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Conservation Genetics

, Volume 18, Issue 5, pp 1091–1104 | Cite as

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

  • Jessica A. RickEmail author
  • Ron A. Moen
  • John D. Erb
  • Jared L. Strasburg
Research Article

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.

Keywords

Canis lupus Population genetics Hunting Dispersal Gene flow 

Notes

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.

Supplementary material

10592_2017_961_MOESM1_ESM.docx (2.3 mb)
Supplementary material 1 (DOCX 2368 KB)

References

  1. Adams LG, Stephenson RO, Dale BW et al (2008) Population dynamics and harvest characteristics of wolves in the central Brooks Range, Alaska. Wildl Monogr 170:1–25CrossRefGoogle Scholar
  2. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325383CrossRefGoogle Scholar
  3. Allendorf FW, Hard JJ (2009) Human-induced evolution caused by unnatural selection through harvest of wild animals. Proc Natl Acad Sci 106:9987–9994CrossRefPubMedPubMedCentralGoogle Scholar
  4. Allendorf FW, England PR, Luikart G et al (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337CrossRefPubMedGoogle Scholar
  5. Andreasen AM, Stewart KM, Longland WS et al (2012) Identification of source-sink dynamics in mountain lions of the Great Basin. Mol Ecol 21:5689–5701CrossRefPubMedGoogle Scholar
  6. Ballard WB, Whitman JS, Gardner CL (1987) Ecology of an exploited wolf population in south-central Alaska. Wildl Monogr 98:3–54Google Scholar
  7. Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326CrossRefPubMedPubMedCentralGoogle Scholar
  8. Benson J, Patterson B, Mahoney P (2014) A protected area influences genotype-specific survival and the structure of a Canis hybrid zone. Ecology 95:254–264CrossRefPubMedGoogle Scholar
  9. 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 317–340Google Scholar
  10. Brainerd SM, Andrén H, Bangs EE et al (2008) The effects of breeder loss on wolves. J Wildl Manag 72:89–98CrossRefGoogle Scholar
  11. 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 11:1784–1795CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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 95:41–59CrossRefGoogle Scholar
  13. Chenaux-Ibrahim Y (2015) Seasonal diet composition of gray wolves (Canis lupus) in northeastern Minnesota determined by scat analysis. Thesis, University of MinnesotaGoogle Scholar
  14. Coltman DW (2008) Molecular ecological approaches to studying the evolutionary impact of selective harvesting in wildlife. Mol Ecol 17:221–235CrossRefPubMedGoogle Scholar
  15. Coltman DW, O’Donoghue P, Jorgenson JT et al (2003) Undesirable evolutionary consequences of trophy hunting. Nature 426:655–658CrossRefPubMedGoogle Scholar
  16. Creel S, Becker M, Christianson D et al (2015) Questionable policy for large carnivore hunting. Science 350:1473–1475CrossRefPubMedGoogle Scholar
  17. 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
  18. 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
  19. 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 14:209–214CrossRefPubMedGoogle Scholar
  20. Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  21. 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
  22. 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
  23. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  24. 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 10:564–567CrossRefPubMedGoogle Scholar
  25. Fenberg FB, Roy K (2008) Ecological and evolutionary consequences of size-selective harvesting: how much do we know? Mol Ecol 17:209–220CrossRefPubMedGoogle Scholar
  26. Francisco LV, Langston AA, Mellersh CS et al (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7:359–362CrossRefPubMedGoogle Scholar
  27. Frank SA (1986) Dispersal polymorphism in subdivided populations. J Theor Biol 122:303–309CrossRefPubMedGoogle Scholar
  28. Frankel OH, Soulé ME (1981) Conservation and evolution. Cambridge University Press, CambridgeGoogle Scholar
  29. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  30. 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 46:493–505CrossRefGoogle Scholar
  31. Fredholm M, Winterø AK (1996) Efficient resolution of parentage in dogs by amplification of microsatellites. Anim Genet 27:19–23CrossRefPubMedGoogle Scholar
  32. Fritts SH (1983) Record dispersal by a wolf from Minnesota. J Mammal 64:166–167CrossRefGoogle Scholar
  33. Fritts SH, Mech LD (1981) Dynamics, movements, and feeding ecology of a newly protected wolf population in northwestern Minnesota. Wildl Monogr 80:3–79Google Scholar
  34. 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 289–316Google Scholar
  35. Fuller TK (1989) Population dynamics of wolves in north-central Minnesota. Wildl Monogr 105:3–41Google Scholar
  36. Fuller TK, Berg WE, Radde GL et al (1992) A history and current estimate of wolf distribution and numbers in Minnesota. Wildl Soc Bull 20:42–55Google Scholar
  37. Garant D, Forde SE, Hedry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 21:434–443CrossRefGoogle Scholar
  38. Gese EM, Mech LD (1991) Dispersal of wolves (Canis lupus) in northeastern Minnesota, 1969–1989. Can J Zool 69:2946–2955CrossRefGoogle Scholar
  39. Getis A, Ord JK (1992) The analysis of spatial association. Geogr Anal 24:189–206CrossRefGoogle Scholar
  40. Goudet J (1995) FSTAT (version 1.2): A computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  41. Greenwood PJ, Harvey PH, Perrins CM (1978) Inbreeding and dispersal in the great tit. Nature 271:52–54CrossRefGoogle Scholar
  42. Grewal SK, Wilson PJ, Kung TK et al (2004) A genetic assessment of the Eastern wolf (Canis lycaon) in Algonquin Provincial Park. J Mammal 85:625–632CrossRefGoogle Scholar
  43. 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
  44. Guyon R, Lorentzen TD, Hitte C et al (2003) A 1-Mb resolution radiation hybrid map of the canine genome. Proc Natl Acad Sci 100:5296–5301CrossRefPubMedPubMedCentralGoogle Scholar
  45. Hamilton WD, May RM (1977) Dispersal in stable habitats. Nature 269:578–581CrossRefGoogle Scholar
  46. Hard JJ, Gross MR, Heino M et al (2008) Evolutionary consequences of fishing and their implications for salmon. Evol Appl 1:388–408CrossRefPubMedPubMedCentralGoogle Scholar
  47. Harris RB, Wall WA, Allendorf FW (2002) Genetic consequences of hunting: what do we know and what should we do? Wildl Soc Bull 30:634–643Google Scholar
  48. 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 23:1801–1806CrossRefPubMedGoogle Scholar
  49. 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 50:3–22CrossRefGoogle Scholar
  50. Jennions MD, Macdonald DW (1994) Cooperative breeding in mammals. Trends Ecol Evol 9:89–93CrossRefPubMedGoogle Scholar
  51. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  52. Kimura M, Weiss G (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576PubMedPubMedCentralGoogle Scholar
  53. Koblmüller S, Nord M, Wayne RK, Leonard JA (2009) Origin and status of the Great Lakes wolf. Mol Ecol 18:2313–2326CrossRefPubMedGoogle Scholar
  54. Koenig WD, Pitelka FA, Carmen WJ et al (1992) The evolution of delayed dispersal in cooperative breeders. Q Rev Biol 67:111–150CrossRefPubMedGoogle Scholar
  55. 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 353–374CrossRefGoogle Scholar
  56. Kuparinen A, Merilä (2007) Detecting and managing fisheries-induced evolution. Trends Ecol Evol 22:652–659CrossRefPubMedGoogle Scholar
  57. 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 30:83–94CrossRefGoogle Scholar
  58. McCullough DR (1996) Spatially structured populations and harvest theory. J Wildl Manag 60:1–9CrossRefGoogle Scholar
  59. Mech LD (1999) Alpha status, dominance, and division of labor in wolf packs. Can J Zool 77:1196–1203CrossRefGoogle Scholar
  60. Mech LD (2006) Estimated age structure of wolves in Northeastern Minnesota. J Wildl Manag 70:1481–1483CrossRefGoogle Scholar
  61. Mech LD (2010) Prediction failure of a wolf landscape model. Wildlife Soc B 34:874–877CrossRefGoogle Scholar
  62. 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 1–34CrossRefGoogle Scholar
  63. Mech LD, Fritts SH, Wagner D (1995) Minnesota wolf dispersal to Wisconsin and Michigan. Am Midl Nat 133:368–370CrossRefGoogle Scholar
  64. Merrill S, Mech LD (2000) Details of extensive movements by Minnesota wolves (Canis lupus). Am Midl Nat 144:428–433CrossRefGoogle Scholar
  65. Messier F (1985) Social organization, spatial distribution and population density of wolves in relation to moose density. Can J Zool 63:1068–1077CrossRefGoogle Scholar
  66. Meyers-Wallen VN, Palmer VL, Acland GM, Hershfield B (1995) Sry-negative XX sex reversal in the American cocker spaniel dog. Mol Reprod Dev 41:300–305CrossRefPubMedGoogle Scholar
  67. 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 PubMedPubMedCentralGoogle Scholar
  68. Milner JM, Nilsen JM, Andreassen HP (2007) Demographic side effects of selective hunting in ungulates and carnivores. Conserv Biol 21:36–47CrossRefPubMedGoogle Scholar
  69. 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 9:279–294CrossRefGoogle Scholar
  70. 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 119–138CrossRefGoogle Scholar
  71. Murray DL, Smith DW, Bangs EE et al (2010) Death from anthropogenic causes is partially compensatory in recovering wolf populations. Biol Conserv 143:2514–2524CrossRefGoogle Scholar
  72. Neff MW, Broman KW, Mellersh CS et al (1999) A second-generation genetic linkage map of the domestic dog, Canis familiaris. Genetics 151:803–820PubMedPubMedCentralGoogle Scholar
  73. 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 159:230–239CrossRefGoogle Scholar
  74. Olivieri I, Michalakis Y, Gouyon PH (1995) Metapopulation genetics and the evolution of dispersal. Am Nat 146:202–228CrossRefGoogle Scholar
  75. Ostrander EA, Sprague G, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics 16:207–213CrossRefPubMedGoogle Scholar
  76. Peakall R, Smouse PE (2012) GenALEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  77. Petkova D, Novembre J, Stephens M (2014) Visualizing spatial population structure with estimated effective migration surfaces. bioRxiv doi: 10.1101/011809 Google Scholar
  78. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  79. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  80. 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 93:722–731CrossRefGoogle Scholar
  81. 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 47:137–149CrossRefPubMedGoogle Scholar
  82. Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253CrossRefGoogle Scholar
  83. Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62CrossRefGoogle Scholar
  84. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106.CrossRefPubMedGoogle Scholar
  85. Rutledge LY, Patterson BR, Mills KJ et al (2010) Protection from harvesting restores the natural social structure of eastern wolf packs. Biol Conserv 143:332–339CrossRefGoogle Scholar
  86. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234CrossRefPubMedGoogle Scholar
  87. Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: The effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452CrossRefGoogle Scholar
  88. Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33CrossRefPubMedGoogle Scholar
  89. Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573CrossRefPubMedGoogle Scholar
  90. 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:e20868CrossRefPubMedPubMedCentralGoogle Scholar
  91. Sparkman AM, Adams JR, Steury TD et al (2012) Evidence for a genetic basis for delayed dispersal in a cooperatively breeding canid. Anim Behav 83:1091–1098CrossRefGoogle Scholar
  92. 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
  93. 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
  94. Thiel RP (1985) The relationships between road densities and wolf habitat in Wisconsin. Am Midl Nat 113:404–407CrossRefGoogle Scholar
  95. 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 191–204CrossRefGoogle Scholar
  96. 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
  97. 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 4:535–538CrossRefGoogle Scholar
  98. Waser PM, Austad SN, Keane B (1986) When should animals tolerate inbreeding? Am Nat 128:529–537CrossRefGoogle Scholar
  99. 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 218–238Google Scholar
  100. Webb N, Allen J, Merrill E (2011) Demography of a harvested population of wolves (Canis lupus) in west-central Alberta, Canada. Can J Zool 752:744–752CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Jessica A. Rick
    • 1
    • 2
    • 3
    Email author
  • Ron A. Moen
    • 2
    • 4
  • John D. Erb
    • 5
  • Jared L. Strasburg
    • 2
  1. 1.Integrated Biosciences ProgramUniversity of MinnesotaDuluthUSA
  2. 2.Department of BiologyUniversity of Minnesota- DuluthDuluthUSA
  3. 3.Department of Botany and Program in EcologyUniversity of WyomingLaramieUSA
  4. 4.Natural Resources Research InstituteDuluthUSA
  5. 5.Minnesota Department of Natural ResourcesGrand RapidsUSA

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