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Pronounced genetic structure and low genetic diversity in European red-billed chough (Pyrrhocorax pyrrhocorax) populations

An Erratum to this article was published on 05 December 2014

Abstract

The red-billed chough (Pyrrhocorax pyrrhocorax) is of conservation concern in the British Isles and continental Europe, with historically declining populations and a highly fragmented distribution. We quantified the distribution of genetic variation within and among European populations to identify isolated populations that may need to be managed as demographically independent units, and assess whether individual populations are denuded of genetic diversity and so may show reduced viability. We genotyped 326 choughs from ten wild populations and 22 from one captive population at 16 nuclear microsatellite loci, and sequenced 34 individuals across three mitochondrial regions to quantify genetic structure, diversity and phylogeography. Microsatellite diversity was low (often <4 alleles per locus), but pairwise population differentiation was high (often D est  > 0.1), with a signature of isolation-by-distance. Bayesian-inferred a posteriori genetic clusters coincided with a priori populations, supporting strong genetic structure. Microsatellites also allowed us to identify the probable origin of the captive choughs and one recently founded wild population. Mitochondrial DNA sequence diversity was low (π = 0.00103). Phylogeographic structure was consequently poorly resolved, but indicated that sampled continental-European populations are ancestral to British Isles populations, which comprised a single clade. Our data suggest that British Isles chough populations are relatively isolated with infrequent gene flow and relatively genetically depauperate, potentially requiring genetic management. These findings should be integrated into conservation management policy to ensure long-term viability of chough populations.

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Acknowledgments

We are extremely grateful to everyone who contributed samples, most particularly Caitlin, Eric and Sue Bignal, Maria Bogdanova, Rob Colley, Tony Cross and Adrienne Stratford (Cross & Stratford Welsh Chough Project), Anne Delestrade, Annie and Bob Haycock, Jane Hodges, David Jardine, Ian Johnstone, Davy McCracken, Allen Moore, Greg Morgan, Claire Mucklow, Mike Peacock, Tom Pennycott, Chris Sharpe, Vic Simpson, Mike Trewby, Gareth Watkins and David Woolcock. We acknowledge the work of DNA Sequencing & Services (MRCPPU, College of Life Sciences, University of Dundee, Scotland, http://www.dnaseq.co.uk), Eurofins MWG GmbH, Ebersberg, Germany and Beckman Coulter Genomics, Takeley, UK. We thank two anonymous reviewers for helpful comments on this manuscript.

This study was funded by the Royal Society (JMR), the Philip Leverhulme Prize (JMR), the University of Aberdeen (MAW) and the Nuffield Foundation Undergraduate Research Bursary (MAW). SBP and JMR are joint last authors of this article.

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Correspondence to Jane M. Reid.

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Stuart B. Piertney and Jane M. Reid are joint last authors.

An erratum to this article is available at http://dx.doi.org/10.1007/s10592-014-0681-1.

Appendix

Appendix

See Tables 5, 6 and 7.

Table 5 Characterisation of three primer pairs to amplify mitochondrial DNA regions in red-billed chough
Table 6 Characterisation of 16 microsatellite loci for red-billed chough
Table 7 Likelihood statistics of Bayesian inference of genetic clusters in structure

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Wenzel, M.A., Webster, L.M.I., Blanco, G. et al. Pronounced genetic structure and low genetic diversity in European red-billed chough (Pyrrhocorax pyrrhocorax) populations. Conserv Genet 13, 1213–1230 (2012). https://doi.org/10.1007/s10592-012-0366-6

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Keywords

  • Connectivity
  • Genetic structure
  • Genetic diversity
  • Microsatellite
  • Mitochondrial DNA
  • Recolonisation
  • Red-billed chough