Wolf population genetics in Europe: a systematic review, meta-analysis and suggestions for conservation and management.
The grey wolf (Canis lupus) is an iconic large carnivore that has increasingly been recognized as an apex predator with intrinsic value and a keystone species. However, wolves have also long represented a primary source of human-carnivore conflict, which has led to long-term persecution of wolves, resulting in a significant decrease in their numbers, genetic diversity and gene flow between populations. For more effective protection and management of wolf populations in Europe, robust scientific evidence is crucial. This review serves as an analytical summary of the main findings from wolf population genetic studies in Europe, covering major studies from the 'pre-genomic era' and the first insights of the 'genomics era'. We analyse, summarize and discuss findings derived from analyses of three compartments of the mammalian genome with different inheritance modes: maternal (mitochondrial DNA), paternal (Y chromosome) and biparental [autosomal microsatellites and single nucleotide polymorphisms (SNPs)]. To describe large-scale trends and patterns of genetic variation in European wolf populations, we conducted a meta-analysis based on the results of previous microsatellite studies and also included new data, covering all 19 European countries for which wolf genetic information is available: Norway, Sweden, Finland, Estonia, Latvia, Lithuania, Poland, Czech Republic, Slovakia, Germany, Belarus, Russia, Italy, Croatia, Bulgaria, Bosnia and Herzegovina, Greece, Spain and Portugal. We compared different indices of genetic diversity in wolf populations and found a significant spatial trend in heterozygosity across Europe from south-west (lowest genetic diversity) to north-east (highest). The range of spatial autocorrelation calculated on the basis of three characteristics of genetic diversity was 650-850 km, suggesting that the genetic diversity of a given wolf population can be influenced by populations up to 850 km away. As an important outcome of this synthesis, we discuss the most pressing issues threatening wolf populations in Europe, highlight important gaps in current knowledge, suggest solutions to overcome these limitations, and provide recommendations for science-based wolf conservation and management at regional and Europe-wide scales.
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia.
Maris
M
Hindrikson
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia.
Jaanus
J
Remm
School of Life Sciences, University of Lincoln, Green Lane, LN6 7DL, Lincoln, UK.
Malgorzata
M
Pilot
CIBIO/InBio - Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, 4485-661, Vairão, Portugal.|Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre s/n, 4169-007, Porto, Portugal.
Raquel
R
Godinho
Department of Chemistry and Bioscience, Section of Biology and Environmental Science, Aalborg University, Fredrik Bajers Vej 7H, DK-9220, Aalborg Øst, Denmark.
Astrid Vik
AV
Stronen
Laboratory of Mammalian Biology, Nature Research Centre, Akademijos 2, 08412, Vilnius, Lithuania.
Laima
L
Baltrūnaité
Mammal Research Institute Polish Academy of Sciences, Waszkiewicza 1, 17-230, Białowieża, Poland.
Sylwia D
SD
Czarnomska
Department of Integrative Ecology, Conservation and Evolutionary Genetics Group, Estación Biológica de Doñana (EBD-CSIC), Avd. Americo Vespucio s/n, 41092, Seville, Spain.
Jennifer A
JA
Leonard
Department of Chemistry and Bioscience, Section of Biology and Environmental Science, Aalborg University, Fredrik Bajers Vej 7H, DK-9220, Aalborg Øst, Denmark.|Laboratorio di Genetica, Istituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA), 40064, Ozzano dell'Emilia, Bologna, Italy.
Ettore
E
Randi
Conservation Genetics Group, Senckenberg Research Institute and Natural History Museum Frankfurt, Clamecystrasse 12, 63571, Gelnhausen, Germany.
Carsten
C
Nowak
Department of Ecology, Grimsö Wildlife Research Station, Swedish University of Agricultural Sciences, SE-730 91, Riddarhyttan, Sweden.
Mikael
M
Åkesson
Research Unit of Biodiversity (UO/CSIC/PA), Oviedo University, 33600, Mieres, Spain.
José Vicente
JV
López-Bao
CIBIO/InBio - Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, 4485-661, Vairão, Portugal.
Francisco
F
Álvares
ARENA Asesores en Recursos Naturales S.L. c/Perpetuo Socorro, n° 12 Entlo 2B, 27003, Lugo, Spain.
Luis
L
Llaneza
Department of Integrative Ecology, Conservation and Evolutionary Genetics Group, Estación Biológica de Doñana (EBD-CSIC), Avd. Americo Vespucio s/n, 41092, Seville, Spain.
Jorge
J
Echegaray
Department of Integrative Ecology, Conservation and Evolutionary Genetics Group, Estación Biológica de Doñana (EBD-CSIC), Avd. Americo Vespucio s/n, 41092, Seville, Spain.
Carles
C
Vilà
Latvian State Forest Research Institute "Silava", Rigas iela 111, LV-2169, Salaspils, Latvia.
Janis
J
Ozolins
Latvian State Forest Research Institute "Silava", Rigas iela 111, LV-2169, Salaspils, Latvia.
Dainis
D
Rungis
Department of Genetics and Physiology, University of Oulu, 90014, Oulu, Finland.
Jouni
J
Aspi
Department of Phytology, Faculty of Forestry, Technical University, T.G. Masaryk str. 24, SK-96053, Zvolen, Slovakia.
Ladislav
L
Paule
Department of Biology, Biotechnical Faculty, University of Ljubljana, Vecna pot 111, 1000, Ljubljana, Slovenia.
Tomaž
T
Skrbinšek
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia.
Urmas
U
Saarma
D000818:Animals; D003247:Conservation of Natural Resources; D005060:Europe; D014644:Genetic Variation; D005828:Genetics, Population; D018895:Microsatellite Repeats / Q000235:genetics; D019596:Wolves / Q000235:genetics*
Canis lupus; European Union policy; SNP; Y chromosome; conservation genomics; gene flow; large carnivores; microsatellites; mitochondrial DNA; wolf management