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Phylogeographic analysis and genetic cluster recognition for the conservation of Ural Owls (Strix uralensis) in Europe

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Abstract

The distribution of the Ural Owl (Strix uralensis) in Europe shrank dramatically at the end of the nineteenth century, largely through direct persecution. No genetic information on this species is available that could provide a basis for ongoing conservation and breeding programs. Here, we genetically analyzed wild and captive populations of European Ural Owls to provide data that can be used to establish sound and sustainable management strategies. We analyzed mitochondrial and nuclear markers to evaluate the morphology-based concept of two subspecies (Strix uralensis liturata and Strix uralensis macroura), to gain insights into the phylogeographic population structure, and to determine genetic clusters for management implications. Our results supported neither the morphological subspecies concept nor a strong phylogeographic population structure. However, they pointed toward a noteworthy genetic exchange in the western range of the distribution of this species. Structure analysis revealed five genetic clusters. We propose that genetic-cluster-based management is better suited to the conservation of European Ural Owls than the separate consideration of each local population. If applied in supportive breeding programs, genetic cluster recognition and its contribution to divergence and diversity would help to preserve the genetic variability of the captive breeding population and enable optimal genetic tuning of the captive population to correspond to the genetic constitution of the supported population.

Zusammenfassung

Phylogeographische Analyse und genetische Clustererkennung zum Schutz des Habichtskauzes ( Strix uralensis ) in Europa

Der Habichtskauz (Strix uralensis) hat gegen Ende des 19. Jahrhunderts viel von seinem früheren Verbreitungsgebiet, vor allem durch direkte Verfolgung verloren. Zu dieser Art ist keine genetische Information als Grundlage für laufende Erhaltungs- und Zuchtprogramme vorhanden. In der vorliegenden Studie haben wir Wild und Zuchtpopulationen genetisch analysiert um Grundlagen für ein solides und nachhaltiges Management zu erarbeiten. Wir analysierten mitochondriale und nukleare Marker, um das morphologie-basierte Konzept der zwei Unterarten (Strix u. liturata und Strix u. macroura) zu evaluieren, um Einblicke in die phylogeographische Struktur der Population zu erhalten und um genetische Cluster die einen Einfluss auf das Management haben, zu bestimmen. Unsere Ergebnisse unterstützt weder das morphologische Unterarten-Konzept, noch zeigen sie eine ausgeprägte phylogeographische Populationsstruktur. Es wurde jedoch ein nennenswerter genetischer Austausch im westlichen Bereich des Verbreitungsgebietes des Habichtkauzes in Europa festgestellt. STRUCTURE-Analysen ergaben fünf genetische Cluster. Managementstrategien auf der Basis von genetischen Clustern sind für die Erhaltung des Europäischen Habichtskautz nach unseren Ergebnissen, gegenüber der Berücksichtigung von einzelnen lokalen Populationen, zu bevorzugen. Die Beachtung von genetischen Clustern sowie deren Beitrag zur genetischen Divergenz und Diversität hilft die genetische Variabilität der Zuchtpopulation zu erhalten und ermöglicht eine optimale Abstimmung dieser an die genetische Konstitution der durch Auswilderungsmaßnahmen zu unterstützenden Population.

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References

  • Bajc M, Čas M, Ballian D, Kunovac S, Zubić G, Grubešić M, Zhelev P, Paule L, Grebenc T, Kraigher H (2011) Genetic differentiation of the western capercaillie highlights the importance of south-eastern Europe for understanding the species phylogeography. PLoS ONE 6(8):e23602

    Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenetics. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Barrowclough GF, Gutierrez RJ, Groth JG (1999) Phylogeography of Spotted Owl (Strix occidentalis) populations based on mitochondrial DNA sequences: gene flow, genetic structure and a novel biogeographic pattern. Evolution 53:919–931

    Article  CAS  Google Scholar 

  • Bauer HG, Bezzel E, Fiedler W (2005) Das Kompendium der Vögel Mitteleuropas, Bd. 1–3, 2nd edn. AULA-Verlag, Wiebelsheim

  • Bello N, Francino O, Sanchez A (2001) Isolation of genomic DNA from feathers. J Vet Diagn Investig 13:162–164

    Article  CAS  Google Scholar 

  • Brito PH (2005) The influence of Pleistocene glacial refugia on tawny owl genetic diversity and phylogeography in Western Europe. Mol Ecol 14:3077–3094

    Article  CAS  PubMed  Google Scholar 

  • Brito PH (2007) Contrasting patterns of mitochondrial and microsatellite genetic structure among Western European populations of tawny owls (Strix aluco). Mol Ecol 16:3423–3437

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Stones-Havas S, Thierer T, Wilson A (2007) Geneious v.3.0. http://www.geneious.com/

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581

    Article  CAS  PubMed  Google Scholar 

  • Engleder T (2006) Wiedereinbürgerung des Habichtskauzes (Strix uralensis) im oberösterreichischen Mühlviertel/Böhmerwald (2001/2002)—ein Erfahrungsbericht. In: Gamauf A, Berg H-M (eds) Greifvögel & Eulen in Österreich. Naturhistorisches Museum, Wien, pp 191–200

  • Engleder T (2007) Re-introduction of the Ural Owl (Strix uralensis) on the Austrian side of the Bohemian Forest Mts. in the year 2001. Tagungsbericht des Nationalparks Bayerischer Wald 8:72–75

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14:2611–2620

    Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  Google Scholar 

  • Fluxus Technology Ltd. (2009) Homepage. http://www.fluxus-engineering.com

  • Francis CM, Saurola P (2004) Estimating components of variance in demographic parameters of Tawny Owls, Strix aluco. Anim Biodiv Conserv 27:489–502

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambrigde

    Book  Google Scholar 

  • Genero F, Benussi E (2007) New data and status of Ural Owl (Strix uralensis) in Italy. Tagungsbericht des Nationalparks Bayerischer Wald 8:36–41

    Google Scholar 

  • Glutz von Blotzheim UN, Bauer KM (1989) Handbuch der Vögel Mitteleuropas Bd. IV: Falconiformes, 2nd edn. Aula-Verlag, Wiesbaden

  • Goudet J (2001) Fstat, a program to estimate and test gene diversities and fixation indices. J Hered 86:485–486

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hausknecht R, Kühn R (2007) Molecular genetic assistance in the breeding program of the Ural Owl (Strix uralensis) in the Bavarian Forest National Park. Tagungsbericht des Nationalparks Bayerischer Wald 8:82–87

    Google Scholar 

  • Hsu YC, Severinghaus LL, Lin YS, Li SH (2003) Isolation and characterization of microsatellite DNA markers from the Lanyu scops owl (Otus elegans botelensis). Mol Ecol Notes 3:595–597

    Article  CAS  Google Scholar 

  • Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting population subdivision. Mol Biol Evol 9:138–151

    CAS  PubMed  Google Scholar 

  • Isaksson M, Tegelström H (2002) Characterization of polymorphic microsatellite markers in a captive population of the eagle owl (Bubo bubo) used for supportive breeding. Mol Ecol Notes 2:91–93

    Article  CAS  Google Scholar 

  • IUCN (1998) Guidelines for re-introductions. IUCN/SSC Re-introduction Specialist Group, Gland/Cambridge

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Kloubec B, Bufka L, Lorenc T (2007) History and current status of the Ural Owl (Strix uralensis) on the Czech side of Bohemian Forest. Tagungsbericht des Nationalparks Bayerischer Wald 8:64–71

    Google Scholar 

  • Kohl S (1977) Über die taxonomische Stellung der südeuropäischen Habichtskäuze Strix uralensis macroura Wolf, 1810. Muzeul Brukenthal, Studii si Communicarie Muz Brukenthal 21:309–334

  • König C, Weick F (2008) Owls of the world, 2nd edn. Christopher Helm, London

    Google Scholar 

  • Koopman ME, Schable NA, Glenn TC (2004) Development and optimization of microsatellite DNA primers for boreal owls (Aegolius funereus). Mol Ecol Notes 4:376–378

    Article  CAS  Google Scholar 

  • Krištin A, Mihók J, Danko Š, Karaska D, Pačenovský S, Saniga M, Bodová M, Balázs C, Šotnár K, Koran J, Olekšák M (2007) Distribution, abundance and conservation of the Ural Owl Strix Uralensis in Slovakia. Tagungsbericht des Nationalparks Bayerischer Wald 8:8–15

    Google Scholar 

  • Lauga B, Cagnon C, D’Amico F, Karama S, Mouches C (2005) Phylogeography of the white-throated dipper Cinclus cinclus in Europe. J Ornithol 146:257–262

    Article  Google Scholar 

  • Lomolino MV, Riddle BR, Whittaker RJ, Brown JH (2006) Biogeography. Sinauer, Sunderland

    Google Scholar 

  • Lüttge U (2010) Plasticity and conservation. Natureza Conservação 8:120–126

    Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Marthinsen G, Wennerberg L, Solheim R, Lifjeld JT (2009) No phylogeographic structure in the circumpolar snowy owl (Bubo scandiacus). Conserv Genet 10:923–933

    Article  CAS  Google Scholar 

  • Mebs T, Scherzinger W (2000) Die Eulen Europas. Kosmos, Stuttgart

    Google Scholar 

  • Mikkola H (1983) Owls of Europe. Poyser, London

    Google Scholar 

  • Moritz C (1994) Defining “evolutionarily significant units” for conservation. Trends Ecol Evol 9:373–375

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Park SDE (2001) Trypanotolerance in West African Cattle and the population genetic effects of selection. Dissertation, University of Dublin, Dublin

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Petit RJ, Mousadik EA, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first generation migrants detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (2001) Selecting models of nucleotide substitution: an application to human immunodeficiency virus 1 (HIV-1). Mol Biol Evol 18:897–906

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multi-locus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9221

    Article  CAS  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  Google Scholar 

  • Saurola P (2007) Finish Ural Owls (Strix uralensis): an overview on population parameters. Tagungsberichte Nationalapark Bayerischer Wald 8:42–49

    Google Scholar 

  • Scherzinger W (2006) Die Wiederbegründung des Habichtskauz-Vorkommens Strix uralensis im Böhmerwald. Ornithol Anz 45:97–156

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) Mega4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

  • Thode AB, Maltbie M, Hansen LA, Green LD, Longmire JL (2002) Microsatellite markers for the Mexican spotted owl (Strix occidentalis lucida). Mol Ecol Notes 2:446–448

    Article  CAS  Google Scholar 

  • Tomiałojć L, Stawarczyk T (2003) Awifauna Polski, Tom II. PTPP “pro Natura,” Wrocław

  • Tyrberg T (1998) Pleistocene birds of the Palearctic: a catalogue. Publications of the Nuttall Ornithological Club, No. 27. Nuttall Ornithological Club, Cambridge

  • Vaurie C (1965) The birds of the Palearctic fauna—a systematic reference. Non-Passeriformes. Witherby, London

  • Vogt G, Huber M, Thiemann M, van den Boogaart G, Schmitz OJ, Schubart CD (2008) Production of different phenotypes from the same genotype in the same environment by developmental variation. J Exp Biol 211:510–523

    Article  CAS  PubMed  Google Scholar 

  • Vrezec A (2009) Melanism and plumage variation in macroura Ural Owl. Dutch Bird 31:159–170

    Google Scholar 

  • Vrezec A, Tome D (2004) Altitudinal segregation between Ural Owl Strix uralensis and Tawny Owl S. aluco: evidence for competitive exclusion in raptorial birds. Bird Study 51:264–269

    Article  Google Scholar 

  • Waples RS (1991) Pacific Salmon, Oncorhynchus spp., and the definition of “species” under the Endangered Species Act. Mar Fish Rev 53:11–20

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Google Scholar 

  • Wright S (1978) Evolution and the genetics of populations. Variability within and among natural populations, vol 4. University of Chicago Press, Chicago

  • Zink R (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proc R Soc Lond B 271:561–564

    Article  Google Scholar 

  • Zink RM, Barrowclough GF, Atwood JL, Blackwell-Rago RC (2000) Genetics, taxonomy, and conservation of the threatened California gnatcatcher. Conserv Biol 14:1394–1405

    Article  Google Scholar 

  • Zink RM, Kessen A, Line TV, Blackwell-Rago RC (2001) Comparative phylogeography of some aridland bird species. Condor 103:1–10

    Article  Google Scholar 

Download references

Acknowledgments

We thank H. Mägdefrau for financial support from the Tiergarten Nürnberg, Germany, G. Firmánszky and A. Avotins for providing samples for this study, and D. Cowley for comments to improve the manuscript.

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Correspondence to Ralph Kuehn.

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Communicated by M. Wink.

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Hausknecht, R., Jacobs, S., Müller, J. et al. Phylogeographic analysis and genetic cluster recognition for the conservation of Ural Owls (Strix uralensis) in Europe. J Ornithol 155, 121–134 (2014). https://doi.org/10.1007/s10336-013-0994-8

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