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Optimizing the genetic management of reintroduction projects: genetic population structure of the captive Northern Bald Ibis population

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Abstract

Many threatened species are bred in captivity for conservation purposes and some of these programmes aim at future reintroduction. The Northern Bald Ibis, Geronticus eremita, is a Critically Endangered bird species, with recently only one population remaining in the wild (Morocco, Souss Massa region). During the last two decades, two breeding programs for reintroduction have been started (in Austria and Spain). As the genetic constitution of the founding population can have strong effects on reintroduction success, we studied the genetic diversity of the two source populations for reintroduction (‘Waldrappteam’ and ‘Proyecto eremita’) as well as the European zoo population (all individuals held ex situ) by genotyping 642 individuals at 15 microsatellite loci. To test the hypothesis that the wild population in Morocco and the extinct wild population in the Middle East belong to different evolutionary significant units, we sequenced two mitochondrial DNA fragments. Our results show that the European zoo population is genetically highly structured, reflecting separate breeding lines. Genetic diversity was highest in the historic samples from the wild eastern population. DNA sequencing revealed only a single substitution distinguishing the wild eastern and wild western population. Contrary to that, the microsatellite analysis showed a clear differentiation between them. This suggests that genetic differentiation between the two populations is recent and does not confirm the existence of two evolutionary significant units. The European zoo population appears to be vital and suitable for reintroduction, but the management of the European zoo population and the two source populations for reintroductions can be optimized to reach a higher level of admixture.

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References

  • Alcaide M, Negro JJ, Serrano D, Antolín JL, Casado S, Pomarol M (2010) Captive breeding and reintroduction of the lesser kestrel Falco naumanni: a genetic analysis using microsatellites. Conserv Genet 11:331–338. https://doi.org/10.1007/s10592-009-9810-7

    Article  Google Scholar 

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709

    Article  PubMed  CAS  Google Scholar 

  • Armstrong DP, Seddon PJ (2008) Directions in reintroduction biology. Trends Ecol Evol 23:20–25

    Article  PubMed  Google Scholar 

  • Attard CRM, Moller LM, Sasaki M, Hammer MP, Bice CM, Brauer CJ, Carvalho DC, Harris JO, Beheregaray LB (2016) A novel holistic framework for genetic-based captive-breeding and reintroduction programs. Conserv Biol 30:1060–1069. https://doi.org/10.1111/cobi.12699

    Article  PubMed  CAS  Google Scholar 

  • Ballou JD, Lacy RC (1995) Identifying genetically important individuals for management of genetic diversity in pedigreed populations. In: Ballou JD, Gilpin M, Foose TJ (eds) Population management for survival & recovery. Analytical methods and strategies in small population conservation. Columbia Univ. Press, New York

    Google Scholar 

  • Ballou JD, Lees C, Faust LJ, Long S, Lynch C, Lackey LB, Foose TJ (2010) Demographic and genetic management of captive populations. In: Kleinmann DJ, Lumpkin S, Allen M, Harris H, Thompson K (eds) Wild mammals in captivity: principles and techniques for zoo management. University of Chicago Press, Chicago, pp 219–252

    Google Scholar 

  • Bartlett SE, Davidson WS (1991) Identification of Thunnus tuna species by the polymerase chain reaction and direct sequence analysis of their mitochondrial cytochrome b genes. Can J Fish Aquat Sci 48:309–317

    Article  CAS  Google Scholar 

  • BirdLife International (2015) Species factsheet: Geronticus eremita, BirdLife. http://datazone.birdlife.org/species/factsheet/22697488. Accessed 06 April 2017

  • Böhm C (2015) Northern Bald Ibis Geronticus eremita EEP studbook. Alpenzoo, Innsbruck

    Google Scholar 

  • Böhm C, Bowden CGR (2016) Northern Bald Ibis Conservation and Translocation Workshop. Report of 4th International Advisory Group for the Northern Bald Ibis (IAGNBI) Meeting Seekirchen, Austria; August 2016; p. 121

  • Böhm C, Pegoraro K (2011) Der Waldrapp. Die Neue Brehmbücherei 659. Westarp, Hohenwarsleben

    Google Scholar 

  • Bowden CGR (2015) International Single Species Action Plan for the Conservation of the NorthernBald Ibis (Geronticus eremita). AEWA Technical Series No. 55. Bonn

  • Bowden CGR, Aghnaj A, Smith KW, Ribi M (2003) The status and recent breeding performance of the critically endangered Northern Bald Ibis Geronticus eremita population on the Atlantic coast of Morocco. Ibis 145:419–431

    Article  Google Scholar 

  • Bowden CGR, Smith KW, El Bekkay M, Oubrou W, Aghnaj A, Jimenez-Armesto M (2008) Contribution of research to conservation action for the Northern Bald Ibis Geronticus eremita in Morocco. Bird Conserv Int 18:S74–S90. https://doi.org/10.1017/S0959270908000403

    Article  Google Scholar 

  • Bowkett AE (2009) Recent captive-breeding proposals and the return of the ark concept to global species conservation. Conserv Biol 23:773–776

    Article  PubMed  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  PubMed  CAS  Google Scholar 

  • Conde DA, Flesness N, Colchero F, Jones OR, Scheuerlein A (2011) An emerging role of zoos to conserve biodiversity. Science 331:1390–1391

    Article  PubMed  CAS  Google Scholar 

  • Conway WG (2011) Buying time for wild animals with zoos. Zoo Biol 30:1–8

    PubMed  Google Scholar 

  • Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843. https://doi.org/10.1111/j.1365-294X.2006.02994.x

    Article  PubMed  Google Scholar 

  • Cuarón AD (2005) Further role of zoos in conservation: monitoring wildlife use and the dilemma of receiving donated and confiscated animals. Zoo Biol 24:115–124. https://doi.org/10.1002/zoo.20040

    Article  Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214. https://doi.org/10.1111/1755-0998.12157

    Article  PubMed  CAS  Google Scholar 

  • Dolman PM, Collar NJ, Scotland KM, Burnside R (2015) Ark or park: the need to predict relative effectiveness of ex situ and in situ conservation before attempting captive breeding. J Appl Ecol 52:841–850. https://doi.org/10.1111/1365-2664.12449

    Article  Google Scholar 

  • Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Geneti Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7

    Article  Google Scholar 

  • Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475

    Article  PubMed  Google Scholar 

  • Edmands S, Timmerman CC (2003) Modeling factors affecting the severity of outbreeding depression: factores de Modelaje que Afectan la Severidad de la Depresión Exogámica. Conserv Biol 17:883–892. https://doi.org/10.1046/j.1523-1739.2003.02026.x

    Article  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. https://doi.org/10.1111/j.1365-294X.2005.02553.x

    Article  PubMed  CAS  Google Scholar 

  • Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107

    Article  Google Scholar 

  • Frankham R (2005) Stress and adaptation in conservation genetics. J Evol Biol 18:750–755. https://doi.org/10.1111/j.1420-9101.2005.00885.x

    Article  PubMed  CAS  Google Scholar 

  • Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333

    Article  PubMed  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, 2nd edn. Cambridge University Press Cambridge

    Book  Google Scholar 

  • Fritz J (2004) The Scharnstein Project: establishing a migratory tradition with handraised Waldrapp Ibises. WAZA Magazine 5: 16–19

    Google Scholar 

  • Fritz J, Unsöld M (2015) Internationaler Artenschutz im Kontext der IUCN reintroduction guidelines: Argumente zur Wiederansiedlung des Waldrapps Geronticus eremita in Europa. Vogelwarte 53:169–179

    Google Scholar 

  • Fritz J, Kramer R, Hoffmann W, Trobe D, Unsöld M (2017) Back into the wild: establishing a migratory Northern bald ibis Geronticus eremita population in Europe. Int Zoo Yearb 51:107–123. https://doi.org/10.1111/izy.12163

    Article  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): A computer program to calculate F-statistics. J Hered 866:485–486

    Article  Google Scholar 

  • Grepom BirdLife Maroc (2014) Rapport sur la reproduction de l’Ibis chauve dans la région de Souss-Massa. Saison 2014. http://grepom.org/programme-de-suivi-de-la-population-delibis-chauve-rapport-de-reproduction-saison-2014/. Accessed 06 April 2017

  • Grueber CE, Hogg CJ, Ivy JA, Belov K (2015) Impacts of early viability selection on management of inbreeding and genetic diversity in conservation. Mol Ecol 24:1645–1653. https://doi.org/10.1111/mec.13141

    Article  PubMed  Google Scholar 

  • Hedrick PW, Garcia-Dorado A (2016) Understanding inbreeding depression, purging and genetic rescue. Trends Ecol Evol 31:940–952. https://doi.org/10.1016/j.tree.2016.09.005

    Article  PubMed  Google Scholar 

  • Holderegger R, Segelbacher G (eds) (2016) Naturschutzgenetik. Ein Handbuch für die Praxis, Hauptverlag, Bern

    Google Scholar 

  • Ishtiaq F, Prakash V, Green RE, Johnson J (2015) Management implications of genetic studies for ex situ populations of three critically endangered Asian Gyps vultures. Anim Conserv 18:259–270

    Article  Google Scholar 

  • Ivy JA, Miller A, Lacy RC, DeWoody JA (2009) Methods and prospects for using molecular data in captive breeding programs: an empirical example using parma wallabies (Macropus parma). J Hered 100:441–454

    Article  PubMed  Google Scholar 

  • 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. https://doi.org/10.1093/bioinformatics/btm233

    Article  PubMed  CAS  Google Scholar 

  • Janes JK, Miller JM, Dupuis JR, Malenfant RM, Gorrell JC, Cullingham CI, Andrew RL (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602. https://doi.org/10.1111/mec.14187

    Article  PubMed  Google Scholar 

  • Jombart T (2015) An introduction to adegent 2.0.0, R-tutorial, Imperial College London

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Kirkwood JK (2003) Welfare, husbandry and veterinary care of wild animals in captivity: changes in attitudes, progress in knowledge and techniques. Int Zoo Yearb 38:124–130

    Article  Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Nat Acad Sci USA 86:6196–6200

    Article  PubMed  CAS  Google Scholar 

  • Lacy RC (1994) Managing genetic diversity in captive populations of animals. In: Bowles ML, Whelan CJ (eds) Restoration of endangered species. conceptual issues, planning and implementation. Cambridge University Press, Cambridge, pp 63–89

    Chapter  Google Scholar 

  • Landmann A (2015) Bestandsschutz, Bestandsstützung, Wiederansiedlung oder Auswilderung-Wie kann oder soll der Waldrapp Geronticus eremita geschützt werden? Vogelwarte 53:169–180

    Google Scholar 

  • Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629

    Article  PubMed  Google Scholar 

  • Muñoz AR, Ramírez J (2017) Reintroduced northern bald ibises from Spain reach Moroco. Oryx 51:204–205. https://doi.org/10.1017/S0030605317000138

    Article  Google Scholar 

  • Palsbøll PJ, Berube M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16

    Article  PubMed  Google Scholar 

  • Paton TA, Baker AJ (2006) Sequences from 14 mitochondrial genes provide a well-supported phylogeny of the Charadriiform birds congruent with the nuclear RAG-1 tree. Mol Phyl Evol 39:657–667

    Article  CAS  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pegoraro K, Föger M, Parson W (2001) First evidence of mtDNA sequence differences between Northern Bald Ibises (Geronticus eremita) of Moroccan and Turkish origin. Journal für Ornithologie 142:425–428

    Article  Google Scholar 

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

    PubMed  PubMed Central  CAS  Google Scholar 

  • Quevedo MA, Sánchez I, Aguilar JM, Cuandrado M 2004: Projecto Eremita: a study of different releasing techniques. WAZA Magazine 5:20–23

    Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Saura M, Perez-Figueroa A, Fernandez J, Toro MA, Caballero A (2008) Preserving population allele frequencies in ex situ conservation programs. Conserv Biol 22:1277–1287. https://doi.org/10.1111/j.1523-1739.2008.00992.x

    Article  PubMed  Google Scholar 

  • Schenker A (1977) Das ehemalige Verbreitungsgebiet des Waldrapps Geronticus eremita in Europa. Ornithologische Beobachtungen 74:13–30

    Google Scholar 

  • Schulte U, Veith M, Hochkirch A (2012) Rapid genetic assimilation of native wall lizard populations (Podarcis muralis) through extensive hybridization with introduced lineages. Mol Ecol 21:4313–4326

    Article  PubMed  Google Scholar 

  • Seddon PJ, Armstrong DP, Maloney RF (2007) Developing the science of reintroduction biology. Conserv Biol 21:303–312. https://doi.org/10.1111/j.1523-1739.2006.00627.x

    Article  PubMed  Google Scholar 

  • Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629

    Article  PubMed  Google Scholar 

  • Serra G, Abdallah M, Assaed A, Abdallah A, Al Qaim G, Fayad T, Williamson D (2004) Discovery of a relict breeding colony of northern bald ibis Geronticus eremita in Syria. Oryx 38:106–108

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thaler E, Ettel E, Job S (1981) Zur Sozialstruktur des WaldrappsGeronticus eremita—Beobachtungen an der Brutkolonie des Alpenzoos Innsbruck. Journal für Ornithologie 122:109–128

    Article  Google Scholar 

  • Tintner A, Kotrschal K (2001) Waldrappen im Freiflug-Das Grünauer Waldrapp-Projekt. Zoologischer Garten 71:118–127

    Google Scholar 

  • Tracy LN, Wallis GP, Efford MG, Jamieson IG (2011) Preserving genetic diversity in threatened species reintroductions: how many individuals should be released? Anim Cons 14:439–446

    Article  Google Scholar 

  • Unsöld M, Fritz J (2011) Der Waldrapp: Ein Vogel zwischen Ausrottung und Wiederkehr. Wildbiologie 2:1–16

    Google Scholar 

  • van Dyke F (2008) Conservation biology: foundations, concepts, applications. Springer Science & Business Media, Berlin

    Book  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DM, Shipley P (2004) MICROCHECKER:MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Wan Q, Wu H, Fujihara T, Fang S (2004) Which genetic marker for which conservation genetics issue? Electrophoresis 25:2165–2176

    Article  PubMed  CAS  Google Scholar 

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756

    Article  PubMed  Google Scholar 

  • Willoughby JR, Sundaram M, Wijayawardena BK, Kimble SJ, Ji Y, Fernandez NB, Antonides JD, Lamb MC, Marra NJ, DeWoody JA (2015) The reduction of genetic diversity in threatened vertebrates and new recommendations regarding IUCN conservation rankings. Biol Cons 191:495–503. https://doi.org/10.1016/j.biocon.2015.07.025

    Article  Google Scholar 

  • Wirtz S, Böhm C, Fritz J, Hankeln T, Hochkirch A (2016) Isolation of microsatellite loci by next-generation sequencing of the critically endangered Northern Bald Ibis, Geronticus eremita. J Hered 107:363–366. https://doi.org/10.1093/jhered/esw013

    Article  PubMed  PubMed Central  Google Scholar 

  • Witzenberger KA, Hochkirch A (2011) Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers Conserv 20:1843–1861. https://doi.org/10.1007/s10531-011-0074-4

    Article  Google Scholar 

  • Witzenberger KA, Hochkirch A (2014) The genetic integrity of the ex situ population of the European Wildcat (Felis silvestris silvestris) is seriously threatened by introgression from domestic cats (Felis silvestris catus). PLoS ONE 9:e106083. https://doi.org/10.1371/journal.pone.0106083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

We thank all institutions (Appendix S1) for kindly providing genetic samples and supporting the project. For the transfer of samples from non-EU member states all necessary CITES permits have been granted.

Funding

This work was supported with 50% contribution of the LIFE financial instrument of the European Union (LIFE + 12-BIO_AT_000143, LIFE Northern Bald Ibis), performed with eight partners from Austria, Italy and Germany. Furthermore, the study is part of a PhD thesis funded by the Friedrich Naumann Foundation for Freedom. SW is also a member of the interdisciplinary graduate school “Cooperation of Science and Jurisprudence in Improving Development and Use of Standards for Environmental Protection—Strategies for Risk Assessment and Management” funded by the German Science Foundation (DFG, GRK 1319).

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Authors and Affiliations

  1. Department of Biogeography, Trier University, 54286, Trier, Germany

    Sarah Wirtz, Michael Veith & Axel Hochkirch

  2. Alpenzoo Innsbruck-Tirol, Weiherburggasse 37, 6020, Innsbruck, Austria

    Christiane Böhm

  3. Waldrappteam, LIFE+12-BIO_AT_000143, Schulgasse 28, 6162, Mutters, Austria

    Johannes Fritz

  4. Core facility Konrad Lorenz Forschungsstelle, University of Vienna, 4645, Grünau, Austria

    Kurt Kotrschal

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  1. Sarah Wirtz
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  2. Christiane Böhm
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  3. Johannes Fritz
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  4. Kurt Kotrschal
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  5. Michael Veith
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  6. Axel Hochkirch
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Correspondence to Sarah Wirtz.

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Wirtz, S., Böhm, C., Fritz, J. et al. Optimizing the genetic management of reintroduction projects: genetic population structure of the captive Northern Bald Ibis population. Conserv Genet 19, 853–864 (2018). https://doi.org/10.1007/s10592-018-1059-6

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