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Population structure and gene flow in a newly harvested gray wolf (Canis lupus) population

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Abstract

The genetic effects of harvest may be especially important in species that form social groups, such as gray wolves (Canis lupus). Though much research exists on the ecology and population dynamics of gray wolves, little research has focused on how anthropogenic harvest relates to the genetics of wolf populations. To analyze the short-term genetic consequences of the first two years of public wolf harvest in Minnesota following delisting under the Endangered Species Act, we genotyped harvested individuals at 18 microsatellite loci and quantified changes in population genetic structure and diversity in the first post-harvest year. If the harvest rate was high enough to create detectable genetic changes, population structure and differentiation between clusters could both increase because of decreased natal dispersal and increased disperser mortality, or they could decrease because of increased immigration from outside the population. In the Minnesota population, heterozygosity and allelic richness were not significantly different between years. However, population genetic structure increased and effective migration decreased among the sampled wolves. While the role of anthropogenic harvest in these changes cannot be distinguished from other confounding factors, this analysis suggests that harvest has a non-negligible effect and indicates the need for continued study to determine whether harvest-induced changes in genetic structure affect the evolutionary trajectory of harvested populations.

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References

  • Adams LG, Stephenson RO, Dale BW et al (2008) Population dynamics and harvest characteristics of wolves in the central Brooks Range, Alaska. Wildl Monogr 170:1–25

    Article  Google Scholar 

  • Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325383

    Article  Google Scholar 

  • Allendorf FW, Hard JJ (2009) Human-induced evolution caused by unnatural selection through harvest of wild animals. Proc Natl Acad Sci 106:9987–9994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allendorf FW, England PR, Luikart G et al (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337

    Article  PubMed  Google Scholar 

  • Andreasen AM, Stewart KM, Longland WS et al (2012) Identification of source-sink dynamics in mountain lions of the Great Basin. Mol Ecol 21:5689–5701

    Article  PubMed  Google Scholar 

  • Ballard WB, Whitman JS, Gardner CL (1987) Ecology of an exploited wolf population in south-central Alaska. Wildl Monogr 98:3–54

    Google Scholar 

  • Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326

    Article  PubMed  PubMed Central  Google Scholar 

  • Benson J, Patterson B, Mahoney P (2014) A protected area influences genotype-specific survival and the structure of a Canis hybrid zone. Ecology 95:254–264

    Article  PubMed  Google Scholar 

  • Boitani L (2003) Wolf conservation and recovery. In: Mech LD, Boitani L (eds) Wolves: behavior, ecology, and conservation. The University of Chicago Press, Chicago, pp 317–340

    Google Scholar 

  • Brainerd SM, Andrén H, Bangs EE et al (2008) The effects of breeder loss on wolves. J Wildl Manag 72:89–98

    Article  Google Scholar 

  • Breen M, Jouquand S, Renier C et al (2001) 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. Genome Res 11:1784–1795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caniglia R, Fabbri E, Galaverni M et al (2014) Noninvasive sampling and genetic variability, pack structure, and dynamics in an expanding wolf population. J Mammal 95:41–59

    Article  Google Scholar 

  • Chenaux-Ibrahim Y (2015) Seasonal diet composition of gray wolves (Canis lupus) in northeastern Minnesota determined by scat analysis. Thesis, University of Minnesota

  • Coltman DW (2008) Molecular ecological approaches to studying the evolutionary impact of selective harvesting in wildlife. Mol Ecol 17:221–235

    Article  PubMed  Google Scholar 

  • Coltman DW, O’Donoghue P, Jorgenson JT et al (2003) Undesirable evolutionary consequences of trophy hunting. Nature 426:655–658

    Article  CAS  PubMed  Google Scholar 

  • Creel S, Becker M, Christianson D et al (2015) Questionable policy for large carnivore hunting. Science 350:1473–1475

    Article  CAS  PubMed  Google Scholar 

  • D’Angelo GJ, Giudice JH (2015) Monitoring population trends of white-tailed deer in Minnesota. Minnesota Department of Natural Resources, St. Paul. http://files.dnr.state.mn.us/wildlife/deer/reports/harvest/popmodel_2015.pdf

  • Delgiudice GD (2014) 2014 Aerial Moose Survey. Minnesota Department of Natural Resources, St. Paul, MN. 6p. http://files.dnr.state.mn.us/wildlife/moose/2014_moosesurvey.pdf

  • Do C, Waples RS, Peel D et al. (2014) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    Article  CAS  PubMed  Google Scholar 

  • Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Erb J, Sampson B (2013) Distribution and abundance of wolves in Minnesota, 2012–2013. Minnesota Department of Natural Resources, Grand Rapids. http://files.dnr.state.mn.us/fish_wildlife/wildlife/wolves/2013/wolfsurvey_2013.pdf

  • Erb J, Humpal C, Sampson B (2014) Minnesota wolf population update 2014. Minnesota Department of Natural Resources, Grand Rapids, 7p. http://files.dnr.state.mn.us/wildlife/wolves/2014/survey_wolf.pdf

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Fenberg FB, Roy K (2008) Ecological and evolutionary consequences of size-selective harvesting: how much do we know? Mol Ecol 17:209–220

    Article  PubMed  Google Scholar 

  • Francisco LV, Langston AA, Mellersh CS et al (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7:359–362

    Article  CAS  PubMed  Google Scholar 

  • Frank SA (1986) Dispersal polymorphism in subdivided populations. J Theor Biol 122:303–309

    Article  CAS  PubMed  Google Scholar 

  • Frankel OH, Soulé ME (1981) Conservation and evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

  • Frantz AC, Cellina S, Krier A et al (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: Clusters or isolation by distance? J Appl Ecol 46:493–505

    Article  Google Scholar 

  • Fredholm M, Winterø AK (1996) Efficient resolution of parentage in dogs by amplification of microsatellites. Anim Genet 27:19–23

    Article  CAS  PubMed  Google Scholar 

  • Fritts SH (1983) Record dispersal by a wolf from Minnesota. J Mammal 64:166–167

    Article  Google Scholar 

  • Fritts SH, Mech LD (1981) Dynamics, movements, and feeding ecology of a newly protected wolf population in northwestern Minnesota. Wildl Monogr 80:3–79

    Google Scholar 

  • Fritts SH, Stephenson RO, Hayes RD, Boitani L (2003) Wolves and humans. In: Mech LD, Boitani L (eds) Wolves: behavior, ecology, and conservation. The University of Chicago Press, Chicago, pp 289–316

    Google Scholar 

  • Fuller TK (1989) Population dynamics of wolves in north-central Minnesota. Wildl Monogr 105:3–41

    Google Scholar 

  • Fuller TK, Berg WE, Radde GL et al (1992) A history and current estimate of wolf distribution and numbers in Minnesota. Wildl Soc Bull 20:42–55

    Google Scholar 

  • Garant D, Forde SE, Hedry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 21:434–443

    Article  Google Scholar 

  • Gese EM, Mech LD (1991) Dispersal of wolves (Canis lupus) in northeastern Minnesota, 1969–1989. Can J Zool 69:2946–2955

    Article  Google Scholar 

  • Getis A, Ord JK (1992) The analysis of spatial association. Geogr Anal 24:189–206

    Article  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): A computer program to calculate F-statistics. J Hered 86:485–486

    Article  Google Scholar 

  • Greenwood PJ, Harvey PH, Perrins CM (1978) Inbreeding and dispersal in the great tit. Nature 271:52–54

    Article  Google Scholar 

  • Grewal SK, Wilson PJ, Kung TK et al (2004) A genetic assessment of the Eastern wolf (Canis lycaon) in Algonquin Provincial Park. J Mammal 85:625–632

    Article  Google Scholar 

  • Grund M (2014) Monitoring population trends of white-tailed deer in Minnesota. Minnesota Department of Natural Resources, St. Paul.http://files.dnr.state.mn.us/wildlife/deer/reports/harvest/popmodel_2014.pdf

  • Guyon R, Lorentzen TD, Hitte C et al (2003) A 1-Mb resolution radiation hybrid map of the canine genome. Proc Natl Acad Sci 100:5296–5301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamilton WD, May RM (1977) Dispersal in stable habitats. Nature 269:578–581

    Article  Google Scholar 

  • Hard JJ, Gross MR, Heino M et al (2008) Evolutionary consequences of fishing and their implications for salmon. Evol Appl 1:388–408

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jędrzejewski W, Branicki W, Veit C et al (2005) Genetic diversity and relatedness within packs in an intensely hunted population of wolves Canis lupus. Acta Theriol 50:3–22

    Article  Google Scholar 

  • Jennions MD, Macdonald DW (1994) Cooperative breeding in mammals. Trends Ecol Evol 9:89–93

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Kimura M, Weiss G (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koblmüller S, Nord M, Wayne RK, Leonard JA (2009) Origin and status of the Great Lakes wolf. Mol Ecol 18:2313–2326

    Article  PubMed  Google Scholar 

  • Koenig WD, Pitelka FA, Carmen WJ et al (1992) The evolution of delayed dispersal in cooperative breeders. Q Rev Biol 67:111–150

    Article  CAS  PubMed  Google Scholar 

  • Koenig WD, Dickinson JL, Emlen ST (2016) Synthesis: Cooperative breeding in the twenty-first century. In: Koenig WD, Dickinson JL (eds) Cooperative breeding in vertebrates: studies of ecology, evolution, and behavior. Cambridge University Press, Cambridge, pp 353–374

    Chapter  Google Scholar 

  • Kuparinen A, Merilä (2007) Detecting and managing fisheries-induced evolution. Trends Ecol Evol 22:652–659

    Article  PubMed  Google Scholar 

  • Lehman N, Clarkson P, Mech LD et al (1992) A study of the genetic relationships within and among wolf packs using DNA fingerprinting and mitochondrial DNA. Behav Ecol Sociobiol 30:83–94

    Article  Google Scholar 

  • McCullough DR (1996) Spatially structured populations and harvest theory. J Wildl Manag 60:1–9

    Article  Google Scholar 

  • Mech LD (1999) Alpha status, dominance, and division of labor in wolf packs. Can J Zool 77:1196–1203

    Article  Google Scholar 

  • Mech LD (2006) Estimated age structure of wolves in Northeastern Minnesota. J Wildl Manag 70:1481–1483

    Article  Google Scholar 

  • Mech LD (2010) Prediction failure of a wolf landscape model. Wildlife Soc B 34:874–877

    Article  Google Scholar 

  • Mech LD, Boitani L (2003) Wolf Social Ecology. In: Mech LD, Boitani L (eds) Wolves: behavior, ecology, and conservation. The University of Chicago Press, Chicago pp 1–34

    Chapter  Google Scholar 

  • Mech LD, Fritts SH, Wagner D (1995) Minnesota wolf dispersal to Wisconsin and Michigan. Am Midl Nat 133:368–370

    Article  Google Scholar 

  • Merrill S, Mech LD (2000) Details of extensive movements by Minnesota wolves (Canis lupus). Am Midl Nat 144:428–433

    Article  Google Scholar 

  • Messier F (1985) Social organization, spatial distribution and population density of wolves in relation to moose density. Can J Zool 63:1068–1077

    Article  Google Scholar 

  • Meyers-Wallen VN, Palmer VL, Acland GM, Hershfield B (1995) Sry-negative XX sex reversal in the American cocker spaniel dog. Mol Reprod Dev 41:300–305

    Article  CAS  PubMed  Google Scholar 

  • Milleret C, Wabakken P, Liberg O et al (2016) Let’s stay together? Intrinsic and extrinsic factors involved in pair bond dissolution in a recolonizing wolf population. J Anim Ecol. doi:10.1111/1365-2656.12587

    PubMed  PubMed Central  Google Scholar 

  • Milner JM, Nilsen JM, Andreassen HP (2007) Demographic side effects of selective hunting in ungulates and carnivores. Conserv Biol 21:36–47

    Article  PubMed  Google Scholar 

  • Mladenoff DJ, Sickley TA, Haight RG, Wydeven AP (1995) A regional landscape analysis and prediction of favorable gray wolf habitat in the northern Great Lakes region. Conserv Biol 9:279–294

    Article  Google Scholar 

  • Mladenoff DJ, Clayton MK, Pratt SD et al (2009) Change in occupied wolf habitat in the northern Great Lakes region. In: Wydeven AP, Van Deelen TR, Heske EJ (eds) Recovery of gray wolves in the Great Lakes region of the United States. Springer Science, New York, pp 119–138

    Chapter  Google Scholar 

  • Murray DL, Smith DW, Bangs EE et al (2010) Death from anthropogenic causes is partially compensatory in recovering wolf populations. Biol Conserv 143:2514–2524

    Article  Google Scholar 

  • Neff MW, Broman KW, Mellersh CS et al (1999) A second-generation genetic linkage map of the domestic dog, Canis familiaris. Genetics 151:803–820

    CAS  PubMed  PubMed Central  Google Scholar 

  • Newby JR, Scott Mills L, Ruth TK et al (2013) Human-caused mortality influences spatial population dynamics: Pumas in landscapes with varying mortality risks. Biol Conserv 159:230–239

    Article  Google Scholar 

  • Olivieri I, Michalakis Y, Gouyon PH (1995) Metapopulation genetics and the evolution of dispersal. Am Nat 146:202–228

    Article  Google Scholar 

  • Ostrander EA, Sprague G, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics 16:207–213

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenALEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petkova D, Novembre J, Stephens M (2014) Visualizing spatial population structure with estimated effective migration surfaces. bioRxiv doi:10.1101/011809

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Rich LN, Mitchell MS, Gude JA, Sime CA (2012) Anthropogenic mortality, intraspecific competition, and prey availability influence territory sizes of wolves in Montana. J Mammal 93:722–731

    Article  Google Scholar 

  • Richman M, Mellersh CS, André C et al (2001) Characterization of a minimal screening set of 172 microsatellite markers for genome-wide screens of the canine genome. J Biochem Biophys Methods 47:137–149

    Article  CAS  PubMed  Google Scholar 

  • Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253

    Article  Google Scholar 

  • Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62

    Article  Google Scholar 

  • Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106.

    Article  PubMed  Google Scholar 

  • Rutledge LY, Patterson BR, Mills KJ et al (2010) Protection from harvesting restores the natural social structure of eastern wolf packs. Biol Conserv 143:332–339

    Article  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  • Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: The effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452

    Article  Google Scholar 

  • Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33

    Article  PubMed  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    Article  PubMed  Google Scholar 

  • Sparkman AM, Waits LP, Murray DL (2011) Social and demographic effects of anthropogenic mortality: a test of the compensatory mortality hypothesis in the red wolf. PLoS ONE 6:e20868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sparkman AM, Adams JR, Steury TD et al (2012) Evidence for a genetic basis for delayed dispersal in a cooperatively breeding canid. Anim Behav 83:1091–1098

    Article  Google Scholar 

  • Stark D, Erb J (2013) 2012 Minnesota wolf season report. Minnesota Department of Natural Resources, Grand Rapids. http://files.dnr.state.mn.us/fish_wildlife/wildlife/wolves/2013/wolfseasoninfo_2012.pdf

  • Stark D, Erb J (2014) 2013 Minnesota wolf season report. Minnesota Department of Natural Resources, Grand Rapids. http://files.dnr.state.mn.us/recreation/hunting/wolf/2013-wolf-season-report.pdf

  • Thiel RP (1985) The relationships between road densities and wolf habitat in Wisconsin. Am Midl Nat 113:404–407

    Article  Google Scholar 

  • Treves A, Martin KA, Wiedenhoeft JE, Wydeven AP (2009) Dispersal of gray wolves in the Great Lakes region. In: Wydeven AP, Van Deelen TR, Heske EJ (eds) Recovery of gray wolves in the Great Lakes region of the United States. Springer Science, New York, pp 191–204

    Chapter  Google Scholar 

  • U.S. Fish and Wildlife Service (2014) Western Great Lakes Distinct Population Segment of the Gray Wolf 2012–2014 Post Delisting Monitoring Annual Report. U.S. Fish and Wildlife Service, Twin Cities Field Office and Midwest Region, Bloomington. https://www.fws.gov/midwest/wolf/monitoring/pdf/Year1PDMReportSept2014.pdf

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Waser PM, Austad SN, Keane B (1986) When should animals tolerate inbreeding? Am Nat 128:529–537

    Article  Google Scholar 

  • Wayne RK, Vilà C (2003) Molecular genetic studies of wolves. In: Mech LD, Boitani L (eds) Wolves: behavior, ecology, and conservation. University of Chicago Press, Chicago, pp 218–238

    Google Scholar 

  • Webb N, Allen J, Merrill E (2011) Demography of a harvested population of wolves (Canis lupus) in west-central Alberta, Canada. Can J Zool 752:744–752

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank the Minnesota Department of Natural Resources for providing the samples used in this study. We would also like to thank D. Petkova and J. Novembre for discussing the use and interpretation of EEMS. Earlier versions of this manuscript were greatly improved by comments from B. Gross, J. Pastor, C. Wagner, and J. Alston. RAM was partially supported by funding from the Minnesota State Environmental and Natural Resources Trust Fund. JLS and JAR were supported by funding from the University of Minnesota- Duluth.

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  1. Jessica A. Rick

    Present address: Department of Botany and Program in Ecology, University of Wyoming, 3165, 1000 E University Ave, Laramie, WY, 82071, USA

Authors and Affiliations

  1. Integrated Biosciences Program, University of Minnesota, Duluth, MN, 55812, USA

    Jessica A. Rick

  2. Department of Biology, University of Minnesota- Duluth, Duluth, MN, 55812, USA

    Jessica A. Rick, Ron A. Moen & Jared L. Strasburg

  3. Natural Resources Research Institute, Duluth, MN, 55811, USA

    Ron A. Moen

  4. Minnesota Department of Natural Resources, Grand Rapids, MN, 55744, USA

    John D. Erb

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Rick, J.A., Moen, R.A., Erb, J.D. et al. Population structure and gene flow in a newly harvested gray wolf (Canis lupus) population. Conserv Genet 18, 1091–1104 (2017). https://doi.org/10.1007/s10592-017-0961-7

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