Abstract
Throughout history the human–wolf interaction has not evolved in favour of the wolf, however, wolves have never been endangered in Russia. The wolf (Canis lupus lupus L., 1758) population in the central part of European Russia is relatively high, where environmental conditions, such as relatively undisturbed habitats, wide forested areas and abundance of natural prey, have always contributed to the long-term survival of the species. The human persecution of wolves has resulted in almost total extinction of the species in many European countries. In Russia, extermination campaigns have led to severe fluctuations in the number of wolves during the second half of the twentieth century, however, since the early 1990s there has been a tendency towards constant growth in the numbers. Previous studies provided preliminary data on population genetics of the wolf population in European Russia and have generally shown homogeneity of the population structure as well as detecting genetic bottleneck. However, the comprehensive study of genetic diversity and population structure during the period following the last severe decline is of great interest. Another important aspect in the study of wolf populations is the assessment of the magnitude of wolf × dog hybridisation, which is a phenomenon of conservation and social significance. We used 101 samples from the wolf population and 32 dogs to examine population structure, genetic diversity and events of interspecific hybridisation in the centre of European Russia, based on analysis of 11 autosomal microsatellites. In the studied region, wolves exhibit a high level of genetic diversity (HE = 0.79 ± 0.03, HO = 0.74 ± 0.01, NA = 10.00 ± 5.02) which is superior to that in most European populations. Analysis of temporal samples suggests a slight increase in heterozygosity over time, although in the first period following population decline, the level of genetic diversity is not depleted. We found a lack of spatial structure and a weak pattern of isolation by distance (b = − 0.007, P < 0.001), which are clear cases of intense gene flow and social organisation of the species. Our preliminary results suggest a relatively low rate of hybridisation in the studied region (around 3%), however, additional studies are needed to provide more reliable conclusions on this topic. This paper is the first attempt at both a detailed study of spatio-temporal population genetics and analysis of hybridisation in the wolves of Central Russia.
Similar content being viewed by others
Availability of data and material
List of individual multilocus genotypes is provided as supplementary Table S1 (Korablev et al_Supplementary material-Table S1.xlsx). Additional tables and plots are provided as supplementary files (Korablev et al_Supplementary material-Tables S2–S3.pdf; Korablev et al_Supplementary material-Fig S1-S2.pdf).
References
Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23(6):327–337. https://doi.org/10.1016/j.tree.2008.02.008
Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229
Andersone Z, Lucchini V, Randi E, Ozolins J (2002) Hybridization between wolves and dogs in Latvia as documented using mitochondrial and microsatellite DNA markers. Mamm Biol 67:79–90. https://doi.org/10.1078/1616-5047-00012
Aspi J, Roininen M, Kiiskila J, Ruokonen M, Kojola I, Bljudnik L, Danilov P, Heikkinen S, Pulliainen E (2009) Genetic structure of the northwestern Russian wolf populations and gene flow between Russia and Finland. Conserv Genet 10:815–826. https://doi.org/10.1007/s10592-008-9642-x
Aspi J, Roininen E, Ruokonen M, Kojola I, Vila C (2006) Genetic diversity, population structure, effective population size and demographic history of the Finnish wolf population. Mol Ecol 15:1561–1576. https://doi.org/10.1111/j.1365-294X.2006.02877.x
Bakan J, Lavadinović V, Popović Z, Paule L (2014) Genetic differentiation of grey wolf population (Canis lupus L.) from Balkan and Carpathians. Balk J Wildl Res 1(1):87–93. https://doi.org/10.15679/bjwr.v1i1.17
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire génome, populations, interactions. CNRS UMR 5000. Université de Montpellier II, France. https://kimura.univmontp2.fr/genetix/. Accessed 12 Feb 2020
Bibikov DI (ed) (1985) The wolf. History, systematics, morphology, ecology. Nauka Publishers, Moscow (in Russian)
Bibikov DI (1994) Wolf problem in Russia. Lutreola 3:10–14
Boitani L (2000) Action plan for the conservation of the wolves (Canis lupus) in Europe. Nat Environ Counc Eur Publ 11:31–86
Boitani L, Phillips M, Jhala Y (2018) Canis lupus. The IUCN red list of threatened species. 2018. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T3746A119623865.en. Accessed 10 Feb 2020
Bondarev AY, Vorobevskaya EA, Politov DV (2013) On the genetic differentiation of the Siberian wolf. Vestn Altai Gos Agrar Univ 9(107):49–57 (in Russian)
Caniglia R, Galaverni M, Velli E, Mattucci F, Canu A, Apollonio M, Mucci N, Scandura M, Fabbri E (2020) A standardized approach to empirically define reliable assignment thresholds and appropriate management categories in deeply introgressed populations. Sci Rep 10:2862. https://doi.org/10.1038/s41598-020-59521-2
Carmichael LE, Nagy JA, Larter NC, Strobeck C (2001) Prey specialization may influence patterns of gene flow in wolves of the Canadian Northwest. Mol Ecol 10:2787–2798. https://doi.org/10.1046/j.0962-1083.2001.01408.x
Corander J, Sirén J, Arjas E (2008) Bayesian spatial modelling of genetic population structure. Comput Stat 23:111–129. https://doi.org/10.1007/s00180-007-0072-x
Cullingham CI, Miller JM, Peery RM, Dupuis JR, Malenfant RM, Gorrell JC, Janes JK (2020) Confidently identifying the correct K value using the ΔK method: when does K = 2? Mol Ecol 29:862–869. https://doi.org/10.1111/mec.15374
Ðan M, Šnjegota D, Veličković N, Stefanović M, Obreht Vidaković D, Ćirović D (2016) Genetic variability and population structure of grey wolf (Canis lupus) in Serbia. Russ J Genet 52(8):821–827. https://doi.org/10.1134/S1022795416080044
De Groot GA, Nowak C, Skrbinšek T, Andersen LW, Aspi J, Fumagalli L, Godinho R, Harms V, Jansman HAH, Liberg O, Marucco F, Mysłajek RW, Nowak S, Pilot M, Randi E, Reinhardt I, Śmietana W, Szewczyk M, Taberlet P, Vilà C, Muñoz-Fuentes (2016) Decades of population genetic research reveal the need for harmonization of molecular markers: the grey wolf Canis lupus as a case study. Mamm Rev 46(1):44–59. https://doi.org/10.1111/mam.12052
Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14(1):209–214. https://doi.org/10.1111/1755-0998.12157
Donfrancesco V, Ciucci P, Salvatori V, Benson D, Andersen LW, Bassi E, Blanco JC, Boitani L, Caniglia R, Canu A, Capitani C, Chapron G, Czarnomska SD, Fabbri E, Galaverni M, Galov A, Gimenez O, Godinho R, Greco C, Hindrikson M, Huber D, Hulva P, Jędrzejewski W, Kusak J, Linnell J, Llaneza L, López-Bao JV, Männil P, Marucco F, Mattioli L, Milanesi P, Milleret C, Mysłajek RW, Ordiz A, Palacios V, Pedersen HC, Pertoldi C, Pilot M, Randi E, Rodríguez A, Saarma U, Sand H, Scandura M, Stronen AV, Tsingaraska E, Mukherjee N (2019) Unravelling the scientific debate on how to address wolf-dog hybridization in Europe. Front Ecol Evol. https://doi.org/10.3389/fevo.2019.175
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361. https://doi.org/10.1007/s12686-011-9548-7
Escudero A, Iriondo JM, Torres ME (2003) Spatial analysis of genetic diversity as a tool for plant conservation. Biol Conserv 113:351–365. https://doi.org/10.1016/S0006-3207(03)00122-8
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
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50. https://doi.org/10.1177/117693430500100003
Fabbri E, Miquel C, Lucchini V, Santini A, Caniglia R, Duchamp C, Weber J-M, Lequette B, Marucco F, Boitani L, Fumagalli L, Taberlet P, Randi E (2007) From the Apennines to the Alps: colonization genetics of the naturally expanding Italian wolf (Canis lupus) population. Mol Ecol 16:1661–1671. https://doi.org/10.1111/j.1365-294X.2007.03262.x
Francisco LV, Langston AA, Mellersh CS, Neal CL, Ostrander EA (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7:359–362. https://doi.org/10.1007/s003359900104
Fredholm M, Wintero AK (1995) Variation of short tandem repeats within and between species belonging to the Canidae family. Mamm Genome 6:11–18. https://doi.org/10.1007/BF00350887
Galaverni M, Caniglia R, Pagani L, Fabbri E, Boattini A, Randi E (2017) Disentangling timing of admixture, patterns of introgression and phenotypic indicators in a hybridizing wolf population. Mol Biol Evol 34:2324–2339. https://doi.org/10.1093/molbev/msx169
Godinho R, Llaneza L, Blanco JC, Lopes S, Alvares F, Garcıa EJ, Palacios V, Cortes Y, Talegon J, Ferrand N (2011) Genetic evidence for multiple events of hybridization between wolves and domestic dogs in the Iberian Peninsula. Mol Ecol 20:5154–5166. https://doi.org/10.1111/j.1365-294X.2011.05345.x
Gómez-Sánchez D, Olalde I, Sastre N, Enseñat C, Carrasco R, Marques-Bonet T, Lalueza-Fox C, Leonard JA, Vilà C, Ramírez O (2018) On the path to extinction: inbreeding and admixture in a declining grey wolf population. Mol Ecol 27:3599–3612. https://doi.org/10.1111/mec.14824
Goudet J (1995) A program for estimating and testing gene diversities and differentiation statistics from codominant genetic markers. J Hered 86(6):485–486. https://doi.org/10.1093/oxfordjournals.jhered.a111627
Gubar YP (1996) The wolf. In: Lomanov IK (ed) Resources of main species of game animals and hunting grounds of Russia (1991–1995). TSNIL Hunting Department of Agricultural Ministry of Russia, Moscow, pp 153–169 (in Russian)
Gubar YP (2007) The wolf. In: Gubar YP (ed) Status of resources game animals in Russian Federation 2003–2007. Hunting Department of Agricultural Ministry of Russia, Moscow, pp 84–89 (in Russian)
Gubar YP (2010) The wolf. In: Lomanova NV (ed) Status of resources game animals in Russian Federation 2008–2010. Department of State Policy and Regulation of Hunting and Preservation of Hunting Resources, Ministry of Natural Resources and Ecology of the Russian Federation, Moscow, pp 145–153 (in Russian)
Hardy OJ, Vekemans X (2002) SPAGEDI: a versatile computer program to analyse spatial genetic structure at the individual or population level. Mol Ecol Notes 2:618–620. https://doi.org/10.1046/j.1471-8286.2002.00305.x
Harris RB, Wall WA, Allendorf FW (2002) Genetic consequences of hunting: what do we know and what should we do? Wildl Soc Bull 30:634–643
Hindrikson M, Mannil P, Ozolins J, Krzywinski A, Saarma U (2012) Bucking the trend in wolf-dog hybridization: first evidence from Europe of hybridization between female dogs and male wolves. PLoS ONE 7:e46465. https://doi.org/10.1371/journal.pone.0046465
Hindrikson M, Remm J, Männil P, Ozolins J, Tammeleht E, Saarma U (2013) Spatial genetic analyses reveal cryptic population structure and migration patterns in a continuously harvested grey wolf (Canis lupus) population in north-eastern Europe. PLoS ONE 8:e75765. https://doi.org/10.1371/journal.pone.0075765
Hindrikson M, Remm J, Pilot M, Godinho R, Stronen AV, Baltrūnaité L, Czarnomska SD, Leonard JA, Randi E, Nowak C, Åkesson M, López-Bao JV, Álvares F, Llaneza L, Echegaray J, Vilà C, Ozolins J, Rungis D, Aspi J, Paule L, Skrbinšek T, Saarma U (2017) Wolf population genetics in Europe: a systematic review, meta-analysis and suggestions for conservation and management. Biol Rev 92:1601–1629. https://doi.org/10.1111/brv.12298
Jędrzejewski W, Schmidt K, Jędrzejewska B, Theuerkauf J, Kowalczyk R, Zub K (2004) The process of a wolf pack splitting in Białowieża Primeval Forest. Poland Acta Theriol 49(2):275–280. https://doi.org/10.1007/BF03192527
Jędrzejewski W, Branicki W, Veit C, Medugorac I, Pilot M, Bunevich AN, Jędrzejewska B, Schmidt K, Theuerkauf J, Okarma H, Gula R, Szymura L, Forster M (2005) Genetic diversity and relatedness within packs in an intensely hunted population of wolves Canis lupus. Acta Theriol 50:3–22. https://doi.org/10.1007/BF03192614
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
Khosravi R, Rezaei HR, Kaboli M (2013) Detecting hybridization between Iranian wild wolf (Canis lupus pallipes) and free-ranging domestic dog (Canis familiaris) by analysis of microsatellite markers. Zool Sci 30(1):27–34. https://doi.org/10.2108/zsj.30.27
Lehman N, Clarkson P, Mech LD, Meier TJ, Wayne RK (1992) A study of the genetic relationships within and among wolf packs using DNA fingerprinting and mitochondrial DNA. Behav Ecol Sociobiol 30:83–94. https://doi.org/10.1007/BF00173944
Liberg O, Andren H, Pedersen H-C, Sand H, Sejberg D, Wabakken P, Akesson M, Bensch S (2005) Severe inbreeding depression in a wild wolf (Canis lupus) population. Biol Lett 1:17–20. https://doi.org/10.1098/rsbl.2004.0266
Linnell JDC, Boitani L (2012) Building biological realism into wolf management policy: the development of the population approach in Europe. Hystrix 23(1):80–91. https://doi.org/10.4404/hystrix-23.1-4676
Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425. https://doi.org/10.1002/j.1537-2197.1995.tb12679.x
Lucchini V, Fabbri E, Marucco F, Ricci S, Boitani L, Randi E (2002) Noninvasive molecular tracking of colonizing wolf (Canis lupus) packs in the western Italian Alps. Mol Ecol 11:857–868. https://doi.org/10.1046/j.1365-294X.2002.01489.x
Mech LD, Boitani L (eds) (2003) Wolves. Behavior, ecology, and conservation. University of Chicago Press, Chicago
Montana L, Caniglia R, Galaverni M, Fabbri E, Ahmed A, Bolfíkovâ BČ, Czarnomska SD, Galov A, Godinho R, Hindrikson M, Hulva P, Jędrzejewska B, Jelenčič M, Kutal M, Saarma U, Skrbinšek T, Randi E (2017) Combining phylogenetic and demographic inferences to assess the origin of the genetic diversity in an isolated wolf population. PLoS ONE 12(5):e0176560. https://doi.org/10.1371/journal.pone.0176560
Moura AE, Tsingarska E, Dąbrowski MJ, Czarnomska SD, Jędrzejewska B, Pilot M (2014) Unregulated hunting and genetic recovery from a severe population decline: the cautionary case of Bulgarian wolves. Conserv Genet 15(2):405–417. https://doi.org/10.1007/s10592-013-0547-y
Nielsen EE, Bach LA, Kotlicki P (2006) HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Mol Ecol Notes 6:971–973. https://doi.org/10.1111/j.1471-8286.2006.01433.x
Ostrander EA, Sprague GF, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics 16:207–213. https://doi.org/10.1006/geno.1993.1160
Ovsyanikov N, Bibikov DI, Bologov VV (1998) Battling with wolves: Russia’s decades-old struggle to manage its fluctuating wolf population. Int Wolf Center Publ 8(1):16–19
Pacheco C, López-Bao JV, García EJ, Lema FJ, Llaneza L, Palacios V, Godinho R (2017) Spatial assessment of wolf–dog hybridization in a single breeding period. Sci Rep 7:42475. https://doi.org/10.1038/srep42475
Park SDE (2008) MStools v 3.1.1: excel spreadsheet toolkit for data conversion. https://animalgenomics.ucd.ie/sdepark/ms-toolkit/. Accessed 21 Nov 2010
Pilot M, Jędrzejewski W, Branicki W, Sidorovich VE, Jędrzejewska B, Stachura K, Funk SM (2006) Ecological factors influence population genetic structure of European grey wolves. Mol Ecol 15:4533–4553. https://doi.org/10.1111/j.1365-294X.2006.03110.x
Pilot M, Greco C, vonHoldt BM, Randi E, Jędrzejewski W, Sidorovich VE, Konopiński MK, Ostrander EA, Wayne RK (2018) Widespread, long-term admixture between grey wolves and domestic dogs across Eurasia and its implications for the conservation status of hybrids. Evol Appl 11:662–680. https://doi.org/10.1111/eva.12595
Plumer L, Keis M, Remm J, Hindrikson M, Jõgisalu I, Männil P, Kübarsepp M, Saarma U (2016) Wolves recolonizing islands: genetic consequences and implications for conservation and management. PLoS ONE 11(7):e0158911. https://doi.org/10.1371/journal.pone.0158911
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Randi E (2011) Genetics and conservation of wolves Canis lupus in Europe. Mamm Rev 41(2):99–111. https://doi.org/10.1111/j.1365-2907.2010.00176.x
Randi E, Hulva P, Fabbri E, Galaverni M, Galov A, Kusak J, Bigi D, Černá Bolfíková B, Smetanová M, Caniglia R (2014) Multilocus detection of wolf × dog hybridization in Italy, and guidelines for marker selection. PLoS ONE 9(3):e91412. https://doi.org/10.1371/journal.pone.0091412
Randi E, Lucchini V, Christensen MF, Mucci N, Funk S, Dolf G, Loeschke V (2000) Mitochondrial DNA analysis indicates low variability and no hybridization in the Italian wolf but high variability and sporadic hybridization in east European wolves. Conserv Biol 14:1–11
Rutledge LY, White BN, Row JR, Patterson BR (2012) Intense harvesting of eastern wolves facilitated hybridization with coyotes. Ecol Evol 2:19–33. https://doi.org/10.1002/ece3.61
Ryabov LS (1993) Wolves of the black Earth. VGU Publishing, Voronezh (in Russian)
Salvatori V, Godinho R, Braschi C, Boitani L, Ciucci P (2019) High levels of recent wolf × dog introgressive hybridization in agricultural landscapes of central Italy. Eur J Wildl Res 65:73. https://doi.org/10.1007/s10344-019-1313-3
Sastre N, Vila C, Salinas M, Bologov VV, Urios V, Sanchez A, Francino O, Ramırez O (2011) Signatures of demographic bottlenecks in European wolf populations. Conserv Genet 12:701–712. https://doi.org/10.1007/s10592-010-0177-6
Seddon JM, Ellegren H (2004) A temporal analysis shows major histocompatibility complex loci in the Scandinavian wolf population are consistent with neutral evolution. Proc R Soc Lond B 271:2283–2291. https://doi.org/10.1098/rspb.2004.2869
Sillero-Zubiri C, Hoffmann M, Macdonald DW (eds) (2004) Canids: foxes, wolves, jackals and dogs. Status survey and conservation action plan. IUCN/SSC Canid Specialist Group, Gland
Silva P, López-Bao JV, Llaneza L, Álvares F, Lopes S, Ojeda Blanco JC, Cortés YJ, García EJ, Palacios V, Rio-Maior H, Ferrand N, Godinho R (2018) Cryptic population structure reveals low dispersal in Iberian wolves. Sci Rep 8:14108. https://doi.org/10.1038/s41598-018-32369-3
Stronen AV, Jędrzejewska B, Pertoldi C, Demontis D, Randi E, Niedziałkowska M, Pilot M, Sidorovich VE, Dykyy I, Kusak J, Tsingarska E, Kojola I, Karamanlidis AA, Ornicans A, Lobkov VA, Dumenko V, Czarnomska SD (2013) North–south differentiation and a region of high diversity in European wolves (Canis lupus). PLoS ONE 8(10):e76454. https://doi.org/10.1371/journal.pone.0076454
Szewczyk M, Nowak S, Niedźwiecka N, Hulva P, Špinkytė-Bačkaitienė R, Demjanovičová K, Bolfíková BČ, Antal V, Fenchuk V, Figura M, Tomczak P, Stachyra P, Stępniak KM, Zwijacz-Kozica T, Mysłajek RW (2019) Dynamic range expansion leads to establishment of a new, genetically distinct wolf population in Central Europe. Sci Rep 9(1):19003. https://doi.org/10.1038/s41598-019-55273-w
Talala MS, Bondarev AY, Zakharov ES, Politov DV (2020) Genetic differentiation of the wolf Canis lupus L. populations from Siberia at microsatellite loci. Russ J Genet 56(1):59–68. https://doi.org/10.1134/S1022795420010123
Valiere N (2002) GIMLET: a computer program for analyzing genetic individual identification data. Mol Ecol Notes 2:377–379. https://doi.org/10.1046/j.1471-8286.2002.00228.x-i2
Verardi A, Lucchini V, Randi E (2006) Detecting introgressive hybridisation between free-ranging domestic dogs and wild wolves (Canis lupus) by admixture linkage disequilibrium analysis. Mol Ecol 15:2845–2855. https://doi.org/10.1111/j.1365-294X.2006.02995.x
Vilà C, Walker C, Sundqvist AK, Flagstad Ø, Andersone Z, Casulli A, Kojola I, Valdmann H, Halverson J, Ellegren H (2003) Combined use of maternal, paternal and bi-parental genetic markers for the identification of wolf–dog hybrids. Heredity 90:17–24. https://doi.org/10.1038/sj.hdy.6800175
Vilà C, Wayne RK (1999) Hybridization between wolves and dogs. Conserv Biol 13:195–198. https://doi.org/10.1046/j.1523-1739.1999.97425.x
Vorobyevskaya EA, Baldina SN (2011) Altai wolf phylogeography (Canis lupus L.) studied by microsatellite markers. Mosc Univ Biol Sci Bull 66(2):53–54. https://doi.org/10.3103/S0096392511020131(in Russian)
Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756. https://doi.org/10.1111/j.1755-0998.2007.02061.x
Weisman AL, Sitsko AA (2017) Wolf question: options for answers. Russ Ohot Zhurn 2:20–25 (in Russian)
Wozencraft WC (2005) Order Carnivora. In: Wilson DE, Reeder DM (eds) Mammal species of the world. A taxonomic and geographic reference, vol 1, 3rd edn. Johns Hopkins University Press, Baltimore, pp 532–722
Acknowledgements
We thank Professor A. V. Zinoviev, who kindly provided samples from the collection of Tver State University. We also thank all the people who have contributed in some way to the collection of material. Finally, we kindly thank the Associate Editor and the three anonymous reviewers who contributed to deeply improve the manuscript. This work was supported by the Russian Foundation for Basic Research (RFBR) and the Government of Tver region (Grant nos. 14-04-97510; 18-44-690001). Genetic analyses were performed in the Laboratory of Population Genetics of Velikiye Luki State Agricultural Academy and in the Joint Usage Center “Instrumental methods in ecology” at the Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences.
Funding
This work was supported by Russian Foundation for Basic Research (RFBR) and the Government of Tver region (Grant nos. 14-04-97510; 18-44-690001).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest/Competing interest
The authors declare that they have no conflict of interest.
Ethics approval
No animals were killed to provide samples for this study. All samples were obtained directly from licensed hunters. Blood samples from dogs were collected by veterinarians with permission and assistance of the owners.
Consent to participate
All co-authors agree to their participation.
Consent for publication
All co-authors agree to be published.
Additional information
Handling editor: Laura Iacolina.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Korablev, M.P., Korablev, N.P. & Korablev, P.N. Genetic diversity and population structure of the grey wolf (Canis lupus Linnaeus, 1758) and evidence of wolf × dog hybridisation in the centre of European Russia. Mamm Biol 101, 91–104 (2021). https://doi.org/10.1007/s42991-020-00074-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42991-020-00074-2