Assessing the genetic structure of capercaillie (Tetrao urogallus) in Romania

Authors

  • Mihai Fedorca 1) National Institute for Research and Development in Forestry “Marin Dracea”, SCDEP Brasov, Closca street 13, Postal code 500040, Brasov, Romania 2) Transilvania University of Brasov, B-dul Eroilor 29, Postal code 500036, Brasov, Romania
  • Ovidiu Ionescu 1) National Institute for Research and Development in Forestry “Marin Dracea”, SCDEP Brasov, Closca street 13, Postal code 500040, Brasov, Romania 2) Transilvania University of Brasov, B-dul Eroilor 29, Postal code 500036, Brasov, Romania
  • Neculae Sofletea Transilvania University of Brasov, B-dul Eroilor 29, Postal code 500036, Brasov, Romania
  • Ancuta Fedorca 1) National Institute for Research and Development in Forestry “Marin Dracea”, SCDEP Brasov, Closca street 13, Postal code 500040, Brasov, Romania 2) Transilvania University of Brasov, B-dul Eroilor 29, Postal code 500036, Brasov, Romania
  • Alexandru Lucian Curtu Transilvania University of Brasov, B-dul Eroilor 29, Postal code 500036, Brasov, Romania
  • Georgeta Ionescu National Institute for Research and Development in Forestry “Marin Dracea”, SCDEP Brasov, Closca street 13, Postal code 500040, Brasov, Romania

DOI:

https://doi.org/10.15287/afr.2020.2025

Keywords:

capercaillie, genetics, gene flow, fragmentation, habitat

Abstract

Romania holds the most extensive mountain range with old-growth forests, in which both habitat surface and capercaillie (Tetrao urogallus) numbers are ones of the highest in Central and Eastern Europe. While previous genetic studies have found that the individuals located in different European mountain ranges are isolated and have highlighted that the species is declining. Here, we are aiming to assess the genetic structure of capercaillie in Romania by genotyping 137 samples collected in the field with 9 STR markers. Expected heterozygosity was 0.586, whereas observed heterozygosity values were 0.859. Population structure analyses indicated weak population differentiation and suggested that sufficient gene flow exists among individuals sampled in different mountain regions. We did not find evidence for a past genetic bottleneck. Our findings contain important information to wildlife managers to focus conservation efforts in areas such as Curvature Carpathians, which serve as a connectivity corridor to avoid eroding the extent or quality of habitat and to prevent further fragmentation.

Author Biographies

Mihai Fedorca, 1) National Institute for Research and Development in Forestry “Marin Dracea”, SCDEP Brasov, Closca street 13, Postal code 500040, Brasov, Romania 2) Transilvania University of Brasov, B-dul Eroilor 29, Postal code 500036, Brasov, Romania

Wildlife Department

Georgeta Ionescu, National Institute for Research and Development in Forestry “Marin Dracea”, SCDEP Brasov, Closca street 13, Postal code 500040, Brasov, Romania

Wildlife Department

References

Alda F., Sastre P., De La Cruz-Cardiel P.J., Doadrio I., 2011. Population genetics of the endangered Cantabrian capercaillie in northern Spain. Animal Conservation 14:249–260. https://doi.org/10.1111/j.1469-1795.2010.00425.x.Augustine B.C., Kéry M., Olano Marin J., Mollet P., Pasinelli G. and Sutherland C., 2019. Sex-specific population dynamics and demography of capercaillie (Tetrao urogallus L.) in a patchy environment. Population Ecology 62:80–90. https://doi.org/10.1002/1438-390X.12031.Bajc M., Čas M., Ballian D., Kunovac S., Zubić G., Grubešić M., Zhelev P., Paule L., Grebenc T., Kraigher H., 2011. Genetic differentiation of the Western Capercaillie highlights the importance of South-Eastern Europe for understanding the species phylogeography. PloSone 6:1-15. https://doi. org/10.1371/journal.pone.0023602.BirdLife International, 2015. Tetrao urogallus (Western Capercaillie). European Red List of Birds - Supplementary Material. European Red List of Birds, Luxembourg: Office for Official Publications of the European Communities 11.Catusse M., 1993. Spatial and temporal plasticity of a capercaillie (Tetrao urogallus) arena in the French Pyrenees. Ethology Ecology & Evolution 5(2):145–156, https://doi.org/10.1080/08927014.1993.9523098.Cazacu C., Adamescu M.C., Ionescu O., Inonescu G., Jurj R., Popa M., Cazacu R., Cotovelea A., 2014. Mapping trends of large and medium size carnivores of conservation interest in Romania. Annals of Forest Research 57:97–107. https://doi. org/10.15287/afr.2014.170.Chen C., Durand E., Forbes F., François O., 2007. Bayesian clustering algorithms ascertaining spatial population structure: A new computer program and a comparison study. Molecular Ecology Notes 7:747–756. https://doi. org/10.1111/j.1471-8286.2007.01769.x.Cornuet J.Ma., Luikart, G., 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144(4):2001–2014.Cushman S.A., McKelvey K.S., Hayden J., Schwartz M.K., 2006. Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Wildlife Biology Faculty Publications 168:486–499. https://doi.org/10.1086/506976.Evanno G., Regnaut S., Goudet, J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005. 02553.x.Fedorca M., Ionescu G., Ciocirlan E., Șofletea N., Fedorca, A., 2020. A simple automated approach to obtain DNA from capercaillie, brown bear and wolf faeces. Conservation Genetics Resources 12:33-36. https://doi.org/10.1007/s12686-018-1061-9.Frantz A.C., Cellina S., Krier A., Schley L., Burke T., 2009. Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population : clusters or isolation by distance ?. Journal of Applied Ecology 46:493–505. https://doi.org/10.1111/j.1365-2664.2008. 01606.x.Gaël A., Begoña A., Mathieu B., Evelyn M., Pierre M., Gregory T., Nicolas T., Marc Mo., Jesús M. P. , Antonio S., 2019 Comparing methods for estimating the abundance of western capercaillie Tetrao urogallus males in Pyrenean leks: singing counts versus genetic analysis of non-invasive samples. BirdStudy 66:565-569. https://doi: 10.1080/ 00063657.2020.1720594Goudet J., 1995. FSTAT (Version 1.2): A computer program to calculate F-statistics. Journal of Heredity 86:485–486. https://doi.org/10.1093/jhered/esh074.Greenwood P.J., Harvey P.H., 1982. The natal and breeding dispersal of birds. Annual review of ecology and systematics., 13:1–21. https://doi.org/10.1146/annurev.es. 13.110182.000245.Grodzińska K., Godzik B., Fra̧czek W., Badea O., Oszlányi J., Postelnicu D., Shparyk Y., 2004. Vegetation of the selected forest stands and land use in the Carpathian Mountains. Environmental Pollution 130:17–32. https://doi.org/10.1016/ j.envpol.2003.10.031.Guillot G., Mortier F., Estoup A., 2005. GENELAND : a computer package for landscape genetics. Molecular Ecology Notes 5:712–715. https://doi.org/10.1111/j.1471-8286.2005.01031.x.Guillot G., Renaud S., Ledevin R., Michaux J., Claude J., 2012. A unifying model for the analysis of phenotypic, genetic, and geographic data. Systematic biology 61:897–911. https://doi.org/10.1093/sysbio/sys038.Gurung A.B., Bokwa A., Chełmicki W., Elbakidze M., Hirschmugl M., Hostert P., Ibisch P., Kozak J., Kuemmerle T., Matei E., Ostapowicz K., Pociask-Karteczka J., Schmidt L., van der Linden S., Zebisch M., 2009. Global change research in the Carpathian Mountain Region. Mountain Research and Development 29:282–288. https://doi.org/10.1659/mrd.1105.Hartl D.L., Grant A., 1997. Principles of population genetics. 3rd edn. Sinauer Associates Inc., Sunderland, MA, 545p. https://doi.org/10.2980/1195-6860(2007)14[544b:POPG]2.0. CO;2.Jacob G., Debrunner R., Gugerli F., Schmid B., Bollmann K., 2010. Field surveys of capercaillie (Tetrao urogallus) in the Swiss Alps underestimated local abundance of the species as revealed by genetic analyses of non-invasive samples. Conservation Genetics 11:33–44. https://doi.org/10.1007/ s10592-008-9794-8.Janes J.K., Malenfant M., Andrew R.L., Miller J.M., Dupuis J.R., Gorrell J.C., Cullingham, C.I., 2017. The K = 2 conundrum. Molecular Ecology 26:3594–3602. https://doi. org/10.1111/mec.14187.Keller L.F., Waller D.M 2002. Inbreeding effects in wild populations. Trends in Ecology and Evolution 17:230–241. https://doi.org/10.1016/S0169-5347(02)02489-8.Kimura M., Weiss, G., 1964. The stepping stone model of populationa structure and the decrease of genetic correlation with distance. Genetics 49(4):561–576.Klinga P., Mikoláš M., Zhelev P., Höglund J., Paule, L., 2015. Genetic differentiation of western capercaillie in the Carpathian Mountains: The importance of post glacial expansions and habitat connectivity. Biological Journal of the Linnean Society 116:873–889. https://doi.org/10.1111/ bij.12643.Lencinas M.V., Cellini J.M., Benitez J., Peri P.L., Martínez Pastur G., 2018. Variable retention forestry conserves habitat of bird species in Patagonian Nothofagus pumilio forests. Annals of Forest Research 61:147–160. https://doi.org/10.15287/afr.2018.1186.Mäki-Petäys H., Corander J., Aalto J., Liukkonen T., Helle P., Orell M., 2007. No genetic evidence of sex-biased dispersal in a lekking bird, the capercaillie (Tetrao urogallus). Journal of evolutionary biology 20:865–873. https://doi.org/10.1111/ j.1420-9101.2007.01314.x.Mikolas M., Svitok M., Tejkal M., Leitão P.J., Morrissey R.C., Svoboda M., Seedre M., Fontaine J.B., 2015. Evaluating forest management intensity on an umbrella species: Capercaillie persistence in central Europe. Forest Ecology and Management 354:26–34, https://doi.org/10.1016/j. foreco.2015.07.001.Mills L.S., Allendorf, F.W., 1996. The one-migrant-per-generation rule in conservation and management. Conservation Biology 10:1509–1518. https://doi.org/10. 1046/j.1523-1739.1996.10061509.xNeville H.M., Isaak D.J., Dunham J.B., Thurow R.F., Rieman B.E., 2006. Fine-scale natal homing and localized movement as shaped by sex and spawning habitat in Chinook salmon: Insights from spatial autocorrelation analysis of individual genotypes. Molecular Ecology 15:4589–4602. https://doi.org/10.1111/j.1365-294X.2006. 03082.x.Peakall R., Smouse P.E., 2012. GenALEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460.Peakall R., Ruibal M., Lindenmayer D.B., 2003. Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution; international journal of organic evolution 57:1182–1195. https://doi.org/10.1111/j.0014-3820.2003.tb00327.x.Piertney S.B., Hoglund J., 2001. Polymorphic microsatellite DNA markers in black grouse (Tetrao tetrix). Molecular Ecology Notes 1:303–304.Piry S., Luikart G., Cornuet J.M., 1999. Computer note. BOTTLE- NECK: a computer program for detecting recent reductions in the effective size using allele frequency data. Journal of Heredity 90:502–503.Pritchard J.K., Stephens M., Donnelly P., 2000. Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1111/j.1471-8286. 2007.01758.x.Puechmaille S.J., 2016. The program STRUCTURE does not reliably recover the correct population structure when sampling is uneven : subsampling and new estimators alleviate the problem. Molecular Ecology Resources 16:608–627. https://doi.org/10.1111/1755-0998.12512.Regnaut S., 2004., Population genetics of capercaillie (Tetrao urogallus) in the Jura and the Pyrenees : A non-invasive approach to avian conservation genetics. PhD thesis, UNIL/CHUV, Lausanne, 180p.Regnaut S., Christe P., Chapuisat M., Fumagalli L., 2006. Genotyping faeces reveals facultative kin association on capercaillie’s leks. Conservation Genetics 7:665–674. https://doi.org/10.1007/s10592-005-9097-2.Rodríguez-Muñoz R., Mirol P.M., Segelbacher G., Fernández A., Tregenza T., 2007. Genetic differentiation of an endangered capercaillie (Tetrao urogallus) population at the Southern edge of the species range. Conservation Genetics 8:659–670. https://doi.org/10.1007/s10592-006-9212-z.Rösner S., Brandl R., Segelbacher G., Lorenc T., Müller J., 2014. Noninvasive genetic sampling allows estimation of capercaillie numbers and population structure in the Bohemian Forest. European Journal of Wildlife Research 60:789–801. https://doi.org/10.1007/s10344-014-0848-6.Rousset F., 1997. Genetic Differentiation and Estimation of Gene Flow from FStatistics Under Isolation by Distance. Genetics 145:1219–1228.Rutkowski R., Niewęgłowski H., Dziedzic R., Kmieć M., Goździewski J., 2005. Genetic variability of Polish population of the capercaillie Tetrao urogallus. Acta Ornithologica 40:27–34.Segelbacher G., 2002. Genetic structure of capercaillie populations : A non-invasive approach at multiple spatial scales. PhD thesis, Technischen Universität München, München, 98 p.Segelbacher G., Piertney S., 2007. Phylogeography of the European capercaillie (Tetrao urogallus) and its implications for conservation. Journal of Ornithology 148:269–274. https://doi.org/10.1007/s10336-007-0153-1.Segelbacher G., Storch, I., 2002. Capercaillie in the Alps : genetic evidence of metapopulation. Molecular Ecology 11:1669–1677.Segelbacher G., Paxton R., Steinbrueck G., Trontelj P., Storch I., 2000. Characterization of microsatellites in capercaillie Tetrao urogallus. Molecular Ecology 9:1934–1935.Segelbacher G., Hoglund J., Storch I., 2003. From connectivity to isolation: genetic consequences of population fragmentation in capercaillie across Europe. Molecular Ecology 12:1773–1780. https://doi.org/10.1046/j. 1365-294X.2003.01873.x.Segelbacher G., Wegge P., Sivkov A. V., Höglund J., 2007. Kin groups in closely spaced capercaillie leks. Journal of Ornithology 148:79–84. https://doi.org/10.1007/s10336-006-0103-3.Segelbacher G., Manel S., Tomiuk J., 2008. Temporal and spatial analyses disclose consequences of habitat fragmentation on the genetic diversity in capercaillie (Tetrao urogallus). Molecular ecology 17:2356–2367. https://doi.org/ 10.1111/j.1365-294X.2008.03767.x.Slatkin M., 1985. Gene flow in natural populations. Annual review of ecology and systematics 16:393–430. https://doi.org/10.1146/annurev.ecolsys.16.1.393.Smouse P.E., Peakall R., Gonzales E., 2008. A heterogeneity test for fine-scale genetic structure. Molecular Ecology 17:3389–3400. https://doi.org/10.1111/j.1365-294X.2008. 03839.x.Soulé M.E., 1987. Viable populations for conservation. Cambridge University Press, Cambridge, 185 p.Storch I., 1993. Habitat selection by capercaillie in summer and autumn: Is bilberry important? Oecologia 93:257–265.Straupe I., Liepa L., Zalite A.A., 2019. Habitat management for capercaillie Tetrao urogallus L. leks: The survey of vegetation changes. Research for Rural Development 1:38–43. https://doi.org/10.22616/rrd.25.2019.006.Tallmon D.A., Luikart G., Waples R.S., 2004. The alluring simplicity and complex reality of genetic rescue. Trends in Ecology and Evolution 19:489–496. https://doi.org/10.1016/ j.tree.2004.07.003.Vallant S., Niederstätter H., Berger B., Lentner R., Parson, W., 2018. Increased DNA typing success for feces and feathers of capercaillie (Tetrao urogallus) and black grouse (Tetrao tetrix). Ecology and Evolution 8:3941–3951. https://doi.org/10.1002/ece3.3951.Van Oosterhout C., Hutchinson W.F., Wills D.P.M., Shipley, P., 2004. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x.Wang J., 2004. Application of the one-migrant-per-generation rule to conservation and management. Conservation Biology 18:332–343.

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2020-12-31

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Research article