer (C. elaphus) in a small geographical area. Molecular Ecology. 2009;18:862–876. PubMed

Senn H, Ogden ROB, Cezard T, Gharbi K, Iqbal Z, et al. Reference-free SNP discovery for the Eurasian beaver from restriction site-associated DNA paired-end data. Molecular Ecology. 2013;22:3141–3150. PubMed

Serzhanin I. 1949;13:242–250. Modern distribution of the beaver in Belarus. Nauchno-Metodicheskie Zapiski Glavnogo Upravlenia po Zapovednikam. SM RSFSR (in Russian)

Sgrò CM, Lowe AJ, Hoffmann AA. Building evolutionary resilience for conserving biodiversity under climate change. Evolutionary Applications. 2011;4:326–337. PubMed PMC

Shephard JM, Ogden R, Tryjanowski P, Olsson O, Galbusera P. Is population structure in the European white stork determined by flyway permeability rather than translocation history? Ecology and Evolution. 2013;3:4881–4895. PubMed PMC

Slate J, David P, Dodds KG, Veenvliet BA, Glass BC, Broad TE, McEwan JC. Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity. 2004;93:255–265. PubMed

Spottiswoode C, Møller AP. Genetic similarity and hatching success in birds. Proceedings of the Royal Society B: Biological Sciences. 2004;271:267–272. PubMed PMC

Tallmon DA, Luikart G, Waples RS. The alluring simplicity and complex reality of genetic rescue. Trends in Ecology and Evolution. 2004;19:489–496. PubMed

Tollington S, Jones CG, reenwood AG, Tatayah V, Raisin C, Burke T, Dawson DA, Groombridge JJ. Long-term, fine-scale temporal patterns of genetic diversity in the restored Mauritius parakeet reveal genetic impacts of management and associated demographic effects on reintroduction programmes. Biological Conservation. 2013;161:28–38.

Townsend SM, Jamieson IG. Inbreeding influences within-brood heterozygosity-fitness correlations (HFCS) in an isolated passerine population. Evolution; International Journal Of Organic Evolution. 2013;67:2299–2308. PubMed

Vignal A, Milan D, SanCristobal M, Eggen A. A review on SNP and other types of molecular markers and their use in animal genetics. Genetics Selection Evolution. 2002;34:275–305. PubMed PMC

Vilas C, Miguel ESAN, Amaro R, Garcia C. Relative contribution of inbreeding depression and eroded adaptive diversity to extinction risk in small populations of shore campion. Conservation Biology. 2006;20:229–238. PubMed

Wang J, Lin M, Crenshaw A, Hutchinson A, Hicks B, Yeager M, Berndt S, et al. High-throughput single nucleotide polymorphism genotyping using nanofluidic Dynamic Arrays. BMC Genomics. 2009;10:561–574. PubMed PMC

Weeks AR, Sgro CM, Young AG, Frankham R, Mitchell NJ, Miller KA, Byrne M, et al. Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evolutionary Applications. 2011;4:709–725. PubMed PMC

Willing E-M, Bentzen P, van Oosterhout C, Hoffmann M, Cable J, Breden F, Weigel D, Dreyer C. Genome-wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies. Molecular Ecology. 2010;19:968–984. PubMed

Wisely SM, Santymire RM, Livieri TM, Mueting SA, Howard J. Genotypic and phenotypic consequences of reintroduction history in the black-footed ferret (Mustela nigripes. Conservation Genetics. 2007;9:389–399.

Zachos FE, Apollonio M, Bärmann EV, Festa-Bianchet M, Göhlich U, Habel JC, Haring E, et al. Species inflation and taxonomic artefacts—A critical comment on recent trends in mammalian classification. Mammalian Biology. 2013;78:1–6.