Skip to main content

Advertisement

SpringerLink
Log in

Genetic structure reveals management units for the yellow cardinal (Gubernatrix cristata), endangered by habitat loss and illegal trapping

Conservation Genetics Aims and scope Submit manuscript

Abstract

The yellow cardinal, Gubernatrix cristata, is an endangered passerine from southern South America. Populations are declining due to the loss of their natural habitat, which has caused a fragmented distribution, and the continuous extraction of individuals from the wild, mainly males, to sell them as cage birds. In this study, we assess the genetic variability of remaining yellow cardinal’s populations and determine whether these populations represent independent management units. We found that the degree of geographic isolation of the remaining populations parallels the genetic differentiation of these populations for both mitochondrial and nuclear markers, and supports the delimitation of four management units for the yellow cardinal (three in Argentina and one in Uruguay). Assignment tests showed that geographic genetic differentiation can be used to assign seized individuals from illegal pet trade to their original populations and thus manage their release.

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

Access this article

Log in via an institution

Price includes VAT (Finland)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • Allendorf FW, Luikart G (2007) Small populations and genetic drift. In: Allendorf FW, Luikart G (eds) Conservation and the genetics of populations. Blackwell Publishing, Malden, pp 117–147

    Google Scholar 

  • Azpiroz AB, Alfaro M, Jiménez S (2012) Lista Roja de las Aves del Uruguay. Dirección Nacional de Medio Ambiente, Montevideo

    Google Scholar 

  • Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744

    Article  PubMed  Google Scholar 

  • Barker K, Burns K, Klicka K, Lanyon S, Lovette I (2013) Going to extremes: contrasting rates of diversification in a recent radiation of New World Passerines Birds. Syst Biol 62:298–320

    Article  PubMed  Google Scholar 

  • BirdLife International (2016) Species factsheet: Gubernatrix cristata. http://www.birdlife.org. Accessed 23 February 2016.

  • Burns KJ, Shultz AJ, Title PO, Mason NA, Barker FK, Klicka J, Scott L, Lovette IJ (2014) Phylogenetics and diversification of tanagers (Passeriformes: Thraupidae), the largest radiation of Neotropical songbirds. Mol Phylogenet Evol 75:41–77

    Article  PubMed  Google Scholar 

  • Campagna L, Geale K, Handford P, Lijtmaer DA, Tubaro PL, Lougheed SC (2011) A molecular phylogeny of the Sierra-Finches (Phrygilus, Passeriformes): extreme polyphyly in a group of Andean specialists. Mol Phylogenet Evol 61:521–533

    Article  PubMed  Google Scholar 

  • Campagna L, Kopuchian C, Tubaro PL, Lougheed SC (2014) Secondary contact followed by gene flow between divergent mitochondrial lineages of a widespread Neotropical songbird (Zonotrichia capensis). Biol J Linn Soc 111:863–868

    Article  Google Scholar 

  • Dobson AP (1996) Conservation and biodiversity. Scientific American Library, New York

    Google Scholar 

  • Earl DA, von Holdt BM (2012) Structure harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–366

    Article  Google Scholar 

  • Estoup A, Jarne P, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604

    Article  CAS  PubMed  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

    Article  CAS  PubMed  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 Resour 10:564–567

    Article  PubMed  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 data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Faria P, Guedes N, Yamashita C, Martuscelli P, Miyaki C (2008) Genetic variation and population structure of the endangered Hyacinth Macaw (Anodorhynchus hyacinthinus): implications for conservation. Biodivers Conserv 17:765–779

    Article  Google Scholar 

  • Fernandes GA, Caparroz R (2013) DNA sequence analysis to guide the release of blue and yellow macaws (Ara ararauna, Psittaciformes, Aves) from the illegal trade back to the wild. Mol Biol Rep 40:2757–2762

    Article  CAS  PubMed  Google Scholar 

  • Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143:1919–1927

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Goudet J (2002) Fstat 2.9.3.2. http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 14 October 2015.

  • Grant WS, Bowen BM (1998) Shallow population histories in deep evolutionary lineages of marine fishes, insights from the sardines and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Haig SM, Bronaugh WM, Crowhurst R, D’Elia J, Eagles-Smith CA, Epps C, Knaus B, Miller MP, Moses ML, Oyler-McCance S, Robinson WD, Sidlauskas B (2011) Genetic applications in avian conservation. Auk 128:205–229

    Article  Google Scholar 

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

    Google Scholar 

  • Hedrick P, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Evol Syst 31:139–162

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) Dna SP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  CAS  PubMed  Google Scholar 

  • Martins-Ferreira C, Haddrath O, Baker AJ, Freitas TRO (2010) Isolation and characterization of 10 microsatellite loci in the Yellow Cardinal Gubernatrix cristata. Mol Ecol Resour 10:751–754

    PubMed  Google Scholar 

  • Martins-Ferreira C, Repenning M, Vargas Damiani R (2013) Gubernatrix cristata. In: Serafini PP (ed) Plano de Ação Nacional para a Conservação dos Passeriformes Ameaçados dos Campos Sulinos e Espinilho. Série Espécies Ameaçadas, Brasília, pp 116–119.

    Google Scholar 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mayr E (1963) Animal species and ecolution. Harvard University Press, Massachusetts

    Book  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Neel MC, Leidner AK, Haines A, Goble DD, Scott JM (2012) By the numbers: how is recovery defined by the US Endangered Species Act? Bioscience 62:646–657

    Article  Google Scholar 

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

    Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  PubMed  Google Scholar 

  • Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–298

    Article  Google Scholar 

  • Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Bëer E, Robinson S, Vásquez-Carrillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

    Article  PubMed  Google Scholar 

  • Pereira M, Leadley PW, Proenca V, Alkemade R, Scharlemann JPW, Fernandez-Manjarres JF, Araujo MB, Balvanera P, Biggs R, Cheung WWL, Chini L, Cooper HD, Gilman EL, Guenette S, Hurtt GC, Huntington HP, Mace GM, Oberdorff T, Revenga C, Rodrigues P, Scholes RJ, Sumaila UR, Walpole M (2010) Scenarios for global biodiversity in the 21st century. Science 330:1496–1501

    Article  CAS  PubMed  Google Scholar 

  • Pessino M, Tittarelli RF (2006) The Yellow Cardinal (Gubernatrix cristata): a diagnosis of its situation in the province of La Pampa, Argentina. Gest Ambient 12:69–76

    Google Scholar 

  • Piry S, Luikart G, Cornuet J (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Porras-Hurtado L, Ruiz Y, Santos C, Phillips C, Carracedo Á, Lareu M (2013) An overview of STRUCTURE: applications, parameter settings and supporting software. Front Genet 4:1–13

    Article  CAS  Google Scholar 

  • Presti FT, Guedes NM, Antas PT, Miyaki CY (2015) Population Genetic Structure in Hyacinth Macaws (Anodorhynchus hyacinthinus) and Identification of the Probable Origin of Confiscated Individuals. J Hered 106:491–502

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rands W, Adams WM, Bennun L, Butchart HM, Clements A, Coomes D, Entwistle A, Hodge I, Kapos V, Scharlemann JPW, Sutherland WJ, Vira B (2010) Biodiversity conservation: challenges beyond 2010. Science 329:1298–1303

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evol Int J org Evol 43:223–225

    Article  Google Scholar 

  • Ridgely RS, Tudor G (2009) Field guide to the songbirds of South America: the Passerines. University of Texas Press, Austin

    Google Scholar 

  • Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Ryan SJ (2006) The role of culture in conservation planning for small or endangered populations. Conserv Biol 20:1321–1324

    Article  CAS  PubMed  Google Scholar 

  • Sambatti JBM, Stahl E, Harrison S (2008) Metapopulation structure and the conservation consequences of population fragmentation. In: Carroll SP, Fox CW (eds) Conservation biology: evolution in action. Oxford University Press, Oxford, pp 50–55

    Google Scholar 

  • Schwartz TS, Karl SA (2008) Population genetic assignment of confiscated gopher tortoises. J Wildl Manage 72:254–259

    Article  Google Scholar 

  • Short LL (1975) A zoogeographic analysis of the South American chaco avifauna. B Am Mus Nat Hist 154:163–352

    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  CAS  PubMed  PubMed Central  Google Scholar 

  • Tarr CL (1995) Primers for amplification and determination of mitochondrialn control-region sequences in oscine passerines. Mol Ecol 4:527–529

    Article  CAS  PubMed  Google Scholar 

  • Waples RS (1991) Genetic methods for estimating the effective size of Cetacean populations. Report International Whaling Commission, Special Issue 13:279–300.

  • Wayne RK, Morin PA (2004) Conservation genetics in the new molecular age. Front Ecol Environ 2:89–97

    Article  Google Scholar 

  • Wiemann A, Andersen LW, Berggren P, Siebert U, Benke H, Teilmann J, Lockyer C, Pawliczka I, Skóra K, Roos A, Lyrholm T, Paulus KB, Ketmaier V, Tiedemann R (2010) Mitochondrial Control Region and microsatellite analyses on Harbour porpoise (Phocoena phocoena) unravel population differentiation in the Baltic Sea and adjacent waters. Conserv Genet 11:195–211

    Article  Google Scholar 

Download references

Acknowledgements

We are very grateful to K. Havenstein, A. Schneider and U. Matthes for technical support and to Conservation Land Trust, Carlos Figuerero, Matias Ayarragaray, and Oscar Blumetto for facilitating access to study sites and samples. We also thank two anonymous reviewers and V. Ferretti for comments on a previous version of the manuscript. Field assistants Martin Hoffman, Alejandro Cinalli and Sergio Briones helped with data collection. DAAD and MINCYT made the international collaboration possible. Funding was provided by CONICET, UBA and Aves Argentinas/AOP.

Author information

Authors and Affiliations

  1. Laboratorio de Ecología y Comportamiento Animal, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Instituto IEGEBA, Universidad de Buenos Aires, Pabellón II, Ciudad Universitaria, C1428EHA, Buenos Aires, Argentina

    Marisol Domínguez, Juan C. Reboreda & Bettina Mahler

  2. Unit of Evolutionary Biology/Systematic Zoology, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, Haus 26, 14476, Potsdam, Germany

    Ralph Tiedemann

  3. Sección Ornitología, División Zoología Vertebrados, Museo de La Plata, Universidad Nacional de La Plata, Paseo del Bosque S/N, La Plata, B1904CCA, Buenos Aires, Argentina

    Luciano Segura

  4. Facultad de Ciencias Exactas y Naturales, Universidad Nacional de La Pampa, Uruguay 151, L6300, La Pampa, Argentina

    Fabián Tittarelli

Authors
  1. Marisol Domínguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ralph Tiedemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juan C. Reboreda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luciano Segura
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fabián Tittarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bettina Mahler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marisol Domínguez.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Domínguez, M., Tiedemann, R., Reboreda, J.C. et al. Genetic structure reveals management units for the yellow cardinal (Gubernatrix cristata), endangered by habitat loss and illegal trapping. Conserv Genet 18, 1131–1140 (2017). https://doi.org/10.1007/s10592-017-0964-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-017-0964-4

Keywords

Search

Navigation