Ecological factors influence population genetic structure of European grey wolves

Although the mechanisms controlling gene flow among populations are particularly important for evolutionary processes, they are still poorly understood, especially in the case of large carnivoran mammals with extensive continuous distributions. We studied the question of factors affecting population genetic structure in the grey wolf, Canis lupus, one of the most mobile terrestrial carnivores. We analysed variability in mitochondrial DNA and 14 microsatellite loci for a sample of 643 individuals from 59 localities representing most of the continuous wolf range in Eastern Europe. We tested an array of geographical, historical and ecological factors to check whether they may explain genetic differentiation among local wolf populations. We showed that wolf populations in Eastern Europe displayed nonrandom spatial genetic structure in the absence of obvious physical barriers to movement. Neither topographic barriers nor past fragmentation could explain spatial genetic structure. However, we found that the genetic differentiation among local populations was correlated with climate, habitat types, and wolf diet composition. This result shows that ecological processes may strongly influence the amount of gene flow among populations. We suggest natal‐habitat‐biased dispersal as an underlying mechanism linking population ecology with population genetic structure.

[1]  C. Sing,et al.  A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. , 1993, Genetics.

[2]  H. Okarma The trophic ecology of wolves and their predatory role in ungulate communities of forest ecosystems in Europe , 1995 .

[3]  L. Excoffier,et al.  A simulated annealing approach to define the genetic structure of populations , 2002, Molecular ecology.

[4]  Kung-Sik Chan,et al.  Snow conditions may create an invisible barrier for lynx. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[5]  C. Moritz Applications of mitochondrial DNA analysis in conservation: a critical review , 1994 .

[6]  R. Wayne,et al.  Estimating population size by genotyping faeces , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  A Coulon,et al.  Genetic structure is influenced by landscape features: empirical evidence from a roe deer population , 2006, Molecular ecology.

[8]  C. Moritz Defining 'Evolutionarily Significant Units' for conservation. , 1994, Trends in ecology & evolution.

[9]  R. Sokal,et al.  Multiple regression and correlation extensions of the mantel test of matrix correspondence , 1986 .

[10]  A. Jones gerud 2.0: a computer program for the reconstruction of parental genotypes from half‐sib progeny arrays with known or unknown parents , 2005 .

[11]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[12]  S. H. Forbes,et al.  Genetic Structure and Migration in Native and Reintroduced Rocky Mountain Wolf Populations , 1997 .

[13]  Jody Hey,et al.  Principles of population genetics (2nd edn) , 1989 .

[14]  Pierre Legendre,et al.  DISTANCE‐BASED REDUNDANCY ANALYSIS: TESTING MULTISPECIES RESPONSES IN MULTIFACTORIAL ECOLOGICAL EXPERIMENTS , 1999 .

[15]  H. Ernest,et al.  Population structure of California coyotes corresponds to habitat‐specific breaks and illuminates species history , 2004, Molecular ecology.

[16]  B. Patterson,et al.  Contrasting levels of genetic differentiation among populations of wolverines (Gulo gulo) from northern Canada revealed by nuclear and mitochondrial loci , 2004, Conservation Genetics.

[17]  R. Pettifor,et al.  Patterns of nuclear DNA degeneration over time — a case study in historic teeth samples , 2003, Molecular ecology.

[18]  K. Crandall,et al.  Considering evolutionary processes in conservation biology. , 2000, Trends in ecology & evolution.

[19]  P. Beier,et al.  Habitat barriers limit gene flow and illuminate historical events in a wide‐ranging carnivore, the American puma , 2005, Molecular ecology.

[20]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[21]  N. Lehman,et al.  Mitochondrial DNA Variability of the Gray Wolf: Genetic Consequences of Population Decline and Habitat Fragmentation , 1992 .

[22]  Nathaniel Valière gimlet: a computer program for analysing genetic individual identification data , 2002 .

[23]  V. Lucchini,et al.  Evidence of genetic distinction and long‐term population decline in wolves (Canis lupus) in the Italian Apennines , 2004, Molecular ecology.

[24]  SAMUEL B. MERRILL,et al.  Details of Extensive Movements by Minnesota Wolves (Canis lupus) , 2000 .

[25]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[26]  Templeton,et al.  Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history , 1998, Molecular ecology.

[27]  D. Swofford PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[28]  R. Petit,et al.  Identifying Populations for Conservation on the Basis of Genetic Markers , 1998 .

[29]  L. Carbyn,et al.  Wolf Predation on Elk in Riding Mountain National Park, Manitoba , 1983 .

[30]  Arnaud Estoup,et al.  A Spatial Statistical Model for Landscape Genetics , 2005, Genetics.

[31]  J. E. Rice,et al.  Multiple and ancient origins of the domestic dog. , 1997, Science.

[32]  M. Dahlheim,et al.  Low genetic variation among killer whales (Orcinus orca) in the eastern north Pacific and genetic differentiation between foraging specialists. , 1998, The Journal of heredity.

[33]  N. Stenseth,et al.  Ecological and genetic spatial structuring in the Canadian lynx , 2003, Nature.

[34]  K. Crandall,et al.  Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus , 1999, Molecular ecology.

[35]  Pierre Legendre,et al.  An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model , 1999 .

[36]  M. Musiani,et al.  PREY SELECTION AND PREDATION BY WOLVES IN BIAŁOWIEŻA PRIMEVAL FOREST, POLAND , 2000 .

[37]  M. S. Roy,et al.  PHYLOGEOGRAPHIC ANALYSIS OF THE BROODING BRITTLE STAR AMPHIPHOLIS SQUAMATA (ECHINODERMATA) ALONG THE COAST OF NEW ZEALAND REVEALS HIGH CRYPTIC GENETIC VARIATION AND CRYPTIC DISPERSAL POTENTIAL , 2002, Evolution; international journal of organic evolution.

[38]  B. Dale,et al.  Functional response of wolves preying on barren-ground caribou in a multiple-prey ecosystem , 1994 .

[39]  F. Rousset,et al.  ARE PARTIAL MANTEL TESTS ADEQUATE? , 2001, Evolution; international journal of organic evolution.

[40]  L. Waits,et al.  Nuclear DNA microsatellite analysis of genetic diversity and gene flow in the Scandinavian brown bear (Ursus arctos) , 2000, Molecular ecology.

[41]  Arnaud Estoup,et al.  Geneland: a computer package for landscape genetics , 2005 .

[42]  E. Ostrander,et al.  Patterns of differentiation and hybridization in North American wolflike canids, revealed by analysis of microsatellite loci. , 1994, Molecular biology and evolution.

[43]  F. Galibert,et al.  Chromosome-specific single-locus FISH probes allow anchorage of an 1800-marker integrated radiation-hybrid/linkage map of the domestic dog genome to all chromosomes. , 2001, Genome research.

[44]  Sudhir Kumar,et al.  MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment , 2004, Briefings Bioinform..

[45]  H. Ellegren,et al.  Cryptic population structure in a large, mobile mammalian predator: the Scandinavian lynx , 2003, Molecular ecology.

[46]  D. Hartl,et al.  Principles of population genetics , 1981 .

[47]  J. Nagy,et al.  Prey specialization may influence patterns of gene flow in wolves of the Canadian Northwest , 2001, Molecular ecology.

[48]  John C. Avise Molecular Markers, Natural History and Evolution , 1994, Springer US.

[49]  Marti J. Anderson,et al.  Climate and habitat barriers to dispersal in the highly mobile grey wolf , 2004, Molecular ecology.

[50]  J. Neigel,et al.  Demographic influences on mitochondrial DNA lineage survivorship in animal populations , 2005, Journal of Molecular Evolution.

[51]  J. Rine,et al.  Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. , 1993, Genomics.

[52]  L. Mech,et al.  Wolf-prey relations , 2003 .

[53]  J. Avise,et al.  Global population genetic structure and male-mediated gene flow in the green turtle (Chelonia mydas): RFLP analyses of anonymous nuclear loci. , 1992, Genetics.

[54]  G. Johnson,et al.  A polymorphic (AGGAAT)n tandem repeat in an intron of the canine von Willebrand factor gene. , 2009, Animal genetics.

[55]  Ulf Dieckmann,et al.  Speciation along environmental gradients , 2003, Nature.

[56]  L. Mech,et al.  Dispersal of wolves (Canis lupus) in northeastern Minnesota , 1991 .

[57]  K. Crandall,et al.  GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes , 2000, Molecular ecology.

[58]  J. Huelsenbeck,et al.  MRBAYES : Bayesian inference of phylogeny , 2001 .

[59]  Luigi Boitani,et al.  Wolves : behavior, ecology, and conservation , 2003 .

[60]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[61]  V. Loeschcke,et al.  Mitochondrial DNA Variability in Italian and East European Wolves: Detecting the Consequences of Small Population Size and Hybridization , 2000 .

[62]  L. Mech,et al.  Minnesota wolf dispersal to Wisconsin and Michigan , 1995 .

[63]  G. Hewitt Some genetic consequences of ice ages, and their role in divergence and speciation , 1996 .

[64]  O. Liberg,et al.  The recovery, distribution, and population dynamics of wolves on the Scandinavian peninsula, 1978-1998 , 2001 .

[65]  P. Hersteinsson,et al.  Population history and genetic structure of a circumpolar species: the arctic fox , 2004 .

[66]  K. Schmidt,et al.  Genetic diversity and relatedness within packs in an intensely hunted population of wolves Canis lupus , 2005 .

[67]  C. Sing,et al.  A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. , 1992, Genetics.

[68]  R. Gula Influence of snow cover on wolf Canis lupus predation patterns in Bieszczady Mountains, Poland , 2004, Wildlife Biology.

[69]  P. Taberlet,et al.  Comparative phylogeography and postglacial colonization routes in Europe , 1998, Molecular ecology.

[70]  O. Hardy,et al.  spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels , 2002 .

[71]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[72]  J. Woolliams,et al.  What is Genetic Diversity , 2007 .

[73]  F. Potvin,et al.  Wolf diet and prey selectivity during two periods for deer in Quebec: decline versus expansion , 1988 .

[74]  N. Stenseth,et al.  The effect of climatic forcing on population synchrony and genetic structuring of the Canadian lynx. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[75]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[76]  University of Poznan , 1941, Nature.

[77]  S. Nowak,et al.  Wilk i ryś w Polsce - wyniki inwentaryzacji w 2001 roku , 2002 .

[78]  G. Hewitt The genetic legacy of the Quaternary ice ages , 2000, Nature.

[79]  K. Crandall,et al.  TCS: a computer program to estimate gene genealogies , 2000, Molecular ecology.

[80]  H. Ellegren,et al.  Two centuries of the Scandinavian wolf population: patterns of genetic variability and migration during an era of dramatic decline , 2003, Molecular ecology.

[81]  H. Shaffer,et al.  Range‐wide molecular analysis of the western pond turtle (Emys marmorata): cryptic variation, isolation by distance, and their conservation implications , 2005, Molecular ecology.

[82]  Ross Ihaka,et al.  Gentleman R: R: A language for data analysis and graphics , 1996 .

[83]  John C. Avise,et al.  Molecular Markers, Natural History, and Evolution , 1993 .

[84]  Mark P. Miller,et al.  Conflicting patterns of genetic structure produced by nuclear and mitochondrial markers in the Oregon slender salamander (Batrachoseps wrighti): Implications for conservation efforts and species management , 2005, Conservation Genetics.

[85]  S. H. Fritts Record dispersal by a wolf from Minnesota , 1983 .

[86]  J. Dudar,et al.  Technical note: improved DNA extraction from ancient bones using silica-based spin columns. , 1998, American journal of physical anthropology.

[87]  François Rousset,et al.  PARTIAL MANTEL TESTS: REPLY TO CASTELLANO AND BALLETTO , 2002 .

[88]  A. Oskooi Molecular Evolution and Phylogenetics , 2008 .

[89]  L. Boitani,et al.  Wolf Social Ecology , 2003 .

[90]  D. Pletscher,et al.  FACTORS CORRELATED WITH FORAGING BEHAVIOR OF WOLVES IN AND NEAR GLACIER NATIONAL PARK, MONTANA , 2004 .

[91]  M. Gompper,et al.  Predation in Vertebrate Communities: The Bialowieza Primeval Forest as a Case Study , 1998 .

[92]  B. Jędrzejewska,et al.  Wolf Canis lupus numbers, diet and damage to livestock in relation to hunting and ungulate abundance in northeastern Belarus during 1990–2000 , 2003, Wildlife Biology.

[93]  C. Mellersh,et al.  Eighteen canine microsatellites. , 2009, Animal genetics.

[94]  Alan R Templeton,et al.  Statistical phylogeography: methods of evaluating and minimizing inference errors , 2004, Molecular ecology.

[95]  E. Thompson,et al.  Performing the exact test of Hardy-Weinberg proportion for multiple alleles. , 1992, Biometrics.

[96]  Brian H. McArdle,et al.  FITTING MULTIVARIATE MODELS TO COMMUNITY DATA: A COMMENT ON DISTANCE‐BASED REDUNDANCY ANALYSIS , 2001 .

[97]  Dr. Bogumiła Jędrzejewska,et al.  Predation in Vertebrate Communities , 1998, Ecological Studies.