Population genetics of the hazel hen Bonasa bonasia in Poland assessed with non-invasive samples
Tóm tắt
Despite a severe decrease in the number of hazel hens during the 20th century, nowadays this grouse species is rather common in the forests of Northeastern and Southern Poland. We used mitochondrial control region and microsatellite markers to examine the genetic variability of Polish populations of hazel hens. We used non-invasively collected faeces to estimate genetic variability within populations, genetic differentiation among populations as well as genetic differentiation between two regions inhabited by two different subspecies of hazel hens. Our results confirm the usefulness of DNA from faeces to obtain reliable information on the population genetics of hazel hens. We found a rather high level of genetic variability in the Polish population. Genetic variability was higher in birds from continuous forests in the South of the country than in birds from fragmented habitats in the Northeast. Genetic differentiation was higher among subpopulations from Northeastern Poland. Additionally, both classes of molecular markers suggested the presence of two distinct genetic groups of birds, corresponding to previously described subspecies. We conclude that the genetic variability of the Polish hazel hen population has been influenced by habitat fragmentation and the history of the population during its post-glacial colonization of Poland from different glacial refugia.
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Cramp S., Simmons K.E.L., (Eds.), Handbook of the Birds of Europe, the Middle East, and North Africa: The Birds of the Western Palearctic, Volume II, Hawks to Bustards, Oxford University Press, 1980
Bergmann H.-H., Klaus S., Distribution, status and limiting factors of hazel grouse in central Europe, particularly in Germany, Gibier Faune Sauvage, 1994, 11, 5–32
Bergmann H.-H., Klaus S., Műller F., Scherzinger W., Swenson J.E., Wiesner J., Hazel hen [Die Haselhűhner], Westarp Wissenschaften, Magdeburg, Germany, 1996, (in German)
Różycki A.Ł, Keller M., Buczek T., Numbers and habitat preferences of the Hazel Grouse Bonasa bonasia in the Lasy Parczewskie forest [Liczebność i preferencje siedliskowe jarząbka Bonasa bonasia w Lasach Parczewskich], Notatki Ornitologiczne, 2007, 48, 151–162, (in Polish)
Tomiałojć L., Stawarczyk T., The avifauna of Poland. Distribution, numbers and trends [Awifauna Polski. Rozmieszczenie, liczebność i zmiany], Wrocław, 2003 (in Polish)
Bonczar Z., Hazel Hen Bonasa bonasia [Jarząbek Bonasa bonasia], In: Sikora A., Rohde Z., Gromadzki M., Neubauer G., Chylarecki P. (Eds.), The atlas of breeding birds in Poland 1985–2004 [Atlas rozmieszczenia ptaków lęgowych Polski 1985–2004], Bogucki Wydawnictwo Naukowe, Poznań, 2007, (in Polish)
Johansen H., The avifauna of Western Siberia - Otides to Gallus [Die Vogelfauna Westsibiriens - Otides bis Gallus], J. Ornitol., 1961, 102, 237–269 (in German)
Glutz von Blotzheim U.N., Bauer K., Bezzel E., Handbook of the birds of Central Europe [Handbuch der Vögel Mitteleuropas], Vol. 5, Galliformes und Gruiformes, 2nd ed., Aula-Verlag, Wiesbaden, 1994 (in German)
de Juana E., Family Tetraonidae, In: del Hoyo J., Elliott A., Sargatal J. (Eds.), Handbook of the Birds of the World, Volume 2, New World Vultures to Guineafowl, Lynx Edicions, Barcelona, 1994
Dementev G.P, Gladkov N.A. (Eds.), Birds of USSR [Pticy Sovetskovo Sojuza], Sovetskaja Nauka, Moskva, 1951 (in Russian)
Storch I., Status Survey and Conservation Action Plan 2000–2004: Grouse, IUCN, Gland, Switzerland and Cambridge, UK and World Pheasant Association, Reading, UK, 2000
Baba Y., Fujimaki Y., Klaus S., Butorina O., Drovetski S., Koike H., Molecular population phylogeny of Hazel Grouse Bonasa bonasia in East Asia inferred from mitochondrial control-region sequences, Wildlife Biol., 2002, 8, 251–259
Baba Y., Klaus S., Sun Y-H., Fujimaki Y. Molecular phylogeny and population history of the Chinese grouse and the hazel grouse, Bulletin of the Graduate School of Social and Cultural Studies, Kyushu University, 2005, 11, 77–82.
Sahlsten J., Thorngren H., Hoglund J., Inference of Hazel Grouse population structure using multilocus data: a landscape genetic approach, Heredity, 2008, 101, 475–482
Swenson J.E., Social organization of hazel grouse and ecological factors influencing it, PhD thesis, University of Alberta, Edmonton, USA, 1991
Segelbacher G., Steinbrück G., Bird faeces for sex identification and microsatellite analysis, Vogelwarte, 2001, 41, 139–142
Idaghdour Y., Broderick D., Korrida A., Faeces as a source of DNA for molecular studies in a threatened population of great bustards, Conserv. Genet., 2003, 4, 789–792
Beja-Pereira A., Oliveira R., Alves P.C., Schwartz M.K., Luikart G., Advancing ecological understandings through technological transformations in noninvasive genetics, Mol. Ecol. Resou., 2009, 9, 1279–1301
Taberlet P., Griffin S., Goossens B., Questiau S., Manceau V., Escaravage N., et al., Reliable genotyping of samples with very low DNA quantities using PCR, Nucleic Acids Res., 1996, 24, 3189–3194
Taberlet P., Waits L.P., Luikart G., Noninvasive genetic sampling: look before you leap, Trends Ecol. Evolut., 1999, 14, 323–327
Bellemain E., Taberlet P., Improved non invasive genotyping method: application to brown bear (Ursus arctos) faeces, Mol. Ecol. Notes, 2004, 4, 519–522
Piggott M.P., Bellemain E., Taberlet P., Taylor A.C, A multiplex pre-amplification method that significantly improves microsatellite amplification and error rates for faecal DNA in limiting conditions, Conserv. Genet., 2004, 5: 417–420
Morin P.A., Chambers K.E., Boesch C., Vigilant L., Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus), Mol. Ecol., 2001, 10, 1835–1844
Campbell N.R., Narum S.R, Quantitative PCR assessment of microsatellite and SNP genotyping with variable quality DNA extracts, Conserv. Genet., 2009, 10, 779–784
Miller C.R., Joyce P., Waits L.P, Assessing allelic dropout and genotype reliability using maximum likelihood, Genetics, 2002, 160, 357–366
Valière N., Berthier P., Mouchiroud D., Pontier D., GEMINI: software for testing the effects of genotyping errors and multitubes approach for individual identification, Mol. Ecol. Notes, 2002, 2, 83–86
Valière N., Bonefant C., Toigo C., Luikart G., Gaillard J-M., Klein F., Importance of a pilot study for non-invasive genetic sampling: genotyping errors and population size estimation in red deer, Conserv. Genet., 2007, 8, 69–78
Regnaut S., Lucas F.S., Fumagalli L., DNA degradation in avian faecal samples and feasibility of non-invasive genetic studies of threatened capercaille populations, Conserv. Genet., 2006, 7, 449–453
Hall T.A., BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT, Nucleic Acids Symp. Ser., 1999, 41, 95–98
Segelbacher G., Paxton R.J., Steinbrueck G., Trontelj P., Storch I., Characterisation of microsatellites in capercaillie (Tetrao urogallus) (AVES), Mol. Ecol., 2000, 9, 1934–1935
Piertney S.B., Höglund J., Polymorphic microsatellite markers in black grouse (Tetrao tetrix), Mol. Ecol. Notes, 2001, 1, 303–304
Caizergues A., Dubois S., Mondor G., Rasplus J-F., Isolation and characterization of microsatellite loci in black grouse (Tetrao tetrix), Mol. Ecol. Notes, 2001, 1, 36–38
Chambers, G.K., MacAvoy, E.S., Microsatellites: consensus and controversy, Comp. Biochem. Phys. B, 2000, 126, 455–476
Valière N., Gimlet: a computer program for analysing genetic individual identification data, Mol. Ecol. Resour., 2002, 2, 377–379
Nei M., Molecular Evolutionary Genetics, Columbia University Press, New York, 1987
Rozas J., Sánchez-DelBarrio J.C., Messeguer X., Rozas R., DnaSP, DNA polymorphism analyses by the coalescent and other methods, Bioinformatics, 2003, 19, 2496–2497
Excoffier L., Lischer H.E.L., Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows, Mol. Ecol. Resour., 2010, 10, 564–567
Fu Y-X., Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection, Genetics, 1997, 147, 915–925
Rogers A.R., Harpending H., Population growth makes waves in the distribution of pairwise genetic differences, Mol. Biol. Evol., 1992, 9, 552–569
Schneider S., Excoffier L., Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA, Genetics, 1999, 152, 1079–1089
Harpending H.C., Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution, Hum. Biol., 1994, 66, 591–660
Excoffier L., Smouse P.E., Quattro J.M., Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data, Genetics, 1992, 131, 479–491
Tamura K., Dudley J., Nei M., Kumar S., MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0, Mol. Biol. Evol., 2007, 24, 1596–1599
Petit R.J., El Mousadik A., Pons O., Identifying populations for conservation on the basis of genetic markers, Conserv. Biol., 1998, 12: 844–855
Nei M., Roychoudhury A.K., Sampling variances of heterozygosity and genetic distance, Genetics, 1974, 76, 379–390
Paekal R., Smouse P.E., GenAlEx V6: Genetic Analysis in Excel. Population genetic software for teaching and research, Mol. Eco. Not., 2006, 6, 288–295
Goudet J., Fstat version 1.2: a computer program to calculate F statistics, J. Hered., 1995, 6, 485–486
Raymond M., Rousset F., GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism, J. Hered., 1995, 86, 248–249
Rousset F., Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux, Mol. Ecol. Resour., 2008, 8, 103–106
Weir B.S., Cockerham C.C, Estimating F-statistics for the analysis of population structure, Evolution, 1984, 38, 1358–1370
Pritchard J.K., Stephens M., Donnelly P., Inference of population structure using multilocus genotype data, Genetics, 2000, 155, 945–959
Evanno G., Regnaut S., Goudet J., Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study, Mol. Ecol., 2005, 14, 2611–2620
Earl D.A., von Holdt B.M., STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method, Conserv. Gen. Res, 2012, 4, 359–361
Jakobsson M., Rosenberg N.A., CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure, Bioinformatics, 2007, 23, 1801–1806
Rosenberg N.A., DISTRUCT, a program for the graphical display of population structure, Mol. Ecol. Not., 2004, 4, 137–138
Piggott M.P., Taylor A.C., Remote collection of animal DNA and its applications in conservation management and under standing the population biology of rare and cryptic species, Wildlife Res., 2003, 30, 1–13
Wattier R., Engel C.R., Saumitou-Laprade P., Valero M., Short allele dominance as a source of heterozygote deficiency at microsatellite loci: experimental evidence at the dinucleotide locus Gv1CT in Gracilaria gracilis (Rhodophyta), Mol. Ecol., 1998, 7, 1569–1573
Broquet T., Ménard N., Petit E., Noninvasive population genetics: a review of sample source, diet, fragment length and microsatellite motif effect on amplification success and genotyping error rates, Conserv. Genet., 2007, 8, 249–260
Hoffman J.L., Amos W., Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion, Mol. Ecol., 2005, 14, 599–612
Kohn M.H., York E.C., Kamradt D.A., Haught G., Sauvajot R.M., Wayne R.K., Estimating population size by genotyping faeces, Proc. R. Soc. Lond. [Biol], 1999, 266, 657–663
Bayes M., Smith K., Alberts S., Altmann J., Bruford M., Testing the reliability of microsatellites typing from faecal DNA in the savannah baboon, Conserv. Genet., 2000, 1, 173–176
Lathuillière M., Ménard N., Gautier-Hion A., Crouau-Roy B., Testing the reliability of noninvasive genetic sampling by comparing analyses of blood and fecal samples in Barbary macaques (Macaca sylvanus), Am. J. Primatol., 2001, 55, 151–158
Lucchini V., Fabbri E., Marucco F., Ricci S, Boitani L., Randi E., Noninvasive molecular tracking of colonizing wolf (Canis lupus) packs in the western Italian Alps, Mol. Ecol., 2002, 11, 857–868
Maudet C., Luikart G., Dubray D., von Hardenberg A., Taberlet P., Low genotyping error rates in wild ungulate faeces sampled in winter, Mol. Ecol. Notes, 2004, 4, 772–775
Monteiro L., Bonnemaison D., Vekris A., Petry K.G., Bonnet J., Vidal R., et al., Complex polysaccharides as PCR inhibitors in feces: Helicobacter pylori model, J. Clin. Microbiol., 1997, 35, 995–998
Liukkonen-Antilla T., Rätti O., Kvist L., Helle P., Orell M., Lack of genetic structuring and subspecies differentiation in the capercaillie (Tetrao urogallus) in Finland, Ann. Zool. Fennici, 2004, 41, 619–633
Rutkowski R., Niewęgłowski H., Dziedzic R., Kmieć M., Goździewski J., Genetic variability of Polish population of the Capercaillie Tetrao urogallus, Acta Ornithologica, 2005, 40, 27–34
Caizergues A., Ratti O., Helle P., Rotelli L., Ellison L., Rasplus J.-F., Population genetic structure of male black grouse (Tetrao tetrix L.) in fragmented vs. continuous landscapes, Mol. Ecol., 2003, 12, 2297–2305
Segelbacher G., Hoglund J., Storch I., From connectivity to isolation: genetic consequences of population fragmentation in Capercaillie across Europe, Mol. Ecol., 2003, 12, 1773–1780
DiBattista J.D., Patterns of genetic variation in anthropogenically impacted populations, Conserv. Genet., 2008, 9, 141–156
Åberg J., Jansson G., Swenson J. E., Angelstam P., The effect of matrix on the occurrence of hazel grouse (Bonasa bonasia) in isolated habitat fragments, Oecologia, 1995, 103, 265–269
Segelbacher G., Storch I., Capercaillie in the Alps:genetic evidence of metapopulation structure and population decline, Mol. Ecol., 2002, 11, 1669–1677
Taberlet P., Fumagalli L., Wust-Saucy A.-G., Cosson J.-F., Comparative phylogeography and postglacial colonization routes in Europe, Mol. Ecol., 1998, 7, 453–464
Marmi J., López-Giráldez F., Macdonald D.W., Calafell F., Zholnerovskaya E., Domingo-Roura X., Mitochondrial DNA reveals a strong phylogeographic structure in the badger across Eurasia, Mol. Ecol., 2006, 15, 1007–1020
Segelbacher G., Piertney S., Phylogeography of the European Capercaillie (Tetrao urogallus) and its implications for conservation, J. Ornithol., 2007, 148, 269–274
Duriez O., Sachet J.M., Menonni E., Pidancier N., Miqulet C., Taberlet P., Phyleography of the capercaillie in Eurasia: what is the conservation status in the Pyrenees and Cantabrian Mounts? Conserv. Genet., 2007, 8, 513–526
Montadert M., Leonard P., Post-juvenile dispersal of Hazel Grouse (Bonasa bonasia) in an expanding population of the Southeastern French Alps, Ibis, 2006, 148, 1–13