Abstract
Dispersal is a key process for the maintenance of intraspecific genetic diversity by ensuring gene flow within and between populations. Despite the ongoing expansion of large carnivores in Europe, lynx populations remain fragmented, isolated, and threatened by inbreeding and loss of genetic diversity. In the course of large carnivore monitoring in the Czech Republic, several biological samples of Eurasian lynx were collected outside the permanent occurrence of this species. Using microsatellite genoty** we identified these as four dispersing lynx males and applied multiple methods (Bayesian clustering in STRUCTURE, Principal Component Analysis (PCA), frequency-based method in GENECLASS2, and machine-learning framework in assignPOP) to assign them to possible source populations. For this we used genotypes from five European lynx populations: the Bohemian-Bavarian-Austrian (N = 36), Carpathian (N = 43), Scandinavian (N = 20), Baltic (N = 15), and Harz (N = 23) population. All four dispersers were successfully assigned to different source populations within Europe and each was recorded at a distance of more than 98 km from the edge of the distribution of the source population identified. Such movements are among the longest described for lynx in Central Europe to this point. The findings indicate the ability of lynx males to disperse in human-dominated landscape thus facilitation of these movements via creation and/or protection of potential migratory corridors together with protection of dispersing individuals should be of high importance in conservation of this iconic predator in Central Europe.
Similar content being viewed by others
Data availability
Genotype data are given in the Supplementary material, Table S2.
References
Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J et al (2013) Hybridization and speciation. J Evol Biol 26:229–246. https://doi.org/10.1111/j.1420-9101.2012.02599.x
Adams JR, Waits LP (2007) An efficient method for screening faecal DNA genotypes and detecting new individuals and hybrids in the red wolf (Canis rufus) experimental population area. Conserv Genet 8:123–131. https://doi.org/10.1007/s10592-006-9154-5
Åkesson M, Liberg O, Sand H, Wabakken P, Bensch S, Flagstad Ø (2016) Genetic rescue in a severely inbred wolf population. Mol Ecol 25(19):4745–4756. https://doi.org/10.1111/mec.13797
Anděl P, Mináriková T, Andreas M (eds) (2010) Ochrana průchodnosti kra**y pro velké savce. Evernia, Liberec, p 137
Anderson E (1949) Introgressive hybridization. John Wiley and Sons, New York. https://doi.org/10.1111/j.1469-185X.1953.tb01379.x
Bagrade G, Ruņģis DE, Ornicāns A, Šuba J, Žunna A, Howlett SJ, Lūkins M, Gailīte A, Stepanova A, Done G, Gaile A, Bitenieks K, Mihailova L, Baumanis J, Ozoliņš J (2016) Status assessment of Eurasian lynx in Latvia linking genetics and demography–a growing population or a source–sink process? Mamm Res 61:337–352. https://doi.org/10.1007/s13364-016-0279-8
Bartoń KA, Zwijacz-Kozica T, Zięba F, Sergiel A, Selva N (2019) Bears without borders: long-distance movement in human-dominated landscapes. Glob Ecol Conserv 1:e00541. https://doi.org/10.1111/j.1365-2907.2011.00192.x
Böer M, Reklewski J, Śmiełowski J, Tyrała P (2000) Reintroduction of the European Lynx to the kampinoski national park/Poland-a field experiment with zooborn individuals. Part III: demographic development of the population from December 1993 until January 2000. Der Zoologische Garten 70(5):304–312
Breitenmoser-Würsten C, Obexer-Ruff G (2003) Population and conservation genetics of two re-introduced lynx (Lynx lynx) populations in Switzerland—a molecular evaluation 30 years after translocation. In: Proceedings of the 2nd Conference on the Status and Conservation of the Alpine Lynx Population (SCALP):7–9
Bull J, Heurich M, Saveljev A, Schmidt K, Fickel J, Förster D (2016) The effect of reintroduction on the genetic variability in Eurasian lynx populations: the cases of Bohemian Bavarian and Vosges-Palatinian populations. Conserv Genet 17:1229–1234. https://doi.org/10.1007/s10592-016-0839-0
Bullock JM, Kenward RE, Hails RS (2002) Dispersal ecology. Cambridge University Press, New York, p 480p
Červený J, Krojerová-Prokešová J, Kušta T, Koubek P (2019) The change in the attitudes of Czech hunters towards Eurasian lynx: is poaching restricting lynx population growth? J Nat Conserv 47:28–37. https://doi.org/10.1016/j.jnc.2018.11.002
Chapron G, Kaczensky P, Linnell JD, von Arx M, Huber D, Andrén H et al (2014) Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346:1517–1519. https://doi.org/10.1126/science.1257553
Chen KY, Marschall EA, Sovic MG, Fries AC, Gibbs HL, Ludsin SA (2018) assignPOP: an R package for population assignment using genetic, non-genetic, or integrated data in a machine learning framework. Methods Ecol Evol 9:439–446. https://doi.org/10.1111/2041-210X.12897
Copernicus Land Monitoring Service (2018) European Environment Agency (EEA), European Union. https://land.copernicus.eu/pan-european/high-resolution-layers/forests/forest-type-1/status-maps/forest-type-2018
Clobert J, Baguette M, Benton TG, Bullock JM (eds) (2012) Dispersal ecology and evolution. Oxford University Press. https://doi.org/10.1093/acprof:oso/9780199608898.001.0001
Crooks KR, Burdett CL, Theobald DM, King SR, Di Marco M, Rondinini C, Boitani L (2017) Quantification of habitat fragmentation reveals extinction risk in terrestrial mammals. PNAS 114:7635–7640. https://doi.org/10.1073/pnas.1705769114
Dobson FS (1982) Competition for mates and predominant juvenile male dispersal in mammals. Anim Behav 30:1183–1192. https://doi.org/10.1016/S0003-3472(82)80209-1
Duľa M, Krofel M (2020) A cat in paradise: hunting and feeding behaviour of Eurasian lynx among abundant naive prey. Mamm Biol. https://doi.org/10.1007/s42991-020-00070-6
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419
Fattebert J, Balme G, Dickerson T, Slotow R, Hunter L (2015) Density-dependent natal dispersal patterns in a leopard population recovering from over-harvest. PLoS ONE 10(4):e0122355. https://doi.org/10.1371/journal.pone.0122355
Flousek J, Zajac T, Kutal M, Zuczkowski M, Palucki A, Pudil M, Kafka P (2014) Velké šelmy (Carnivora) v Krkonoších, Jizerských horách, Górach Stołowych a na Broumovsku (Česká republika, Polsko) – minulost a přítomnost. Opera Corcontica 51:37–59
Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, pp. 617 ISBN 9780521639859
Frankham R (2015) Genetic rescue of small, inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618. https://doi.org/10.1111/mec.13139
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162. https://doi.org/10.1016/S0003-3472(80)80103-5
Groff C, Dalpiaz D, Frapporti C, Zanghellini P (eds) (2009) Rapporto Orso 2008 del Servizio Foreste e Fauna della Provincia Autonoma di Trento
Goudet J (2005) Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186. https://doi.org/10.1111/j.1471-8286.2004.00828.x
Gour DS, Bhagavatula J, Bhavanishankar M, Reddy PA, Gupta JA, Sarkar MS et al (2013) Philopatry and dispersal patterns in tiger (Panthera tigris). PLoS ONE 8(7):e66956. https://doi.org/10.1371/journal.pone.0066956
Herrero A, Heikkinen J, Holmala K (2020) Movement patterns and habitat selection during dispersal in Eurasian lynx. Mamm Res 65:523–533. https://doi.org/10.1007/s13364-020-00499-7
Janečka JE, Blankenship TL, Hirth DH, Kilpatrick CW, Tewes ME, Grassman LIJ (2007) Evidence for male-biased dispersal in bobcats Lynx rufus using relatedness analysis. Wildl Biol 13:38–47. https://doi.org/10.2981/0909-6396(2007)13[38:EFMDIB]2.0.CO;2
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Kaczensky P, Chapron G, Arx M von, Huber D, Andrén H, Linnell J (eds) (2013) Status, management and distribution of large carnivores—bear, lynx, wolf and wolverine—in Europe (Report to the EU Commission, Part 1 and Part 2, 2013)
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Res 15(5):1179–1191. https://doi.org/10.1111/1755-0998.12387
Kratochvíl J, Vala F (1968) History of occurrence of the lynx in Bohemia and Moravia. In: Kratochvíl J. (ed.) History of the distribution of the lynx in Europe. Acta Sc Nat Brno 2(4):35–48
Krojerová-Prokešová J, Turbaková B, Jelenčič M, Bojda M, Kutal M, Skrbinšek T, Koubek P, Bryja J (2019) Genetic constraints of population expansion of the Carpathian lynx at the western edge of its native distribution range in Central Europe. Heredity 122(6):785–799. https://doi.org/10.1038/s41437-018-0167-x
Kutal M, Belotti E, Volfová J, Mináriková T, Bufka L, Poledník L, Krojerová J, Bojda M, Váňa M, Kutalová L, Beneš J, Flousek J, Tomášek V, Kafka P, Poledníková K, Pospíšková J, Dekař P, Machciník B, Koubek P, Duľa M (2017) Occurrence of large carnivores – Lynx lynx, Canis lupus, and Ursus arctos – and of Felis silvestris in the Czech Republic and western Slovakia in 2012–2016 (Carnivora). Lynx, New Series 48(1):93–107. https://doi.org/10.2478/lynx-2017-0006
Large Carnivore Initiative for Europe, LCIE (2020) Online at https://www.lcie.org/. Accessed on 12. 10. 2020
Li YL, Liu JX (2018) StructureSelector: a web-based software to select and visualize the optimal number of clusters using multiple methods. Mol Ecol Res 18:176–177. https://doi.org/10.1111/1755-0998.12719
Lucena-Perez M, Marmesat E, Kleinman-Ruiz D et al (2020) Genomic patterns in the widespread Eurasian lynx shaped by late quaternary climatic fluctuations and anthropogenic impacts. Mol Ecol 29:812–828. https://doi.org/10.1111/mec.15366
Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629. https://doi.org/10.2307/2409915
Mueller SA, Reiners TE, Middelhoff TL, Anders O, Kasperkiewicz A, Nowak C (2020) The rise of a large carnivore population in Central Europe: genetic evaluation of lynx reintroduction in the Harz Mountains. Conserv Genet. https://doi.org/10.1007/s10592-020-01270-w
Mysłajek RW, Kwiatkowska I, Diserens TA, Haidit A, Nowak S (2019) Occurrence of Eurasian lynx in western Poland after two decades of strict protection. Cat News 69:12–13
Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354. https://doi.org/10.1111/j.1365-294X.1995.tb00227.x
Paetkau D, Slade R, Burden M, Estoup A (2004) Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65. https://doi.org/10.1046/j.1365-294X.2004.02008.x
Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539. https://doi.org/10.1093/jhered/esh074
Port M, Henkelmann A, Schröder F, Waltert M, Middelhoff L, Anders O, Jokisch S (2020) Rise and fall of a Eurasian lynx (Lynx lynx) step**-stone population in central Germany. Mamm Res. https://doi.org/10.1007/s13364-020-00527-6
Pritchard JK, 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 SJ (2016) The program structure does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol Ecol Res 16:608–627. https://doi.org/10.1111/1755-0998.12512
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.
Ratkiewicz M, Matosiuk M, Saveljev AP, Sidorovich V, Ozolins J, Männil P, Balciauskas L, Kojola I, Okarma H, Kowalczyk R, Schmidt K (2014) Long-range gene flow and the effects of climatic and ecological factors on genetic structuring in a large, solitary carnivore: the Eurasian lynx. PLoS ONE 9(12):e115160. https://doi.org/10.1371/journal.pone.0115160
Reklewski JA (2006) Ryś w Puszczy Kampinoskiej. Kampinoski Park Narodowy, Izabelin, p 68
Samelius G, Andrén H, Liberg O, Linnell JDC, Odden J, Ahlqvist P, Segerström P, Sköld K (2012) Spatial and temporal variation in natal dispersal by Eurasian lynx in Scandinavia. J Zool 286:120–130. https://doi.org/10.1111/j.1469-7998.2011.00857.x
Schmidt K (1998) Maternal behaviour and juvenile dispersal in the Eurasian lynx. Acta Theriol 43:391–408. https://doi.org/10.4098/AT.ARCH.98-37
Seidler RG, Long RA, Berger J, Bergen S, Beckmann JP (2015) Identifying impediments to long-distance mammal migrations. Conserv Biol 29:99–109. https://doi.org/10.1111/cobi.12376
Sindičić M, Polanc P, Gomerčić T, Jelenčič M, Huber Đ, Trontelj P, Skrbinšek T (2013) Genetic data confirm critical status of the reintroduced Dinaric population of Eurasian lynx. Conserv Genet 14:1009–1018. https://doi.org/10.1007/s10592-013-0491-x
Støen O-G, Zedrosser A, Sæbø S, Swenson JE (2006) Inversely density-dependent natal dispersal in brown bears Ursus arctos. Oecologia 148:356–364. https://doi.org/10.1007/s00442-006-0384-5
Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N et al (1996) Reliable genoty** of samples with very low DNA quantities using PCR. Nucleic Acids Res 26:3189–3194. https://doi.org/10.1093/nar/24.16.3189
Trakhtenbrot A, Nathan R, Perry G, Richardson DM (2005) The importance of long-distance dispersal in biodiversity conservation. Divers Distrib 11(2):173–181. https://doi.org/10.1111/j.1366-9516.2005.00156.x
von Arx M, Breitenmoser-Würsten C, Breitenmoser U (2009) Lessons from the reintroduction of the Eurasian lynx in Central and West Europe (Lecciones aprendidas a partir de la reintroducción dellince boreal en Europa Central y Occidental). In Iberian Lynx ex situ conservation: an interdisciplinary approach, pp. 403–409.
Wabakken P, Sand H, Kojola I, Zimmermann B, Arnemo JM, Pedersen HC, Liberg O (2007) Multistage, long-range natal dispersal by a global positioning system-collared Scandinavian wolf. J Wildl Manage 71:1631–1634. https://doi.org/10.2193/2006-222
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol 38:1358–1370. https://doi.org/10.1111/j.1558-5646.1984.tb05657.x
Wultsch C, Caragiulo A, Dias-Freedman I, Quigley H, Rabinowitz S, Amato G (2016) Genetic diversity and population structure of Mesoamerican Jaguars (Panthera onca): implications for conservation and management. PLoS ONE 11(10):e0162377. https://doi.org/10.1371/journal.pone.0162377
Zimmermann F, Breitenmoser-Würsten C, Breitenmoser U (2005) Natal dispersal of Eurasian lynx (Lynx lynx) in Switzerland. J Zool 267(4):381–395. https://doi.org/10.1017/S0952836905007545
Zimmermann F, Breitenmoser-Würsten C, Breitenmoser U (2007) Importance of dispersal for the expansion of a Eurasian lynx Lynx lynx population in a fragmented landscape. Oryx 41(3):358–368. https://doi.org/10.1017/S0030605307000712
Acknowledgements
We would like to thank to all volunteers of Wolf/Lynx patrols and members of NP and PLA administrations (especially Dana Bartošová, Hana Bednářová, Michal Bojda, Radim Chrobok, Vladimír Čech, Peter Drengubiak, Rostislav Dvořák, Michal Gajdár, Martin Gendiar, Ľuboslav Hrdý, František Jaskula, Petr Konupka, Martin Kraus, Jiří Labuda, Beňadik Machciník, Leona Marčáková, Stanislav Němec, Peter Pecík, Martin Špilák, Jerguš Tesák, Luděk Toman, Václav Tomášek, Martin Váňa) and to Ole Anders and the Lynx Harz team for their help with sample collection, to Josef Bryja and Petr Koubek for valuable comments to previous drafts of the manuscript, and Anna Bryjová for technical support in fragment analysis. Also, we would like to thank Rory Putman for revision of English and all valuable suggestions to the manuscript.
Funding
This article is based upon work from COST Action G-Bike (CA18134), supported by COST (European Cooperation in Science and Technology). The study was financially supported by INTER-EXCELLENCE – INTER-COST (LTC20021), Interreg V-A SR-CR (304021D016), Interreg Central Europe (CE1001; 3Lynx) and by Institutional Research Plan (RVO: 68081766).
Author information
Authors and Affiliations
Contributions
BG wrote the first draft of the manuscript and performed statistical analyses. BG and JKP performed laboratory analyses and designed the study. All authors collected samples and edited/approved previous versions of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Consent to participate
The manuscript does not contain any individual person’s data – not applicable.
Consent to publish
All authors consent to submitting this article to Conservation Genetics.
Research involving human and animal rights
Genetic material was collected in accordance with institutional, national, and international guidelines. Permits for animal capture and handling were obtained from the PLA Moravian Karst Administration and the Ministry of Environment of the Czech Republic, permit numbers: SR/0081/JM/2017; 34128/ENV/17-2146/630/17. No animals were killed due to sampling.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gajdárová, B., Belotti, E., Bufka, L. et al. Long-distance Eurasian lynx dispersal – a prospect for connecting native and reintroduced populations in Central Europe. Conserv Genet 22, 799–809 (2021). https://doi.org/10.1007/s10592-021-01363-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-021-01363-0