Continental-scale assessment of the hybrid zone between bobcat and Canada lynx

Biological Conservation

Volumn 178, Issue , 2014, Pages 107-115

  Koen, Erin L ^a,b   Bowman, Jeff ^b   Lalor, Jillian L ^a   Wilson, Paul J ^a  

^a TRENT UNIVERSITY   (Canada)

^b ONTARIO MINISTRY OF NATURAL RESOURCES   (Canada)

Author keywords

Climate change; Hybrid zone; Interspecific hybridization; Introgression; Lynx canadensis; Lynx rufus

Indexed keywords

ADAPTATION; ASSESSMENT METHOD; FELID; FITNESS; GLOBAL WARMING; HYBRIDIZATION; INTROGRESSION; ABUNDANCE; CONSERVATION; EXTINCTION; HETEROSIS; HYBRID ZONE; SYMPATRY; WARMING;

NORTH AMERICA; ALASKA; CANADA; UNITED STATES;

LYNX CANADENSIS; LYNX RUFUS;

EID: 84906345512     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2014.07.016     Document Type: Article

References (76)

1. Allendorf F.W., Leary R.F., Spruell P., Wenburg J.K. The problems with hybrids: setting conservation guidelines. Trends Ecol. Evol. 2001, 16(11):613-622.
2. Anderson E.C., Thompson E.A. A model-based method for identifying species hybrids using multilocus genetic data. Genetics 2002, 160(3):1217-1229.
3. Anderson E.M., Lovallo M.J. Bobcat and Lynx. Wild mammals of North America 2003, vol. II:758-786. Johns Hopkins University Press, Baltimore, Maryland, USA.
4. Austin J.D., Gorman T.A., Bishop D., Moler P. Genetic evidence of contemporary hybridization in one of North America's rarest anurans, the Florida bog frog. Anim. Conserv. 2011, 14(5):553-561.
5. Barton N.H., Hewitt G.M. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 1985, 16:113-148.
6. Beaumont M., Barratt E.M., Gottelli D., Kitchener A.C., Daniels M.J., Pritchard J.K., Bruford M.W. Genetic diversity and introgression in the Scottish wildcat. Mol. Ecol. 2001, 10(2):319-336.
7. Bigelow R.S. Hybrid zones and reproductive isolation. Evolution 1965, 19(4):449-458.
8. Brocke, R.H., Gustafson, K.A., 1992 Lynx in New York State. Cat News, Issue 17. http://lynx.uio.no/lynx/nancy/news/cn17_01.htm.
9. Buskirk S.W., Ruggiero L.F., Krebs C.J. Habitat fragmentation and interspecific competition: Implications for lynx conservation. Ecology and Conservation of Lynx in the United States 1999, 83-100. University Press of Colorado, Boulder. L.F. Ruggerio, J.R. Squires, S.W. Buskirk, K.B. Aubry, K.S. McKelvey, G. Koehler, C.J. Krebs (Eds.).
10. Carmichael L.E., Clark W., Strobeck C. Development and characterization of microsatellite loci from lynx (Lynx canadensis), and their use in other felids. Mol. Ecol. 2000, 9:2197-2198.
11. Carroll C. Interacting effects of climate change, landscape conversion, and harvest on carnivore populations at the range margin: marten and lynx in the northern Appalachians. Conserv. Biol. 2007, 21(4):1092-1104.
12. Devineau O., Shenk T.M., White G.C., Doherty P.F., Lukacs P.M., Kahn R.H. Evaluating the Canada lynx reintroduction programme in Colorado: patterns in mortality. J. Appl. Ecol. 2010, 47(3):524-531.
13. De Vos A. Range changes of mammals in the Great Lakes region. Am. Midl. Nat. 1964, 71(1):210-231.
14. Dobzhansky T. Speciation as a stage in evolutionary divergence. Am. Natural. 1940, 74(753):312-321.
15. Douzery E., Randi E. The mitochondrial control region of Cervidae: evolutionary patterns and phylogenetic content. Mol. Biol. Evol. 1997, 14(11):1154-1166.
16. Dray S., Dufour A.B. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 2007, 22(4):1-20.
17. Earl D.A., vonHoldt B.M. Structure harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conserv. Genet. Resour. 2012, 4(2):359-361.
18. Evanno G., Regnaut S., Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 2005, 14(8):2611-2620.
19. Fitzpatrick B.M., Shaffer H.B. Hybrid vigor between native and introduced salamanders raises new challenges for conservation. Proc. Natl. Acad. Sci. 2007, 104(40):15793-15798.
20. Garroway C.J., Bowman J., Cascaden T.J., Holloway G.L., Mahan C.G., Malcolm J.R., Steele M.A., Turner G., Wilson P.J. Climate change induced hybridization in flying squirrels. Glob. Change Biol. 2010, 16(1):113-121.
21. Gharrett A.J., Smoker W.W., Reisenbichler R.R., Taylor S.G. Outbreeding depression in hybrids between odd-and even-brood year pink salmon. Aquaculture 1999, 173(1):117-129.
22. Gill F.B. Historical aspects of hybridization between blue-winged and golden-winged warblers. Auk 1980, 1-18.
23. Haig S.M., Allendorf F.W. Hybrids and policy. The Endangered Species Act at Thirty, Volume 2: Conserving biodiversity in human-dominated landscapes 2006, 150-163. Island Press, Washington. J.M. Scott, D.D. Goble, F.W. Davis (Eds.).
24. Hedrick P.W. Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol. Ecol. 2013, 22(18):4606-4618.
25. Hoffmann A.A., Sgrò C.M. Climate change and evolutionary adaptation. Nature 2011, 470(7335):479-485.
26. Homyack J.A., Vashon J.H., Libby C., Lindquist E.L., Loch S., McAlpine D.F., Pilgrim K.L., Schwartz M.K. Canada lynx-bobcat (Lynx canadensis×L. rufus) hybrids at the southern periphery of lynx range in Maine, Minnesota and New Brunswick. Am. Midland Natural. 2008, 159(2):504-508.
27. IUCN, 2013. IUCN Red List of Threatened Species. Version 2013.2. 09.04.14. http://www.iucnredlist.org.
28. Jakobsson M., Rosenberg N.A. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 2007, 23(14):1801-1806.
29. Johnson W.E., Onorato D.P., Roelke M.E., Land E.D., Cunningham M., Belden R.C., McBride R., Jansen D., Lotz M., Shindle D., Howard J., Wildt D.E., Penfold L.M., Hostetler J.A., Oli M.K., O'Brien S.J. Genetic restoration of the Florida panther. Science 2010, 329(5999):1641-1645.
30. Jombart T. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 2008, 24:1403-1405.
31. Kidd A.G., Bowman J., Lesbarrères D., Schulte-Hostedde A.I. Hybridization between escaped domestic and wild American mink (Neovison vison). Mol. Ecol. 2009, 18:1175-1186.
32. Koen E.L., Bowman J., Murray D.L., Wilson P.J. Climate change reduces genetic diversity of Canada lynx at the trailing range edge. Ecography 2014, 37(8):754-762.
33. Laliberte A.S., Ripple W.J. Range contractions of North American carnivores and ungulates. Bioscience 2004, 54:123-138.
34. Latch E.K., Kierepka E.M., Heffelfinger J.R., Rhodes O.E. Hybrid swarm between divergent lineages of mule deer (Odocoileus hemionus). Mol. Ecol. 2011, 20(24):5265-5279.
35. Lewontin R.C., Birch L.C. Hybridization as a source of variation for adaptation to new environments. Evolution 1966, 20(3):315-336.
36. Lopez J.V., Cevario S., O'Brien S.J. Complete nucleotide sequences of the domestic cat (Felis catus) mitochondrial genome and a transposed mtDNA tandem repeat (Numt) in the nuclear genome. Genomics 1996, 33(2):229-246.
37. Marshall T.C., Spalton J.A. Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Anim. Conserv. 2000, 3(3):241-248.
38. McKelvey K.S., Aubry K.B., Ortega Y.K. History and distribution of lynx in the contiguous United States. Ecology and Conservation of Lynx in the United States 2000, 207-264. University Press of Colorado, Boulder. L.F. Ruggerio, J.R. Squires, S.W. Buskirk, K.B. Aubry, K.S. McKelvey, G. Koehler, C.J. Krebs (Eds.).
39. Menotti-Raymond M., David V.A., Lyons L.A., Schaffer A.A., Tomlin J.F., Hutton M.K., O'Brien S.J. A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 1999, 57:9-23.
40. Morgan J.A., Harry A.V., Welch D.J., Street R., White J., Geraghty P.T., Macbeth W.G., Tobin A., Simpfendorfer C.A., Ovenden J.R. Detection of interspecies hybridisation in Chondrichthyes: hybrids and hybrid offspring between Australian (Carcharhinus tilstoni) and common (C. limbatus) blacktip shark found in an Australian fishery. Conserv. Genet. 2012, 13(2):455-463.
41. Nielsen E.E., Bach L.A., Kotlicki P. HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Mol. Ecol. Notes 2006, 6(4):971-973.
42. Parmesan C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 2006, 37:637-669.
43. Parmesan C., Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 2003, 421:37-42.
44. Peers M.J.L., Thornton D.H., Murray D.L. Evidence for large-scale effects of competition: niche displacement in carnivores. Proc. R. Soc. Lond. B 2013, 280:20132495.
45. Pierpaoli M., Biro Z.S., Herrmann M., Hupe K., Fernandes M., Ragni B., Szemethy L., Randi E. Genetic distinction of wildcat (Felis silvestris) populations in Europe, and hybridization with domestic cats in Hungary. Mol. Ecol. 2003, 12(10):2585-2598.
46. Price T.D., Bouvier M.M. The evolution of F1 postzygotic incompatibilities in birds. Evolution 2002, 56(10):2083-2089.
47. Pritchard J.K., Stephens M., Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
48. Quinn N.W., Gardner J.F. Relationships of age and sex to lynx pelt characteristics. J. Wildl. Manag. 1984, 48(3):953-956.
49. R Development Core Team, 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (accessed November 2013). http://www.R-project.org.
50. Reding, D.M., 2011. Patterns and processes of spatial genetic structure in a mobile and continuously distributed species, the bobcat (Lynx rufus). Dissertation, Iowa State University.
51. Reding D.M., Bronikowski A.M., Johnson W.E., Clark W.R. Pleistocene and ecological effects on continental-scale genetic differentiation in the bobcat (Lynx rufus). Mol. Ecol. 2012, 21(12):3078-3093.
52. Rhymer J.M., Simberloff D. Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst. 1996, 83-109.
53. Rhymer J.M., Williams M.J., Braun M.J. Mitochondrial analysis of gene flow between New Zealand mallards (Anas platyrhynchos) and grey ducks (A. superciliosa). Auk 1994, 970-978.
54. Riley S.P., Bradley Shaffer H., Randal Voss S., Fitzpatrick B.M. Hybridization between a rare, native tiger salamander (Ambystoma californiense) and its introduced congener. Ecol. Appl. 2003, 13(5):1263-1275.
55. Roberts N.M., Crimmins S.M. Bobcat population status and management in North America: evidence of large-scale population increase. J. Fish Wildlife Manage. 2010, 1(2):169-174.
56. Rosenberg N.A. DISTRUCT: a program for the graphical display of population structure. Mol. Ecol. Notes 2004, 4(1):137-138.
57. Row J.R., Gomez C., Koen E.L., Bowman J., Murray D.L., Wilson P.J. Dispersal promotes high gene flow among Canada lynx populations across North America. Conserv. Genet. 2012, 13(5):1259-1268.
58. Row J.R., Wilson P.J., Gomez C., Koen E.L., Bowman J., Thornton D., Murray D.L. Projecting the impacts of climate change on environmentally-mediated genetic structure in Canada lynx. Glob. Change Biol. 2014, 20(7):2076-2086.
59. Rubidge E.M., Taylor E.B. An analysis of spatial and environmental factors influencing hybridization between native westslope cutthroat trout (Oncorhynchus clarki lewisi) and introduced rainbow trout (O. mykiss) in the upper Kootenay River drainage, British Columbia. Conserv. Genet. 2005, 6(3):369-384.
60. Rueness E.K., Stenseth N.C., O'Donoghue M., Boutin S., Ellegren H., Jakobsen K.S. Ecological and genetic spatial structuring in the Canadian lynx. Nature 2003, 425:69-72.
61. Sanders K.L., Rasmussen A.R., Guinea M.L. High rates of hybridisation reveal fragile reproductive barriers between endangered Australian sea snakes. Biol. Conserv. 2014, 171:200-208.
62. Sanz N., Araguas R.M., Fernández R., Vera M., García-Marín J.L. Efficiency of markers and methods for detecting hybrids and introgression in stocked populations. Conserv. Genet. 2009, 10(1):225-236.
63. Schwartz M.K., Pilgrim K.L., McKelvey K.S., Lindquist E.L., Claar J.J., Loch S., Ruggiero L.F. Hybridization between Canada lynx and bobcats: genetic results and management implications. Conserv. Genet. 2004, 5(3):349-355.
64. Slough B.G. Estimating lynx population age ratio with pelt-length data. Wildl. Soc. Bull. 1996, 495-499.
65. Smith K.L., Hale J.M., Kearney M.R., Austin J.J., Melville J. Molecular patterns of introgression in a classic hybrid zone between the Australian tree frogs, Litoria ewingii and L. paraewingi: evidence of a tension zone. Mol. Ecol. 2013, 22(7):1869-1883.
66. Stebbins C.L. Variation and Evolution in Plants 1950, Columbia University Press, New York.
67. Steeves T.E., Maloney R.F., Hale M.L., Tylianakis J.M., Gemmell N.J. Genetic analyses reveal hybridization but no hybrid swarm in one of the world's rarest birds. Mol. Ecol. 2010, 19(23):5090-5100.
68. Sturtevant A.H. Essays on evolution III. On the origin of interspecific sterility. Q. Rev. Biol. 1938, 13(3):333-335.
69. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
70. Taylor S.A., White T.A., Hochachka W.M., Ferretti V., Curry R.L., Lovette I. Climate-mediated movement of an avian hybrid zone. Curr. Biol. 2014, 24(6):671-676.
71. Trigo T.C., Freitas T.R.O., Kunzler G., Cardoso L., Silva J.C.R., Johnson W.E., O'Brien S.J., Bonatto S.L., Eizirik E. Inter-species hybridization among Neotropical cats of the genus Leopardus, and evidence for an introgressive hybrid zone between L. geoffroyi and L. tigrinus in southern Brazil. Mol. Ecol. 2008, 17(19):4317-4333.
72. Trigo T.C., Schneider A., de Oliveira T.G., Lehugeur L.M., Silveira L., Freitas T.R., Eizirik E. Molecular data reveal complex hybridization and a cryptic species of Neotropical wild cat. Curr. Biol. 2013, 23(24):2528-2533.
73. U.S. Fish and Wildlife Service, 2000. Endangered and threatened wildlife and plants; determination of threatened status for the contiguous U.S. distinct population segment of the Canada lynx and related rule; final rule. 65(58):16052-16086.
74. Vaha J.P., Primmer C.R. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol. Ecol. 2006, 15(1):63-72.
75. Van Oosterhout C., Hutchinson W.F., Wills D.P., Shipley P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 2004, 4(3):535-538.
76. Weaver, J.L., 1999. Lynx survey in the Adirondack Park. Unpublished Report. Wildlife Conservation Society, Bronx, New York.