Population genetic structure of gray wolves (Canis lupus) in a marine archipelago suggests island-mainland differentiation consistent with dietary niche

Annals of Occupational and Environmental Medicine

Astrid V Stronen⁵  Erin L Navid¹  Michael S Quinn²  Paul C Paquet³  Heather M Bryan⁴  Christopher T Darimont⁴ 

[1] Faculty of Environmental Design, University of Calgary, 2500 University Dr. NW, Calgary, Alberta T2N 1 N4, Canada

[2] Institute for Environmental Sustainability, Mount Royal University, 4825 Mount Royal Gate SW, Calgary, Alberta T3E 6 K6, Canada

[3] Raincoast Conservation Foundation, PO Box 86 Denny Island, British Columbia V0T 1B0, Canada

[4] Hakai Beach Institute, Box 309, Heriot Bay, British Columbia V0P 1H0, Canada

[5] Department of Biotechnology, Chemistry and Environmental Engineering, Aalborg University, Sohngaardsholmsvej 57, Aalborg 9000, Denmark

关键词: Wolf;    Traditional ecological knowledge;    Population genetic structure;    Niche;    Marine resources;    Ecological divergence;    Canis lupus;   

Others  :  834655
DOI  :  10.1186/1472-6785-14-11

 received in 2013-09-25, accepted in 2014-04-15,  发布年份 2014

【 摘 要 】

Background

Emerging evidence suggests that ecological heterogeneity across space can influence the genetic structure of populations, including that of long-distance dispersers such as large carnivores. On the central coast of British Columbia, Canada, wolf (Canis lupus L., 1758) dietary niche and parasite prevalence data indicate strong ecological divergence between marine-oriented wolves inhabiting islands and individuals on the coastal mainland that interact primarily with terrestrial prey. Local holders of traditional ecological knowledge, who distinguish between mainland and island wolf forms, also informed our hypothesis that genetic differentiation might occur between wolves from these adjacent environments.

Results

We used microsatellite genetic markers to examine data obtained from wolf faecal samples. Our results from 116 individuals suggest the presence of a genetic cline between mainland and island wolves. This pattern occurs despite field observations that individuals easily traverse the 30 km wide study area and swim up to 13 km among landmasses in the region.

Conclusions

Natal habitat-biased dispersal (i.e., the preference for dispersal into familiar ecological environments) might contribute to genetic differentiation. Accordingly, this working hypothesis presents an exciting avenue for future research where marine resources or other components of ecological heterogeneity are present.

【 授权许可】

   
2014 Stronen et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Bowen BW, Karl SA: Population genetics and phylogeography of sea turtles. Mol Ecol 2007, 16:4886-4907.
• [2]André C, Larsson LC, Laikre L, Bekkevold D, Brigham D, Carvalho GR, Dahlgren TG, Hutchinson WF, Mariani S, Mudde K, Ruzzante DE, Ryman N: Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs putatively selected loci. Heredity 2011, 106:270-280.
• [3]Milano I, Babbucci M, Cariani A, Atanassova M, Bekkevold D, Carvalho GR, Espiñeira M, Fiorentino F, Garofalo G, Geffen AJ, Hansen JH, Helyar SJ, Nielsen EE, Ogden R, Patarnello T, Stagioni M, Tinti F, Bargelloni L, FishPopTrace Consortium: Outlier markers reveal fine-scale genetic structuring across European hake populations (Merluccius merluccius). Mol Ecol 2014, 23:118-135.
• [4]Hoelzel AR, Hey J, Dahlheim M, Nicholson C, Burkanov V, Black N: Evolution of population structure in a highly social top predator, the killer whale. Mol Biol Evol 2007, 24:1407-1415.
• [5]McRae BH, Beier P, Dewald LE, Huynh LY, Keim P: Habitat barriers limit gene flow and illuminate historical events in a wide-ranging carnivore, the American puma. Mol Ecol 2005, 14:1965-1977.
• [6]Rueness EK, Stenseth NC, O’Donoghue M, Boutin S, Ellegren H, Jacobsen KS: Ecological and genetic spatial structuring in the Canadian lynx. Nature 2003, 425:69-72.
• [7]Sacks BN, Brown SK, Ernest HB: Population structure of California coyotes corresponds to habitat-specific breaks and illuminates species history. Mol Ecol 2004, 13:1265-1275.
• [8]Musiani M, Leonard JA, Cluff HD, Gates CC, Mariani S, Paquet PC, Vilà C, Wayne RK: Differentiation of tundra and boreal coniferous forest wolves: genetics, coat color and association with migratory caribou. Mol Ecol 2007, 16:4149-4170.
• [9]Pilot M, Jędrzejewski W, Sidorovich VE, Meier-Augustein W, Hoelzel AR: Dietary differentiation and the evolution of population genetic structure in a highly mobile carnivore. PLoS ONE 2012, 7:e39341.
• [10]Weckworth BV, Talbot S, Sage GK, Person DK, Cook J: A signal for independent coastal and continental histories among North American wolves. Mol Ecol 2005, 14:917-931.
• [11]Weckworth BV, Talbot SL, Cook JA: Phylogeography of wolves (Canis lupus) in the Pacific Northwest. J Mammal 2010, 91:363-375.
• [12]Weckworth BV, Dawson NG, Talbot SL, Flamme MJ, Cook JA: Going Coastal: Shared evolutionary history between Coastal British Columbia and Southeast Alaska wolves (Canis lupus). PLoS ONE 2011, 6:e19582.
• [13]Muñoz-Fuentes V, Darimont CT, Wayne RK, Paquet PC, Leonard JA: Ecological factors drive differentiation in wolves from British Columbia. J Biogeogr 2009, 36:1516-1531.
• [14]Davis JM, Stamps JA: The effect of natal experience on habitat preferences. Trends Ecol Evol 2004, 19:411-416.
• [15]Nosil P, Vines TH, Funk DJ: Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 2005, 59:705-719.
• [16]Edelaar P, Siepielski AM, Clobert J: Matching habitat choice causes direct gene flow: a neglected dimension in evolution and ecology. Evolution 2008, 62:2462-2472.
• [17]Darimont CT, Paquet PC: The gray wolves, Canis lupus, of British Columbia’s central and north coast: distribution and conservation assessment. Can Field-Nat 2002, 116:416-422.
• [18]Paquet PC, Alexander SM, Swan PL, Darimont CT: The influence of natural landscape fragmentation and resource availability on connectivity and distribution of marine gray wolf populations on the Central Coast, British Columbia, Canada. In Connectivity Conservation. Edited by Crooks K, Sanjayan MA. Cambridge: Cambridge University Press; 2006:130-156.
• [19]Darimont CT, Paquet PC, Reimchen TE: Spawning salmon disrupt trophic coupling between wolves and ungulate prey in coastal British Columbia. BMC Ecol 2008, 8:14. BioMed Central Full Text
• [20]Darimont CT, Paquet PC, Reimchen TE: Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. J Anim Ecol 2009, 78:126-133.
• [21]Darimont CT, Price MHH, Winchester NN, Gordon-Walker J, Paquet PC: Predators in natural fragments: foraging ecology of wolves in British Columbia’s central and north coast archipelago. J Biogeogr 2004, 31:1867-1877.
• [22]Bryan HM, Darimont CT, Hill JE, Paquet PC, Thompson RCA, Wagner B, Smits JE: Seasonal and biogeographical patterns of gastrointestinal parasites in large carnivores: wolves in a coastal archipelago. Parasitology 2012, 139:781-790.
• [23]Navid EL: Examination of genotyping success and population genetic structure of wolves in coastal British Columbia using non-invasive molecular markers. University of Calgary, Calgary: Faculty of Environmental Design; 2009. [MSc thesis]
• [24]Darimont CT: Ecological and evolutionary causes and consequences of intra-population variability in foraging niche; predator and prey in a marine archipelago. University of Victoria, Victoria: Department of Biology; 2007. [PhD dissertation]
• [25]McAllister I, Darimont CT: The Last Wild Wolves. Berkeley: University of California Berkeley Press; 2007. [Ghosts of the Rainforest]
• [26]Breen M, Jouquand S, Renier C, Mellersh CS, Hitte C, Holmes NG, Chéron A, Suter N, Vignaux F, Bristow AE, Priat C, McCann E, André C, Boundy S, Gitsham P, Thomas R, Bridge WL, Spriggs HF, Ryder EJ, Curson A, Sampson J, Ostrander EA, Binns MM, Galibert F: 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 2001, 11:1784-1795.
• [27]Guyon R, Lorentzen TD, Hitte C, Kim L, Cadieu E, Parker HG, Quignon P, Lowe JK, Renier C, Gelfenbeyn B, Vignaux F, DeFrance HB, Gloux S, Mahairas GG, André C, Galibert F, Ostrander EA: A 1-Mb resolution radiation hybrid map of the canine genome. Proc Natl Acad Sci USA 2003, 100:5296-5301.
• [28]Neff MW, Broman KW, Mellersh CS, Ray K, Acland GM, Aguirre GD, Ziegle JS, Ostrander EA, Rine J: A second-generation genetic linkage map of the domestic dog, Canis familiaris. Genetics 1999, 151:803-820.
• [29]Sundquist AK, Ellegren H, Olivier M, Vilà C: Y-chromosome haplotyping in Scandinavian wolves (Canis lupus) based on microsatellite markers. Mol Ecol 2001, 10:1959-1966.
• [30]Park SDE: Trypanotolerance in West African cattle and the population genetic effects of selection. University of Dublin, Dublin: Smurfit Institute of Genetics; 2001. [PhD dissertation]
• [31]van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P: MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 2004, 4:535-538.
• [32]Nei M: Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 1978, 89:583-590.
• [33]Raymond M, Rousset F: Genepop (version 1.2): Population genetics software for exact tests and ecuminiscism. J Hered 1995, 86:248-249.
• [34]Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F: GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Montpellier (France): Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II; 2004.
• [35]Weir BS, Cockerham CC: Estimating F-statistics for the analyses of population structure. Evolution 1984, 38:1358-1370.
• [36]Guo SW, Thompson EA: Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 1992, 48:361-372.
• [37]Verhoeven KJF, Simonsen KL, McIntyre LM: Implementing false discovery rate control: Increasing your power. Oikos 2005, 108:643-647.
• [38]Jombart T: adegenet: a R package for the multivariate analysis of genetic markers. Biochem Genet 2008, 10:149-163.
• [39]R Development Core Team: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2012. ISBN 3-900051-07-0. [http://www.R-project.org/ webcite]
• [40]Jombart T, Devillard S, Durfour A-B: Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 2008, 101:92-103.
• [41]Peakall R, Smouse PE: GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 2012, 28:2537-2539.
• [42]Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H: Vegan: Community Ecology Package. 2013. R-package version 2.0-10. http://CRAN.R-project.org/package=vegan webcite
• [43]Carmichael LE, Krizan J, Nagy JA, Dumond M, Johnson D, Veitch A, Strobeck C: Northwest passages: conservation genetics of Arctic Island wolves. Conserv Genet 2008, 9:879-892.
• [44]Santini A, Lucchini V, Fabbri E, Randi E: Ageing and environmental factors affect PCR success in wolf (Canis lupus) extremental DNA samples. Mol Ecol Notes 2007, 7:955-961.
• [45]Mech LD, Boitani L: Introduction. In Wolves: Behaviour, Ecology and Conservation . Edited by Mech LD, Boitani L. Chicago: University of Chicago Press; 2003. xv-xvii
• [46]Klein DR: The introduction, increase, and demise of wolves on Coronation Island, Alaska. In Ecology and conservation of wolves in a changing world. Edited by Carbyn LN, Fritts SH, Seip DR. Edmonton: Canadian Circumpolar Institute, Occasional Publication No. 35; 1995:275-280.
• [47]Mech LD, Boitani L: Wolf social ecology. In Wolves: Behaviour, Ecology and Conservation . Edited by Mech LD, Boitani L. Chicago: University of Chicago Press; 2003:1-34.
• [48]Palsbøll PJ, Bérubé M, Allendorf FW: Identification of management units using population genetic data. Trends Ecol Evol 2006, 22:11-16.
• [49]Turner NJ, Ignace MB, Ignace R: Traditional ecological knowledge and wisdom of aboriginal peoples in British Columbia. Ecol Appl 2000, 10:1275-1287.
• [50]Person DK, Kirchhoff M, Van Ballenberghe V, Iverson GC, Grossman E: The Alexander Archipelago wolf: a conservation assessment. Portland, OR: U.S: Department of Agriculture, Forest Service, Pacific Research Station; 1996. [Gen. Tech. Rep. PNW-GTR-384]
• [51]Shields GF, Adams D, Garner G, Labelle M, Pietsch J, Ramsay M, Schwartz C, Titus K, Williamson S: Phylogeography of Mitochondrial DNA Variation in Brown Bears and Polar Bears. Mol Phylogenet Evol 2000, 15:319-326.