Abstract
The mallard (Anas platyrhynchos L.), the most abundant waterfowl species, is an important migratory component of the Holartic fauna. In Europe, massive numbers of farm-reared mallards of unknown genetic origin are released into the wild for hunting and in urban areas for ornamental purposes. Human manipulations have caused shifts in range, influenced migration propensity, led to behavioural modifications and altered the genetics of this duck species. With the aim to contribute to knowledge on the genetic consequences of large-scale game releases of mallards in southern Europe, we analysed the relationship among 245 individuals (wild and captive-bred) from eight localities in central and northern Italian regions and four from North America, by using nine microsatellite loci. In most Italian sites, a large admixture of mallard strains were observed, whereas significant genetic differentiation levels were found between urban and wild populations and among the wild population from North America and all European populations.
Similar content being viewed by others
References
Allendorf J (2009) Human-induced evolution caused by unnatural selection through harvest of wild animals. Proc Natl Acad Sci U S A 106:9987–9994
Arcamone E, Dall’Antonia P, Puglisi L (2007) Lo svernamento degli uccelli acquatici in Toscana—1984–2006. Regione Toscana Edizioni
Baccetti N, Dall’Antonia P, Magagnoli P, Melega L, Serra L, Soldatini C, Zenatello M (2002) Risultati dei censimenti degli uccelli acquatici svernanti in Italia. Biol Conservazione Fauna 111:234
Baratti M, Cordaro M, Dessi’-Fulgheri F, Vannini M, Fratini S (2009) Molecular and ecological characterization of urban population of the mallard (Anas platyrhynchos L.) in Italy. Ital J Zool 1:1–10
Belkhir K, Borsa P, Chikhi L, Raufauste N, Bonhomme F (2001) GENETIX 4.02, logiciel sous Windows TM pour la génétique des populations Laboratoire Génome, Populations, Interections CNRS UMR 5000, Universitè de Montpellier II, Montpellier (France). Available at http://www.univ-montp2.fr/genetix/genetix/genetix.html.
Brichetti P, Fracasso G (2003) Ornitologia Italiana. Vol. 1 Gaviidae, Falconidae. Alberto Perdisa Editore, Bologna
Champagnon J, Guillemain M, Elmberg J, Folkesson KE, Gauthier-Clerc M (2010) Changes in Mallard Anas platyrhynchos bill morphology after 30 years of supplemental stocking. Bird Study 57:1–8
Champagnon J, Elmberg J, Guillemain M, Massez G, Cavallo F, Gauthier-Clerc J (2012a) Low survival after release into the wild: assessing “the burden of captivity” on Mallard physiology and behaviour. Eur J Wildl Res 58:255–267
Champagnon J, Guillemain M, Gauthier-Clerc M, Lebreton JD (2012b) Conspecifics can be aliens too: a review of effects of restocking practices in vertebrates. J Nat Conserv 20:231–241
Champagnon J, Crochet PA, Kreisinger J, Čìžková D, Gauthier-Clerc M, Massez G, Söderquist P, Albrecht T, Guillemain M (2013) Assessing the genetic impact of massive restocking on wild mallard. Anim Conserv 16:295–305
Čìžková D, Javurková V, Champagnon J, Kreisinger J (2012) Duck’s not dead: does restocking with captive bred individuals affect the genetic integrity of wild mallard (Anas platyrhynchos) population? Biol Conserv 152:231–240
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottleneck from alleles frequency data. Genetics 144:2001–2014
Cornuet JM, Luikart G, Piry S, Estoup A, Solignac M (1999) New methods employing Multilocus genotypes to select or exclude populations for origin of individuals. Genetics 153:1989–2000
Crooijmans RPMA, Van Oers PAM, Strijk JA, Van Der Poel JJ, Groenen MAM (1996) Preliminary linkage map of the chicken (Gallus domesticus) genome based on microsatellite markers. Poult Sci 75:746–754
Dalby L, Söderquist P, Christensen TK, Clausen P, Einarsson A, Elmberg J, Fox AD, Holmqvist N, Langendoen T, Lehikoinen A, Lindström A, Lorentsen S, Nilsson L, Pöysä H, Rintala J, Sigfússon A, Svenning JC (2013) The status of the Nordic populations of the Mallard (Anas platyrhynchos) in a changing world. Ornis Fenn 90:2–15
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Cons Genet Resour 4:359–361
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
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
Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Fowler AC, Eadie JM, Engilis A (2009) Identification of endangered Hawaiian ducks (Anas wyvilliana), introduced North American mallards (A. platyrhynchos) and their hybrids using multilocus genotypes. Conserv Genet 10:1747–1758
Gotti C (2004) Introgressione di tratti “domestici” in popolazioni naturali di Germano reale (Anas platyrhynchos) del Parco del Delta del Po mediante analisi della variabilità genetica e morfometrica. Phd Dissertation, University of Bologna
Goudet J (2001) FSTAT, a program to estimate and test gene diversites and fixation indices 2.9.3. J Hered 86:485–486
Gunnarsson G, Elmberg J, Waldenström J (2011) Trends in body mass of ducks over time: the hypotheses in Guillemain et. Revisited. Ambio 40:338–340
Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372
He DQ, Zhu Q, Chen SY, Wang HY, Liu YP, Yao YG (2008) A homogenous nature of native Chinese duck matrilineal pool. BMC Evol Biol 8:298
Hou ZC, Yang FX, Qu LJ, Zheng JX, Brun JM, Basso B, Pitel F, Yang N, Xu GY (2012) Genetic structure of Eurasian and North American mallard ducks based on mtDNA data. Anim Genet 43:352–355
Huang YT, Tu J, Cheng X, Tang B, Hu X, Liu Z, Feng J (2005) Characterization of 35 novel microsatellite DNA markers from the duck (Anas platyrhynchos) genome and cross-amplification in other birds. Genet Sel Evol 5:455–472
Huang Y, Li Y, Burt DW, Chen H, Zhang Y, Qian W, Kim H, Gan S, Zhao Y, Li J, Yi K, Feng H, Zhu P, Li B, Liu Q, Fairley S, Magor KE, Du Z, Hu X, Goodman L, Tafer H, Vignal A, Lee T, Kim KW, Sheng Z, An Y, Searle S, Herrero J, Groenen MA, Crooijmans RP, Faraut T, Cai Q, Webster RG, Aldridge JR, Warren WC, Bartschat S, Kehr S, Marz M, Stadler PF, Smith J, Kraus RH, Zhao Y, Ren L, Fei J, Morisson M, Kaiser P, Griffin DK, Rao M, Pitel F, Wang J, Li N (2013) The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nat Genet 45:776–783
Jacobsson 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
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94
Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189
Kraus RH, Zeddeman A, van Hooft P, Sartakov D, Soloviev SA, Ydenberg RC, Prins HH (2011) Evolution and connectivity in the world-wide migration system of the mallard: inferences from mitochondrial DNA. BMC Genet 12:99
Kraus RH, Kerstens HHD, van Hooft P, Megens HJ, Elmberg J, Tsvey AD (2012) Widespread horizontal genomic exchange does not erode species barriers among sympatric ducks. BMC Evol Biol 12:45
Kraus RH, van Hooft P, Megens HJ, Tsvey A, Fokin SY, Ydenberg RC, Prins HH (2013) Global lack of flyway structure in a cosmopolitan bird revealed by a genome wide survey of single nucleotide polymorphisms. Mol Ecol 22:41–55
Kulikova V, Chelomina GN, Zhuravlev YN (2003) Low genetic differentiation of and close evolutionary relationships between Anas platyrhynchos and Anas poecylorhyncha RAPD-PCR evidence. Russ J Genet 38:699–703
Kulikova V, Zhuravlev YN, McCracken KG (2004) Asymmetric hybridization and sex-biased gene flow between eastern spot-billed ducks (Anas zonorhyncha) and mallards (Anas platyrhynchos) in the Russian far east. Auk 121:930–949
Kulikova V, Drovetski DD, Gibson RJ, Harrigan S, Sorenson MD, Winker K (2005) Phylogeography of the mallard (Anas platyrhynchos): hybridization, dispersal and lineage sorting contributes to complex geographic structure. Auk 122:949–965
Kulikova IV, Poysa H, Zhuravlev IN (2012) Phylogeography of the mallard Anas platyrhynchos from Eurasia inferred from sequencing of the mtDNA control region. Genetika 48:835–843
Luikart G, Cornuet JM, Allendorf FW (1998) Temporal changes in allele frequencies provide estimates of population bottleneck size. Conserv Biol 89:238–247
Maak S, Neumann K, Von Lengerken G, Gattermann R (2000) First seven microsatellites developed for the Pecking duck (Anas platyrhynchos). Anim Genet 32:228–241
Maak S, Wimmers K, Weigend S, Neumann K (2003) Isolation and characterization of 18 microsatellites in the Pecking duck (Anas platyrhynchos) and their application in the waterfowl species. Mol Ecol Notes 3:224
Mank JE, Carlson JE, Brittingham MC (2004) A century of hybridization: decreasing genetic distance between American black ducks and mallards. Conserv Genet 5:395–403
McCracken KG, Johnson WP, Sheldon FH (2001) Molecular population genetics, phylogeography, and conservation biology of the mottled duck (Anas fulgivola). Conserv Genet 2:87–102
Mundkur T, Nagy S (2012) Waterbird Populations Estimates. 5th Edition and online database at http://wpe.wetlands.org/
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283
Rhymer JM, Williams M, Braun MJ (1994) Mitochondrial analysis of gene flow between New Zealand mallards (Anas platyrhynchos) and grey ducks (A. superciliosa). Auk 111:970–978
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Scott DA, Rose PM (1996) Atlas of Anatidae populations in Africa and Western Eurasia. Wetlands International Press, Wageningen
Snow DW, Perrins CM (1998) The birds of the western Palearctic vol. 1: non-passerines. Oxford University Press, Oxford
Söderquist P, Gunnarsson G, Elmberg J (2012) Longevity and migration distance differ between wild and hand-reared mallards Anas platyrhynchos in Northern Europe. Eur J Wild 59:159–166
Spina F, Volponi S (2008) Atlante della Migrazione degli Uccelli in Italia. Vol. 1–2—Non Passeriformi, Passeriformi. Istituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA)
Van Oosterhout C, Hutchinson WF, Wills D, Shipley P (2004) MICRO-CHECKER: software to identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Williams CL, Brust RC, Fendley TT (2005) A comparison of hybridization between mottled ducks (Anas fulvigula) and mallards (A. platyrhynchos) in Florida and South Carolina using microsatellite DNA analysis. Conserv Genet 6:445–453
Zhang TJ, Li HF, Chen KW, Chang H, Tang QP, Zhang JX (2007) Genetic diversity and systematic evolution of Chinese domestic ducks along the Yangtze-Huai River. Biochem Genet 45:823–837
Acknowledgments
Many thanks go to Paolo Sposimo and Sara Fratini for suggestions and sampling assistance. We also thank Kevin McCracken and Jeff Peters for the support in the study and in providing samples from Canada. We also thank anonymous reviewers to revise the MS with many improvements. This research was funded by the Tuscany Region, the Department of Agricultural Development, Fishing and Hunting, and A.R.S.I.A. (Regional Agency for Agricultural Development and Innovation).
Conflict of interests
The authors of this study had no financial and personal relationships with other people or organizations that could inappropriately influence or bias their work
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Gortázar
Rights and permissions
About this article
Cite this article
Baratti, M., Baccetti, N., Cordaro, M. et al. Investigating the puzzling genetic structure of mallard populations (Anas platyrhynchos L.) in Italy. Eur J Wildl Res 61, 81–89 (2015). https://doi.org/10.1007/s10344-014-0876-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10344-014-0876-2