Skip to main content

Advertisement

Log in

Genetic diversity of the great bustard in Iberia and Morocco: risks from current population fragmentation

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

We studied the genetic diversity of great bustards (Otis tarda) in Iberia and Morocco, the main stronghold of this globally endangered species. Samples were collected from 327 individuals covering most of the distribution range within the study area. Sequence variation in a 657 bp fragment of the mtDNA control region revealed 20 variable sites defining 22 haplotypes, two of them exclusive to Morocco. Genetic diversity showed marked regional differences (π = 0–0.53, h = 0–0.89). Multidimensional scaling analysis based on F ST values showed a clear division between Morocco and the Iberian Peninsula, with no evidence of current gene flow between them. Our results suggest that Morocco, where few matrilines have persisted to present, was colonized from Iberia thousands of years ago. Last century reports suggest dispersal through Gibraltar, when the species was more abundant at both sides of the Strait but later population declines and the Strait’s barrier effect have favoured current genetic isolation. Within Iberia, only the most peripheral populations (Navarra, Aragón and Andalusia) differed significantly from the main ones in central Spain. The first two showed extremely low genetic diversity and are probably threatened by inbreeding depression. Diversity was higher in Andalusia, where three exclusive haplotypes were found, suggesting some degree of isolation from other populations. Andalusia and Morocco could be regarded as separate management units which hold a significant proportion of the current genetic diversity and thus deserve urgent conservation measures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allard MW, Miyamoto MM, Bjorndal KA, Bolten AB, Bowen BW (1994) Support for natal homing in green turtles from mitochondrial DNA sequences. Copeia 1994:34–41

    Article  Google Scholar 

  • Alonso JC (coord) (2007) La Avutarda Común en Andalucía. Gypaetus-Junta de Andalucía, Sevilla

  • Alonso JC, Martín E, Alonso JA, Morales MB (1998) Proximate and ultimate causes of natal dispersal in the great bustard Otis tarda. Behav Ecol 3:243–252

    Article  Google Scholar 

  • Alonso JC, Morales MB, Alonso JA (2000) Partial migration, and lek and nesting area fidelity in female great bustards. The Condor 102:127–136

    Article  Google Scholar 

  • Alonso JA, Martín CA, Alonso JC, Morales MB, Lane SJ (2001) Seasonal movements of male great bustards (Otis tarda) in central Spain. J Field Ornithol 72(4):504–508

    Google Scholar 

  • Alonso JC, Palacín C, Martín CA (2003) Status and recent trends of the great bustard (Otis tarda) population in the Iberian Peninsula. Biol Conserv 110:185–195

    Article  Google Scholar 

  • Alonso JC, Martín CA, Alonso JA, Palacín C, Magaña M, Lane SJ (2004) Distribution dynamics of a great bustard metapopulation throughout a decade: influence of conspecific attraction and recruitment. Biod Conserv 13:1659–1674

    Article  Google Scholar 

  • Alonso JC, Palacín C, Martín CA, Mouati M, Arhzaf ZL, Azizi D (2005a) The Great Bustard Otis tarda in Morocco: a re-evaluation of its status based on recent survey results. Ardeola 53:79–90

    Google Scholar 

  • Alonso JC, Martín CA, Palacín C, Martín B, Magaña M (2005b) The Great Bustard Otis tarda in Andalusia, southern Spain: status, distribution and trends. Ardeola 53:67–78

    Google Scholar 

  • Avise JC (1994) Molecular markers, natural histroy and evolution. Chapman & Hall, New York

    Google Scholar 

  • Avise JC (1996) Three fundamental contributions of molecular genetics to avian ecology and evolution. Ibis 138:16–25

    Google Scholar 

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Ann Rev Ecol Syst 18:489–522

    Google Scholar 

  • Bandelt H, Forster P, Rohl A (1999) Median joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    PubMed  CAS  Google Scholar 

  • BirdLife International (2000) Threatened birds of the world. Lynx Edicions & BirdLife International, Barcelona & Cambridge

    Google Scholar 

  • BirdLife International (2001) Threatened birds of Asia. The BirdLife International Red Data Book. BirdLife International, Cambridge

    Google Scholar 

  • BirdLife International (2007) Species factsheet: Otis tarda. http://www.birdlife.org Accessed 30 May 2007

  • Broderick D, Idaghdour Y, Korrida A, Hellmich J (2003) Gene flow in great bustard populations across the Strait of Gibraltar as elucidated from excremental PCR and mtDNA sequencing. Conserv Genet 4:93–800

    Article  Google Scholar 

  • Brown WM, Wilson MG, Wallace AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971

    Article  PubMed  CAS  Google Scholar 

  • Cavalcanti MJ (1999) Mantel for windows, Version 1.00 Rio de Janeiro Brasil

  • Chapman A, Buck WJ (1893) Wild Spain. Gurney & Jackson, London

    Google Scholar 

  • Collar NJ, Crosby MJ, Stattersfield AJ (1994) Birds to watch 2: the world list of threatened birds, vol 4. BirdLife Conservation, Cambridge

    Google Scholar 

  • Danchin E, Wagner R (1997) The evolution of coloniality: the emergence of new perspectives. TREE 12:342–347

    Google Scholar 

  • Del Hoyo J, Elliot A, Sargatal J (1996) Handbook of the birds of the world, vol 3. Lynx, Barcelona

    Google Scholar 

  • Edwards SV (1993) Mitochondrial gene genealogy and gene flow among island and mainland populations of a sedentary songbird, the gray-crowned babbler (Pomatostomus temporalis). Evolution 47(4):1118–1137

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Frankham R (1995) Inbreeding and conservation: a threshold effect. Conserv Biol 9:792–799

    Article  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Glutz UN, Bauer KM, Bezzel E (1973) Handbuch der Vögel Mitteleuropas, vol 5. Akademische Verlagsgesellschaft, Frankfurt a M

    Google Scholar 

  • Haig SM (1998) Molecular contributions to conservation. Ecology 79(2):413–425

    Article  Google Scholar 

  • Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biol 66:591–600

    PubMed  CAS  Google Scholar 

  • Hartert E, Jourdain FCR (1923) The hitherto known birds of Morocco. Novitates Zoologicae 30:91–146

    Google Scholar 

  • Hellmich J, Idaghdour Y (2002) The Great Bustard Otis tarda population in Morocco 1998–2001. Bird Conserv Int 12:19–23

    Article  Google Scholar 

  • Hewitt GM (2001) Speciation, hybrid zones and phylogeography––or seeing genes in space and time. Mol Ecol 10:537–550

    Article  PubMed  CAS  Google Scholar 

  • Hood GM (2005) PopTools version 2.6.6. Available at http://www.cse.csiro.au/poptools

  • Idaghdour Y, Broderick D, Korrida A (2003) Faeces as a source of DNA for molecular studies in a threatened population of great bustards. Conserv Genet 4(6):789–792

    Article  CAS  Google Scholar 

  • Irby LH (1895) The ornithology of the Strait of Gibraltar. R. H. Porter, London

    Google Scholar 

  • Junta de Andalucía (2001) Libro Rojo de los Vertebrados Amenazados de Andalucía. Consejería de Medio Ambiente, Junta de Andalucía, Sevilla

    Google Scholar 

  • Knapen D, Knaepkens G, Bervoets L, Taylor MI, Eens M, Verheyen E (2003) Conservation units based on mitochondrial and nuclear DNA variation among European bullhead populations (Cottus gobio L., 1758) from Flanders, Belgium. Conserv Genet 4(2):129–140

    Article  CAS  Google Scholar 

  • Lahanas PN, Miyamoto MM, Bjorndal KA, Bolten AB (1994) Molecular evolution and population genetics of Greater Caribbean green turtles (Chelonia mydas) as inferred from mitochondrial DNA control region sequences. Genetica 94:57–67

    Article  PubMed  CAS  Google Scholar 

  • Magaña M (2007) Compotamiento reproductivo de la Avutarda Común. PhD thesis. Universidad Complutense, Madrid

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

    PubMed  CAS  Google Scholar 

  • Marshall HD, Baker AJ (1997) Structural conservation and variation in the mitochondrial control region of fringilline finches (Fringilla spp) and the greenfinch (Carduelis chloris). Mol Biol Evol 14:173–184

    PubMed  CAS  Google Scholar 

  • Martín CA (2001) Dispersión y estructura genética de la población de avutardas de la Comunidad de Madrid. PhD thesis. Universidad Autónoma, Madrid

  • Martín E (1997) Dispersión juvenil y cuidado maternal en la avutarda (Otis tarda). PhD thesis. Universidad Autónoma, Madrid

  • Martín CA, Alonso JC, Alonso J, Pitra C, Lieckfeldt D (2002) Great bustard population structure in central Spain: concordant results from genetic analysis and dispersal study. Proc R Soc Lond Ser B-Biol Sci 269:119–125

    Article  Google Scholar 

  • Martín CA, Alonso JC, Alonso J, Palacín C, Magaña M, Martín B (2008) Natal dispersal in great bustards: the effect of sex, local population size and spatial isolation. J Anim Ecol 77:326–334

    Article  PubMed  Google Scholar 

  • Milot E, Gibbs HL, Hobson KA (2000) Phylogeography and genetic structure of northern populations of the yellow warbler (Dendroica petechia). Mol Ecol 9:667–681

    Article  PubMed  CAS  Google Scholar 

  • Morales MB, Alonso JC, Alonso JA, Martin E (2000) Migration patterns in male great bustards. The Auk 117:493–498

    Article  Google Scholar 

  • Moritz C (1994) Applications of mitochondrial DNA analysis in conservation: a critical review. Mol Ecol 3:401–411

    Article  CAS  Google Scholar 

  • Moritz C, Dowling TE, Brown M (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Ann Rev Ecol Syst 18:269–292

    Article  Google Scholar 

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

    Google Scholar 

  • Nielsen R (2002) MDIV software Available at http://www.biom.cornell.edu/Homepages/Rasmus_Nielsen/files.html

  • Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896

    PubMed  CAS  Google Scholar 

  • O’Corry-Crowe GM, Suydam RS, Rosenberg A, Frost KJ, Dizon AE (1997) Phylogeography, population structure and dispersal patterns of the beluga whale Delphinapterus leucasin in the western Nearctic revealed by mitochondrial DNA. Mol Ecol 6:955–970

    Article  CAS  Google Scholar 

  • Palacín C (2007) Comportamiento migratorio de la Avutarda Común en la Península Ibérica. PhD thesis. Universidad Complutense, Madrid

  • Palacín C, Alonso JC, Martín CA, Alonso J, Martín B, Magaña M (2007) Comportamiento migratorio de los machos. In: Alonso JC (coord) La Avutarda Común en Andalucía. Gypaetus-Junta de Andalucía, Jaén, pp 145–156

  • Park SD (2001) Trypanotolerance in West African Cattle and the Population Genetic Effects of Selection. PhD thesis. Universtiy of Dublin. Availbale at http://www.animalgenomics.ucd.ie/sdepark/ms-toolkit/

  • Pitra C, Lieckfeldt D, Alonso JC (2000) Population subdivision in Europe’s great bustard inferred from mitochondrial and nuclear DNA sequence variation. Mol Ecol 9:1165–1170

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) genepop (Version 1.2): population genetics software for exact test and ecumenicism. J Heredity 86:248–249

    Google Scholar 

  • Reed MJ, Dobson AP (1993) Behavioural constraints and conservation biology: conspecific attraction and recruitment. TREE 8:253–256

    Google Scholar 

  • Riddle BR (1996) The molecular phylogeographic bridge between deep and shallow history in continental biotas. TREE 11(5):207–211

    Google Scholar 

  • Rozas J, Rozas R (1999) DNASP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Saunders H (1871) A list of the birds of Southern Spain. Ibis 1:54–68, 205–225, 384–402

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin, a software program for population genetics data analysis, Version 2.000. Genetics and Biometry Laboratory, Department of Anthropology, University of Geneva, Switzerland

    Google Scholar 

  • SEO/BirdLife (2001) Programa Migres. Seguimiento de la Migración en el Estrecho. Informe 2000. Unpublished report. SEO/BirdLife—Consejería de Medio Ambiente, Junta de Andalucía, Sevilla

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90

    Article  CAS  Google Scholar 

  • Sgariglia EA, Burns KJ (2003) Phylogeography of the California thrasher (Toxostoma redivivum) based on Nested Clade Analysis of mitochondrial DNA variation. Auk 120:346–361

    Article  Google Scholar 

  • Shepherd TM, Burns KJ (2007) Intraspecific genetic analysis of the summer tanager Piranga rubra: implications for species limits and conservation. J Avian Biol 38:13–27

    Article  Google Scholar 

  • Slatkin M (1985) Gene flow in natural-populations. Ann Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • Slatkin M (1991) Inbreeding coefficients and coalescence times. Genet Res Camb 58:167–175

    Article  CAS  Google Scholar 

  • Smith AT, Peacock MM (1990) Conspecific attraction and the determination of metapopulation colonization rates. Conserv Biol 4:320–323

    Article  Google Scholar 

  • Sork VL, Nason J, Campbell DR, Fernández JF (2001) Landscape approaches to historical and contemporary gene flow in plants. TREE 14:219–224

    Google Scholar 

  • Stamps JA (1988) Conspecific attraction and aggregation in territorial species. Am Nat 131:329–347

    Article  Google Scholar 

  • Stanley HF, Casey S, Carnahan JM, Goodman S, Harwood J, Wayne RK (1992) Worldwide patterns of mitochondrial DNA differentiation in the harbour seal (Phoca vitulina). Mol Biol Evol 13:368–382

    Google Scholar 

  • StatSoft (2001) STATISTICA (data analysis software system), version 6. Tulsa, USA. www.statsoft.com

  • Stoneking M, Hedgecock D, Higuchi RG, Vigilant L, Erlich HA (1991) Population variation of human mtDNA control region sequences detected by enzymatic amplification and sequence-specific oligonucleotide probes. Am J Human Genet 48:370–382

    CAS  Google Scholar 

  • Suárez-Seoane S, Osborne PE, Alonso JC (2002) Large-scale habitat selection by agricultural steppe birds in Spain: identifying species–habitat responses using generalized additive models. J Appl Ecol 39:755–771

    Article  Google Scholar 

  • Taberlet P (1991) A single plucked feather as a source of DNA for bird genetics. Auk 108:959–960

    Google Scholar 

  • Taberlet P, Fumagalli LW, St-Saucy AG, Cosson J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

    Article  PubMed  CAS  Google Scholar 

  • Trigo de Yarto E (1971) La avutarda en España. XVIII Triennial General Meeting of the International Council for Hunting. Unpublished report. Federación Española de Caza, Madrid

  • Urban EK, Fry CH, Keith S (1986) The birds of Africa. Academic Press, London

    Google Scholar 

  • Wenink PW, Baker AJ, Tilanus MGJ (1993) Hypervariable-control-region sequences reveal global population structuring in a long-distance migrant shorebird, the dunlin (Calidris alpina). Proc Natl Acad Sci USA 90(1):94–98

    Article  PubMed  CAS  Google Scholar 

  • Wenink PW, Baker AJ, Tilanus MGJ (1994) Mitochondrial control-region sequences in two shorebird species, the turnstone and the dunlin, and their utility in population genetic studies. Mol Biol Evol 11(1):22–31

    PubMed  CAS  Google Scholar 

  • Wilson AC, Cann RL, Carr SM et al (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linn Soc 26:375–400

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    PubMed  CAS  Google Scholar 

  • Zink RM, Blackwell RC (1998) Molecular systematics and biogeography of aridland gnatcatchers (genus Polioptila) and evidence supporting species status of the California gnatcatcher (Polioptila californica). Mol Phyl Evol 9:26–32

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgements

We thank Anke Schmidt for technical assistance. We also thank Beatriz Martín, Manuel Morales, Enrique Martín, Alejandro Onrubia, José A. Cruz and Diego González for their help during fieldwork. The study was financed by the Dirección General de Investigación (projects PB91-0081, PB94-0068, PB97-1252 and BOS2002-01543), and Agencia Española de Cooperación Internacional of the Spanish Ministry of Foreign Affairs (project 2000MA1000 in Morocco), with contributions from the Instituto Nacional para la Conservación de la Naturaleza, Dirección General del Medio Natural of Madrid Community, the Junta de Andalucía, and the Junta de Castilla y León. The Consejerías de Medio Ambiente of Madrid Community, Junta de Andalucía, Junta de Castilla y León and Navarra allowed us to capture the birds.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan C. Alonso.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alonso, J.C., Martín, C.A., Alonso, J.A. et al. Genetic diversity of the great bustard in Iberia and Morocco: risks from current population fragmentation. Conserv Genet 10, 379–390 (2009). https://doi.org/10.1007/s10592-008-9605-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-008-9605-2

Keywords

Navigation