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Genetic assessment of the Iberian wolf Canis lupus signatus captive breeding program

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Abstract

The main goal of ex situ conservation programs is to improve the chances of long term survival of natural populations by founding and managing captive colonies that can serve as a source of individuals for future reintroductions or to reinforce existing populations. The degree in which a captive breeding program has captured the genetic diversity existing in the source wild population has seldom been evaluated. In this study we evaluate the genetic diversity in wild and captive populations of the Iberian wolf, Canis lupus signatus, in order to assess how much genetic diversity is being preserved in the ongoing ex situ conservation program for this subspecies. A sample of domestic dogs was also included in the analysis for comparison. Seventy-four wolves and 135 dogs were genotyped at 13 unlinked microsatellite loci. The results show that genetic diversity in Iberian wolves is comparable in magnitude to that of other wild populations of gray wolf. Both the wild and the captive Iberian wolf populations have a similarly high genetic diversity indicating that no substantial loss of diversity has occurred in the captive-breeding program. The effective number of founders of the program was estimated as ∼ ∼16, suggesting that all founders in the studbook pedigree were genetically independent. Our results emphasize also the genetic divergence between wolves and domestic dogs and indicate that our set of 13 microsatellite loci provide a powerful diagnostic test to distinguish wolves, dogs and their hybrids.

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References

  • Alonso P, Barrientos LM, Fernández A, Llaneza L, Rico M, de la Torre JA, Vilà C (1999) Situación actual del lobo en España. Quercus 157, 24–25

    Google Scholar 

  • Altet L, Francino O, Sánchez A (2001) Microsatellite polymorphism in closely related dogs. J. Hered. 92, 276–279

    Article  PubMed  CAS  Google Scholar 

  • Andersone Z, Lucchini V, Randi E, Ozolins J (2002) Hybridisation between wolves and dogs in Latvia as documented using mitochondrial and microsatellite DNA markers. Mamm. Biol. 67, 79–90

    Google Scholar 

  • Ballou JD, Foose TJ (1996) Demographic and genetic management of captive populations. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S (eds), Wild Mammals in Captivity. Principles and Techniques. The University of Chicago Press, Chicago, pp. 263–283

    Google Scholar 

  • Ballou JD, Lacy RC (1995) Identifying genetically important individuals for management of genetic diversity in pedigreed populations. Population Management for Survival and Recovery Analytical Methods and Strategies in Small Population Conservation. Columbia University Press, New York, pp. 76–111

    Google Scholar 

  • Baillie JEM, Hilton-Taylor C, Stuart SN (eds), (2004) IUCN Red List of Threatened Species. A Global Species Assessment. IUCN – The World Conservaqtion Union, Gland, Switzerland

    Google Scholar 

  • Blanco JC, Cuesta L, Reig S (1992) Distribution, status, and conservation problems of the wolf Canis lupus in Spain. Biol. Conserv. 60: 73–80

    Article  Google Scholar 

  • Blanco JC, Cortés Y (2002) Ecología, censos, percepción y evolución del lobo en España: Análisis de un conflicto. Sociedad Española para la Conservación y Estudio de los Mamíferos, Málaga, Spain

    Google Scholar 

  • Boitani L (2003) Wolf conservation and recovery. In: Mech LD, Boitani L (eds), Wolves. Behavior, Ecology, and Conservation. The University of Chicago Press, Chicago, pp. 317–344

    Google Scholar 

  • Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Amer. J. Hum. Genet., 32, 314–331

    PubMed  CAS  Google Scholar 

  • Bouman I, Bouman J (1994) The History of Przewalski’s Horse. In: Boyd L, Houpt KA (eds), Przewalski’s horse: The History and Biology of an Endangered Species. State University of New York Press, Albany, New York, pp. 5–39

    Google Scholar 

  • Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellite. Nature 368, 455–457

    Article  PubMed  CAS  Google Scholar 

  • Cabrera A (1907) Los lobos de España. Bol. R. Soc. Esp. Hist. Nat. 7, 193–198

    Google Scholar 

  • Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881–10890

    PubMed  CAS  Google Scholar 

  • Crandall KA, Bininda-Emonds OR, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol. Evol. 15, 290–295

    Article  PubMed  Google Scholar 

  • Denniston C (1978) Small population size and genetic diversity: Implications for endangered species. In: Temple (eds), Endangered Birds: Management Techniques for Preserving Threatened Species. University of Wisconsin Press, Madison, pp. 281–289

    Google Scholar 

  • Ellegren H (1999) Inbreeding relatedness in Scandinavian grey wolves Canis lupus. Hereditas 130, 239–244

    Article  PubMed  CAS  Google Scholar 

  • Enseñat C (1996) European Regional Studbook. Lobo ibérico Canis lupus signatus. Parc Zoològic de Barcelona, Barcelona, Spain

    Google Scholar 

  • Forbes SH, Boyd DK (1996) Genetic variation of naturally colonizing wolves in the central rocky mountains. Conserv. Biol. 10, 1082–1090

    Article  Google Scholar 

  • Francino O, Amills M, Sánchez A (1997) Canine Mhc DRB1 phenotyping by PCR-RFLP analysis. Anim. Genet. 28, 41–45

    Article  PubMed  CAS  Google Scholar 

  • Francisco LV, Langston AA, Mellersh CS, Neal CL, Ostrander EA (1996) A class of highly polymorphic tetranucleotide repeats for the canine genetic mapping. Mamm. Genome 7, 359–362

    Article  PubMed  CAS  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to Conservation Genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Fredholm M, Wintero AK (1995) Variation of short tandem repeats within and between species belonging to the Canidae family. Mamm. Genome 6, 11–18

    Article  PubMed  CAS  Google Scholar 

  • Fredrickson R, Hedrick P (2002) Body size in endangered Mexican wolves: effects of inbreeding and cross-lineage matings. Anim. Conserv. 5, 39–43

    Google Scholar 

  • Garcia-Moreno J, Matocq MD, Roy MS, Geffen E, Wayne RK (1996) Relationships ang genetic purity of the endangered mexican wolf based on análisis of microsatellite loci. Conserv. Biol. 10, 376–389

    Article  Google Scholar 

  • Geyer CJ, Ryder OA, Chemnick LG, Thompson EA (1993) Analysis of relatedness in the California condors, from DNA fingerprints. Mol. Biol. Evol. 10, 571–589

    CAS  Google Scholar 

  • Gottelli D, Sillero-Zubiri C, Applebaum GD, Roy MS, Girman DJ, Garcia-Moreno J, Ostranders EA, Wayne RK (1994) Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis. Mol. Ecol. 3, 301–312

    PubMed  CAS  Google Scholar 

  • Goudet J (2000) FSTAT Version 2.9.1. Computer Package for PCs. Institute of Ecology, Biology building, UNIL, CH-1015 Lausane, Switzerland

    Google Scholar 

  • Gray AP (1954) Mammalian Hybrids; A Check-List with Bibliography. Commonwealth Agricultural Bureaux, Famham Royal, Bucks, UK

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportions for multiple alleles. Biometrics 48, 361–372

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW, Miller PS, Geffen E, Wayne RK (1997) Genetic evaluation of the three captive mexican wolf lineages. Zoo Biol. 16, 47–69

    Article  Google Scholar 

  • Hedrick PW (2005) Genetics of Populations. 3rd ed. edition. Jones and Bartlett Publishers, Sudbyry Massachusetts

    Google Scholar 

  • Jamielson A (1994) The effectiveness of using codominant polymorphic allelic series for (1) checking pedigrees and (2) distinguishing full-sib pair members. Anim. Genet. 25, 37–44

    Google Scholar 

  • Kalinowski ST, Hedrick PW, Miller PS (1999) No inbreeding depression observed in Mexican and red wolf captive breeding programs. Conserv. Biol. 13, 131–137

    Article  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245

    Article  PubMed  CAS  Google Scholar 

  • Laikre L, Ryman N (1991) Inbreeding depression in a captive wolf (Canis lupus) population. Conserv. Biol. 5, 33–40

    Article  Google Scholar 

  • Laikre L, Ryman N, Thompson A (1993) Hereditary blindness in a captive wolf (Canis lupus) population: frequency reduction of a deleterious allele in relation to gene conservation. Conserv. Biol. 7, 592–601

    Article  Google Scholar 

  • Lariviere S, Crete M (1993) The size of eastern coyotes (Canis latrans): a comment. J. Mammal. 74, 1072–1074

    Article  Google Scholar 

  • Lehman N, Eisenhawer A, Hansen K, Mech LD, Peterson RO, Gogan PJP, Wayne RK (1991). Introgression of coyote mitochondrial-DNA into sympatric North-American Gray wolf populations. Evolution 45, 104–119

    Article  Google Scholar 

  • Lucchini V, Galov A, Randi E (2004) Evidence of genetic distinction and long-term population decline in wolves (Canis lupus) in the Italian Apennines. Mol. Ecol. 13, 523–536

    Article  PubMed  CAS  Google Scholar 

  • Mellersh CS, Langston AA, Acland GM, Fleming MA, Ray K, Wiegand NA, Francisco LV, Gibbs M, Aguirre G, Ostrander, EA (1997) A linkage map of the canine genome. Genomics 46, 326–336

    Article  PubMed  CAS  Google Scholar 

  • Mellersh CS, Hitte C, Richman M, Vignaux F, Priat C, Jouquand S, Werner P, Andraae C, DeRose S, Patterson DF, Ostrander EA, Galibert F (2000) An integrated linkage-radiation hybrid map of the canine genome. Mamm. Genome 11, 120–130

    Article  PubMed  CAS  Google Scholar 

  • Mengel RM (1971) A study of dog-coyotes hybrids and implications concerning hybridization in Canis. J. Mammal. 52, 316–336

    Article  PubMed  CAS  Google Scholar 

  • Mercure A, Ralls K, Koepfli KP, Wayne RK (1993) Genetic subdivisions among small canids – mitochondrial-DNA differentiation of swift, kit, and arctic foxes. Evolution 47, 1313–1328

    Article  Google Scholar 

  • Minch E, Ruiz-Linares A, Goldstein DB, Feldman MW, Cavalli-Sforza LL (1995) Microsat (version 1.4d): a computer program for calculating various statistics on microsatellite allele data. http://www.human.stanford.edu/microsat/microsat.html

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. USA 70, 3321–3323

    Article  PubMed  CAS  Google Scholar 

  • Nowak RM, (1979) North American Quaternary Canis. No. 6. Museum of Natural History, University of Kansas, Lawrence

    Google Scholar 

  • Nowak RM (2003) Wolf evolution and taxonomy. In: Mech LD, Boitani L (eds), Wolves. Behavior, Ecology, and Conservation. The University of Chicago Press, Chicago, pp. 239–258

    Google Scholar 

  • Ostrander EA, Mapa FA, Yee M, Rine J (1995) One hundred and one simple sequence repeats-based markers for the canine genome. Mamm. Genome 6, 192–195

    Article  PubMed  CAS  Google Scholar 

  • Pemberton JM, Slate J, Bamcroft DR, Barrett JA (1995) Nonamplifying alleles at microsatellites loci: a caution for parentage and population studies. Mol. Ecol. 4, 294–352

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Randi E, Lucchini V, Christensen MF, Mucci N, Funk SM, Dolf G, Loeschcke V (2000) Mitochondrial DNA variability in Italian and East European wolves: detecting the consequences of small population size and hybridization. Conserv. Biol. 14, 464–473

    Article  Google Scholar 

  • Randi E, Lucchini V (2002) Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analyses of microsatellite variation. Conserv. Biol. 3, 31–45

    CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (Version 3.1): population genetics software for exact test and ecumenicism. J. Hered. 86, 248–249

    Google Scholar 

  • Roy MS, Geffen E, Smith D, Ostrander EA, Wayne RK (1994) Patterns of differentiation and hybridization in North American wolflike canids, revealed by analysis of microsatellite loci. Mol. Biol. Evol. 11, 553–570

    PubMed  CAS  Google Scholar 

  • Roy MS, Geffen E, Smith D, Wayne RK (1996) Molecular genetics of pre-1940 red wolves. Conserv. Biol. 10, 1413–1424

    Article  Google Scholar 

  • Russello MA, Amato G (2004) Ex situ population management in the absence of pedigree information. Mol. Ecol. 13, 2829–2840

    Article  PubMed  CAS  Google Scholar 

  • Saccone C, Attimonelli M, Sbisa E (1987) Structural elements highly preserved during the evolution of the D-loop-containing region in vertebrate mitochondrial DNA. J. Mol. Evol. 26, 205–211

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425

    PubMed  CAS  Google Scholar 

  • Sillero-Zubiri C, Hoffman M, Macdonald DW (2004) Canids: foxes, wolves, jackals and dogs. Status survey and conservation action plan. IUCN/SSC Canid Specialist Group, Gland, Switzerland and Cambridge, UK

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research. W.H. Freeman and Co, New York

    Google Scholar 

  • Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc. Natl. Acad. Sci. USA 101, 15261–15264

    Article  PubMed  CAS  Google Scholar 

  • Storme V, Vanden Broeck A, Ivens B, et al. (2004) Ex-situ conservation of Black poplar in Europe: genetic diversity in nine gene bank collections and their value for nature development. Theor. Appl. Genet. 08, 969–981

    Article  CAS  Google Scholar 

  • Swofford DL, Selander R (1999) BIOSYS-2: A Computer Program for the Analysis of Allelic Variation in Population Genetics and Biochemical Systematics (Release 2.0). University of Illinois, Urbana, Champaign, IL

    Google Scholar 

  • Taberlet P (1996) The use of mitochondrial DNA control region sequencing in conservation genetics. In: Smith TB, Wayne RK (eds), Molecular Genetic Approaches in Conservation. Oxford University Press, New York, pp. 125–142

    Google Scholar 

  • Thurber JM, Peterson RO (1991) Changes in body size associated with range expansion in the coyote (Canis latrans). J. Mammal. 72, 750–755

    Article  Google Scholar 

  • USFWS (1998) Endangered and Threatened Wildlife and Plants: Establishment of a nonessential experimental population of the Mexican gray wolf in Arizona and New Mexico. Federal Register, 63, 1752–1772

    Google Scholar 

  • Vilà C (1993) Aspectos morfológicos y ecológicos del lobo ibérico Canis lupus. L. PhD Thesis, Universidad de Barcelona

  • Vilà C, Savolainen P, Maldonado JE, et al. (1997) Multiple and ancient origins of the domestic dog. Science 276, 1687–1689

    Article  PubMed  Google Scholar 

  • Vilà C, Wayne RK (1999) Hybridization between wolves and dogs. Conserv. Biol. 13, 195–198

    Article  Google Scholar 

  • Vilà C, Amorin IR, Leonard JA, Posada D, Castroviejo SJ, Petrucci-Fonseca F, Crandall A, Ellegren SH, Wayne RK (1999) Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus. Mol. Ecol. 8, 2089–2103

    Article  PubMed  Google Scholar 

  • Vilà C, Walker C, Sundqvist AK, et al. (2003) Combined use of maternal, paternal and bi-parental genetic markers for the identification of wolf–dog hybrids. Heredity 90, 17–24

    Article  PubMed  CAS  Google Scholar 

  • Wayne RK, Jenks SM (1991) Mitochondrial-DNA analysis implying extensive hybridization of the endangered red wolf Canis-Rufus. Nature 351, 565–568

    Article  CAS  Google Scholar 

  • Wayne RK, Brown DM (2001) Hybridization and conservation of carnivores. In: Gittleman JL, Funk SM, Macdonald D, Wayne RK, Carnivore Conservation. Cambridge University Press, Cambridge

    Google Scholar 

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

    Article  Google Scholar 

  • Wyner YM, Amato G, Desalle R (1999) Captive breeding, reintroduction, and the conservation genetics of black and white ruffed lemurs, Varecia variegata variegata. Mol. Ecol. 8, S107-S115

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This study would not have been possible without the help of the institutions who collected and provided wolf and dog samples: Zoo Aquarium de la casa de Campo, Parc Zoològic de Barcelona, Parque Ecológico Bizcaia, Jardim Zoológico de Lisboa, Parque Zoológico de Jerez, Zoológico Municipal de Guadalajara, Zoológico de Santillana del Mar, Safari Park Vergel, and Servei Veterinari de Genètica Molecular (UAB). This work was supported by grant BMC2002-01708 from the Dirección General de Investigación, Ministerio de Ciencia y Tecnología (Spain).

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Authors and Affiliations

  1. Departament de Ciència Animal i dels Aliments, Universitat Autònoma de Barcelona, Barcelona, Spain

    Oscar Ramirez, Laura Altet & Armand Sanchez

  2. Parc Zoològic de Barcelona, Barcelona, Spain

    Conrad Enseñat

  3. Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden

    Carles Vilà

  4. Departament de Genètica i Microbiologia, Facultat de Ciències – Edifici C, Universitat Autònoma de Barcelona, 08193, Bellaterra, Barcelona, Spain

    Alfredo Ruiz

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  1. Oscar Ramirez
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Correspondence to Alfredo Ruiz.

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Ramirez, O., Altet, L., Enseñat, C. et al. Genetic assessment of the Iberian wolf Canis lupus signatus captive breeding program. Conserv Genet 7, 861–878 (2006). https://doi.org/10.1007/s10592-006-9123-z

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