Advertisement

Journal of Ornithology

, Volume 155, Issue 1, pp 121–134 | Cite as

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

  • Roland Hausknecht
  • Susanne Jacobs
  • Jörg Müller
  • Richard Zink
  • Hans Frey
  • Roar Solheim
  • Al Vrezec
  • Anton Kristin
  • Jozef Mihok
  • Ilze Kergalve
  • Pertti Saurola
  • Ralph Kuehn
Original Article

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.

Keywords

Recovery strategy Subspecies Mitochondrial control region Microsatellites Supportive breeding 

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.

Notes

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.

References

  1. 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
  2. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenetics. Mol Biol Evol 16:37–48PubMedCrossRefGoogle Scholar
  3. 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 53:919–931CrossRefGoogle Scholar
  4. Bauer HG, Bezzel E, Fiedler W (2005) Das Kompendium der Vögel Mitteleuropas, Bd. 1–3, 2nd edn. AULA-Verlag, WiebelsheimGoogle Scholar
  5. Bello N, Francino O, Sanchez A (2001) Isolation of genomic DNA from feathers. J Vet Diagn Investig 13:162–164CrossRefGoogle Scholar
  6. Brito PH (2005) The influence of Pleistocene glacial refugia on tawny owl genetic diversity and phylogeography in Western Europe. Mol Ecol 14:3077–3094PubMedCrossRefGoogle Scholar
  7. Brito PH (2007) Contrasting patterns of mitochondrial and microsatellite genetic structure among Western European populations of tawny owls (Strix aluco). Mol Ecol 16:3423–3437PubMedCrossRefGoogle Scholar
  8. 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/
  9. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581PubMedCrossRefGoogle Scholar
  10. 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 191–200Google Scholar
  11. 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 8:72–75Google Scholar
  12. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14:2611–2620Google Scholar
  13. 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 10:564–567CrossRefGoogle Scholar
  14. 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 131:479–491PubMedGoogle Scholar
  15. Fluxus Technology Ltd. (2009) Homepage. http://www.fluxus-engineering.com
  16. Francis CM, Saurola P (2004) Estimating components of variance in demographic parameters of Tawny Owls, Strix aluco. Anim Biodiv Conserv 27:489–502Google Scholar
  17. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambrigdeCrossRefGoogle Scholar
  18. Genero F, Benussi E (2007) New data and status of Ural Owl (Strix uralensis) in Italy. Tagungsbericht des Nationalparks Bayerischer Wald 8:36–41Google Scholar
  19. Glutz von Blotzheim UN, Bauer KM (1989) Handbuch der Vögel Mitteleuropas Bd. IV: Falconiformes, 2nd edn. Aula-Verlag, WiesbadenGoogle Scholar
  20. Goudet J (2001) Fstat, a program to estimate and test gene diversities and fixation indices. J Hered 86:485–486Google Scholar
  21. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  22. 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 8:82–87Google Scholar
  23. 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 3:595–597CrossRefGoogle Scholar
  24. Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting population subdivision. Mol Biol Evol 9:138–151PubMedGoogle Scholar
  25. 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 2:91–93CrossRefGoogle Scholar
  26. IUCN (1998) Guidelines for re-introductions. IUCN/SSC Re-introduction Specialist Group, Gland/CambridgeGoogle Scholar
  27. 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 23:1801–1806PubMedCrossRefGoogle Scholar
  28. 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 8:64–71Google Scholar
  29. Kohl S (1977) Über die taxonomische Stellung der südeuropäischen Habichtskäuze Strix uralensis macroura Wolf, 1810. Muzeul Brukenthal, Studii si Communicarie Muz Brukenthal 21:309–334Google Scholar
  30. König C, Weick F (2008) Owls of the world, 2nd edn. Christopher Helm, LondonGoogle Scholar
  31. Koopman ME, Schable NA, Glenn TC (2004) Development and optimization of microsatellite DNA primers for boreal owls (Aegolius funereus). Mol Ecol Notes 4:376–378CrossRefGoogle Scholar
  32. 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 8:8–15Google Scholar
  33. Lauga B, Cagnon C, D’Amico F, Karama S, Mouches C (2005) Phylogeography of the white-throated dipper Cinclus cinclus in Europe. J Ornithol 146:257–262CrossRefGoogle Scholar
  34. Lomolino MV, Riddle BR, Whittaker RJ, Brown JH (2006) Biogeography. Sinauer, SunderlandGoogle Scholar
  35. Lüttge U (2010) Plasticity and conservation. Natureza Conservação 8:120–126Google Scholar
  36. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  37. Marthinsen G, Wennerberg L, Solheim R, Lifjeld JT (2009) No phylogeographic structure in the circumpolar snowy owl (Bubo scandiacus). Conserv Genet 10:923–933CrossRefGoogle Scholar
  38. Mebs T, Scherzinger W (2000) Die Eulen Europas. Kosmos, StuttgartGoogle Scholar
  39. Mikkola H (1983) Owls of Europe. Poyser, LondonGoogle Scholar
  40. Moritz C (1994) Defining “evolutionarily significant units” for conservation. Trends Ecol Evol 9:373–375PubMedCrossRefGoogle Scholar
  41. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  42. Park SDE (2001) Trypanotolerance in West African Cattle and the population genetic effects of selection. Dissertation, University of Dublin, DublinGoogle Scholar
  43. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  44. Petit RJ, Mousadik EA, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  45. 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 95:536–539PubMedCrossRefGoogle Scholar
  46. Posada D, Crandall KA (2001) Selecting models of nucleotide substitution: an application to human immunodeficiency virus 1 (HIV-1). Mol Biol Evol 18:897–906PubMedCrossRefGoogle Scholar
  47. Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multi-locus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  48. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9221PubMedCrossRefGoogle Scholar
  49. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  50. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedGoogle Scholar
  51. Saurola P (2007) Finish Ural Owls (Strix uralensis): an overview on population parameters. Tagungsberichte Nationalapark Bayerischer Wald 8:42–49Google Scholar
  52. Scherzinger W (2006) Die Wiederbegründung des Habichtskauz-Vorkommens Strix uralensis im Böhmerwald. Ornithol Anz 45:97–156Google Scholar
  53. Tamura K, Dudley J, Nei M, Kumar S (2007) Mega4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599Google Scholar
  54. Thode AB, Maltbie M, Hansen LA, Green LD, Longmire JL (2002) Microsatellite markers for the Mexican spotted owl (Strix occidentalis lucida). Mol Ecol Notes 2:446–448CrossRefGoogle Scholar
  55. Tomiałojć L, Stawarczyk T (2003) Awifauna Polski, Tom II. PTPP “pro Natura,” WrocławGoogle Scholar
  56. Tyrberg T (1998) Pleistocene birds of the Palearctic: a catalogue. Publications of the Nuttall Ornithological Club, No. 27. Nuttall Ornithological Club, CambridgeGoogle Scholar
  57. Vaurie C (1965) The birds of the Palearctic fauna—a systematic reference. Non-Passeriformes. Witherby, LondonGoogle Scholar
  58. 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 211:510–523PubMedCrossRefGoogle Scholar
  59. Vrezec A (2009) Melanism and plumage variation in macroura Ural Owl. Dutch Bird 31:159–170Google Scholar
  60. 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 51:264–269CrossRefGoogle Scholar
  61. Waples RS (1991) Pacific Salmon, Oncorhynchus spp., and the definition of “species” under the Endangered Species Act. Mar Fish Rev 53:11–20Google Scholar
  62. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  63. Wright S (1978) Evolution and the genetics of populations. Variability within and among natural populations, vol 4. University of Chicago Press, ChicagoGoogle Scholar
  64. Zink R (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proc R Soc Lond B 271:561–564CrossRefGoogle Scholar
  65. Zink RM, Barrowclough GF, Atwood JL, Blackwell-Rago RC (2000) Genetics, taxonomy, and conservation of the threatened California gnatcatcher. Conserv Biol 14:1394–1405CrossRefGoogle Scholar
  66. Zink RM, Kessen A, Line TV, Blackwell-Rago RC (2001) Comparative phylogeography of some aridland bird species. Condor 103:1–10CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2013

Authors and Affiliations

  • Roland Hausknecht
    • 1
  • Susanne Jacobs
    • 1
  • Jörg Müller
    • 2
    • 10
  • Richard Zink
    • 3
  • Hans Frey
    • 4
  • Roar Solheim
    • 5
  • Al Vrezec
    • 6
  • Anton Kristin
    • 7
  • Jozef Mihok
    • 4
  • Ilze Kergalve
    • 8
  • Pertti Saurola
    • 9
  • Ralph Kuehn
    • 1
    • 11
  1. 1.Chair of Zoology, Department of Animal SciencesCenter for Life and Food Sciences Weihenstephan, Technische Universität MünchenFreisingGermany
  2. 2.Nationalparkverwaltung Bayerischer WaldGrafenauGermany
  3. 3.Forschungsinstitut für Wildtierkunde und ÖkologieViennaAustria
  4. 4.Department für Pathobiologie, Institut für Parasitologie und ZoologieVet. Med. Universität WienViennaAustria
  5. 5.Agder Museum of Natural HistoryKistiansand SNorway
  6. 6.National Institute of BiologyLjubljanaSlovenia
  7. 7.Institute of Forest Ecology SASZvolenSlovakia
  8. 8.Baltic Environmental Forum LatviaRigaLatvia
  9. 9.Finnish Museum of Natural History, University of HelsinkiHelsinkiFinland
  10. 10.Terrestrial Ecology Research Group, Department of Ecology and Ecosystem ManagementCenter for Life and Food Sciences Weihenstephan, Technische Universität München FreisingFreisingGermany
  11. 11.Department of Fish, Wildlife and Conservation Ecology and Molecular Biology ProgramNew Mexico State UniversityLas CrucesUSA

Personalised recommendations