Genetic diversity and structure in Canadian northern leopard frog (Rana pipiens) populations: Implications for reintroduction programs

Canadian Journal of Zoology

Volumn 86, Issue 8, 2008, Pages 863-874

  Wilson, G A ^a,c   Fulton, T L ^a   Kendell, K ^b   Scrimgeour, G ^b   Paszkowski, C A ^a   Coltman, D W ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b Alberta Conservation Association   (Canada)

^c ENVIRONMENT CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EVOLUTION; FROG; GENETIC DIFFERENTIATION; GENETIC STRUCTURE; GENETIC VARIATION; HABITAT FRAGMENTATION; POPULATION DECLINE; POPULATION GENETICS; REINTRODUCTION; TRANSLOCATION;

ALBERTA; CANADA; NORTH AMERICA;

ANURA; FELIDAE; RANA PIPIENS;

EID: 49249095010     PISSN: 00084301     EISSN: None     Source Type: Journal    
DOI: 10.1139/Z08-062     Document Type: Article

References (96)

1. Alberta Sustainable Resource Development. 2003. Status of the northern leopard frog (Rana pipiens) in Alberta: update 2003. Wildlife Status Report No. 9 (update 2003). Alberta Sustainable Resource Development, Fish and Wildlife Division, and Alberta Conservation Association, Edmonton.
2. Allendorf, F.W., and Luikart, G. 2007. Conservation and the genetics of populations. Blackwell Publishing, Malden, Mass.
3. Barber, P.H. 1999. Patterns of gene flow and population genetic structure in the canyon treefrog, Hyla arenicolor (Cope). Mol. Ecol. 8: 563-576. doi:10.1046/j.1365-294x.1999.00594.x. PMID: 10327657.
4. Beebee, T.J.C., and Rowe, G. 2000. Microsatellite analysis of natterjack toad Bufo calamita Laurenti populations: consequences of dispersal from a Pleistocene refugium. Biol. J. Linn. Soc. 69: 367-381. doi:10.1006/bijl.1999.0368.
5. Berven, K.A. 1990. Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology, 71: 1599-1608. doi:10.2307/1938295.
6. Blaustein, A.R., Wake, D.B., and Sousa, W.P. 1994. Amphibian declines: judging stability, persistence, and susceptibility of populations to local and global extinctions. Conserv. Biol. 8: 60-71. doi:10.1046/j.1523-1739. 1994.08010060.x.
7. Bradford, D.F. 1989. Allotropic distribution of native frogs and introduced fishes in high Sierra Nevada lakes of California: implication of the negative effect of fish introductions. Copeia, 1989: 775-778. doi:10.2307/1445515.
8. Canestrelli, D., Cimmaruta, R., Costantini, V., and Nascetti, G. 2006. Genetic diversity and phylogeography of the Apennine yellow-bellied toad Bombina pachypus, with implications for conservation. Mol. Ecol. 15: 3741-3754. doi:10.1111/j.1365-294X.2006.03055.x. PMID:17032271.
9. Conant, S. 1988. Saving endangered species by translocation: are we tinkering with evolution? BioScience, 38: 254-257. doi:10.2307/1310848.
10. Corander, J., and Marttinen, P. 2006. Bayesian identification of admixture events using multilocus molecular markers. Mol. Ecol. 15: 2833-2843. doi:10.1111/j.1365-294X.2006.02994.x. PMID:16911204.
11. Corn, P.S., and Fogleman, J.C. 1984. Extinction of montane populations of the northern leopard frog (Rana pipiens) in Colorado. J. Herpetol. 18: 147-152. doi:10.2307/1563742.
12. Cornuet, J.M., and Luikart, G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144: 2001-2014. PMID:8978083.
13. Daszak, P., Berger, L., Cunningham, A.A., Hyatt, A.D., Green, D.E., and Speare, R. 1999. Emerging infectious diseases and amphibian population declines. Emerg. Infect. Dis. 5: 735-748. PMID:10603206.
14. Denton, J.S., Hitchings, S.P., Beebee, T.J.C., and Gent, A. 1997. A recovery program for the natterjack toad (Bufo calamita) in Britain. Conserv. Biol. 11: 1329-1338. doi:10.1046/j.1523-1739. 1997.96318.x.
15. Dobzhansky, T. 1970. Genetics of the evolutionary process. Columbia University Press, New York.
16. Dole, J.W. 1971. Dispersal of recently metamorphosed leopard frogs, Rana pipiens. Copeia, 1971: 221-228. doi:10.2307/1442821.
17. Driscoll, D.A. 1998. Genetic structure of the frogs Geocrinia lutea and Geocrinia rosea reflects extreme population divergence and range changes, not dispersal barriers. Evolution, 52: 1147-1157. doi:10.2307/2411244.
18. Evanno, G., Regnaut, S., and Goudet, J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14: 2611-2620. doi:10.1111/j.1365-294X.2005.02553.x. PMID:15969739.
19. Fischer, J., and Lindenmayer, D.B. 2000. An assessment of the published results of animal relocations. Biol. Conserv. 96: 1-11. doi:10.1016/S0006-3207(00)00048-3.
20. Fisher, C. 1999. Feasibility of northern leopard frog translocations in Alberta: a review of physiological, ecological, methodological requirements for successful repatriations and results from field investigations. Alberta Environment, Fisheries, and Wildlife Management Division, Edmonton.
21. Fitzsimmons, N.N., Buskirk, S.W., and Smith, M.H. 1995. Population history, genetic variability, and horn growth in bighorn sheep. Conserv. Biol. 9: 314-323. doi:10.1046/j.1523-1739. 1995.9020314.x.
22. Funk, W.C., Blouin, M.S., Corn, P.S., Maxell, B.A., Pilliod, D.S., Amish, S., and Allendorf, F.W. 2005. Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol. Ecol. 14: 483-496. doi:10.1111/j.1365-294X.2005.02426.x. PMID:15660939.
23. Garza, J.C., and Williamson, E.G. 2001. Detection of reduction in population size using data from microsatellite loci. Mol. Ecol. 10: 305-318. doi:10.1046/j.1365-294X.2001.01190.x. PMID:11298947.
24. Gonzalez, A., Lawton, J.H., Gilbert, F.S., Blackburn, T.M., and Evans-Freke, I. 1998. Metapopulation dynamics, abundance, and distribution in a microecosystem. Science (Washington, D.C.), 281: 2045-2047. doi:10.1126/science.281.5385.2045. PMID:9748167.
25. Goudet, J. 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. J. Hered. 86: 485-486.
26. Griffith, B., Scott, J.M., Carpenter, J.W., and Reed, C. 1989. Translocation as a species conservation tool - status and strategy. Science (Washington, D.C.), 245: 477-480. doi:10.1126/science. 245.4917.477. PMID:17750257.
27. Guillot, G., Mortier, F., and Estoup, A. 2005. GENELAND: a computer package for landscape genetics. Mol. Ecol. Notes, 5: 712-715. doi:10.1111/j.1471-8286.2005.01031.x.
28. Halverson, M.A., Skelly, D.K., and Caccone, A. 2006. Inbreeding linked to amphibian survival in the wild but not in the laboratory. J. Hered. 97: 499-507. doi:10.1093/jhered/esl019. PMID:16957048.
29. Hedrick, P.W., Hedgecock, D., Hamelberg, S., and Croci, S.J. 2000. The impact of supplementation in winter-run chinook salmon on effective population size. J. Hered. 91: 112-116. doi:10. 1093/jhered/91.2.112. PMID:10768123.
30. Hewitt, G.M. 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58: 247-276. doi:10.1006/bijl.1996.0035.
31. Hewitt, G.M. 1999. Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68: 87-112. doi:10.1006/bijl.1999.0332.
32. Hine, R.L., Les, B.L., and Hellmich, B.F. 1981. Leopard frog populations and mortality in Wisconsin, 1974-1976. Wis. Dep. Nat. Resour. Tech. Bull. 122.
33. Hoffman, E.A., and Blouin, M.S. 2004a. Historical data refute recent range contraction as cause of low genetic diversity in isolated frog populations. Mol. Ecol. 13: 271-276. doi:10.1046/j.1365-294X.2003.02057. x. PMID:14717886.
34. Hoffman, E.A., and Blouin, M.S. 2004b. Evolutionary history of the northern leopard frog: reconstruction of phylogeny, phylogeography, and historical changes in population demography from mitochondrial DNA. Evolution, 58: 145-159. doi:10.1554/02-584. PMID:15058727.
35. Hoffman, E.A., Ardren, W.R., and Blouin, M.S. 2003. Nine polymorphic microsatellite loci for the northern leopard frog (Rana pipiens). Mol. Ecol. Notes, 3: 115-116. doi:10.1046/j.1471-8286.2003.00371.x.
36. Hoffman, E.A., Schueler, F.W., and Blouin, M.S. 2004. Effective population sizes and temporal stability of genetic structure in Rana pipiens, the northern leopard frog. Evolution, 58: 2536-2545. doi:10.1111/j.0014-3820.2004.tb00882.x. PMID:15612296.
37. Hutchinson, D.W., and Templeton, A.R. 1999. Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution, 53: 1898-1914.
38. Ibrahim, K.M., Nichols, R.A., and Hewitt, G.M. 1996. Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity, 77: 282-291. doi:10.1038/hdy.1996.142.
39. James, S.M., Little, E.E., and Semlitsch, R.D. 2004. The effect of soil composition and hydration on the bioavailability and toxicity of cadmium to hibernating juvenile American toads (Bufo americanus). Environ. Pollut. 132: 523-532. doi:10.1016/j.envpol.2004.05.005. PMID:15325468.
40. Jehle, R., Wilson, G.A., Arntzen, J.W., and Burke, T. 2005a. Contemporary gene flow and the spatio-temporal genetic structure of subdivided newt populations (Triturus cristatus, T. marmoratus). J. Evol. Biol. 18: 619-628. doi:10.1111/j.1420-9101.2004.00864.x. PMID:15842491.
41. Jehle, R., Burke, T., and Arntzen, J.W. 2005b. Delineating finescale genetic units in amphibians: probing the primacy of ponds. Conserv. Genet. 6: 227-234. doi:10.1007/s10592-004-7832-8.
42. Jensen, J.L., Bohonak, A.J., and Kelley, S.T. 2005. Isolation by distance, web service. BMC Genet. 6: 13. doi:10.1186/1471-2156-6-13. PMID:15760479.
43. Kendell, K. 2002. Alberta inventory for the northern leopard frog (2000/2001). Alberta species at risk report No. 44. Alberta Sustainable Resource Development, Fish and Wildlife Division, Edmonton.
44. Kendell, K. 2004. Northern leopard frog recovery program: year 5 (2003). Available from Alberta Conservation Association, Edmonton.
45. Kendell, K., Stevens, S., and Prescott, D. 2007. Alberta Northern Leopard Survey, 2005. Tech. Rep. D-2006-000. Alberta Conservation Association, Edmonton.
46. Kimberling, D.N., Ferreira, A.R., Shuster, S.M., and Keim, P. 1996. RAPD marker estimation of genetic structure among isolated northern leopard frog populations in the south-western USA. Mol. Ecol. 5: 521-529. doi:10.1111/j.1365-294X.1996.tb00344.x. PMID:8794561.
47. Lacy, R.C. 1997. Importance of genetic variation to the viability of mammalian populations. J. Mammal. 78: 320-335. doi:10.2307/1382885.
48. La Marca, E., Lips, K.R., Lotters, S., Puschendorf, R., Ibanez, R., Rueda-Almonacid, J.V., Schulte, R., Marty, C., Castro, F., Manzanilla-Puppo, J., Garcia-Perez, J.E., Bolanos, F., Chaves, G., Pounds, J.A., Toral, E., and Young, B.E. 2005. Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica, 37: 190-201. doi:10.1111/j.1744-7429.2005.00026.x.
49. Lampert, K.P., Rand, A.S., Mueller, U.G., and Ryan, M.J. 2003. Fine-scale genetic pattern and evidence for sex-biased dispersal in the tungara frog, Physalaemus pustulosus. Mol. Ecol. 12: 3325-3334. doi:10.1046/j.1365-294X.2003.02016.x. PMID:14629349.
50. Lannoo, M.K., Lang, K., Waltz, T., and Philips, G.S. 1994. An altered amphibian assemblage: Dickson County, Iowa, 70 years after Frank Blanchard's survey. Am. Midl. Nat. 131: 311-319. doi:10.2307/2426257.
51. Latch, E.K., Harveson, L.A., King, J.S., Hobson, M.D., and Rhodes, O.E. 2006. Assessing hybridization in wildlife populations using molecular markers: a case study in wild turkeys. J. Wildl. Manag. 70: 485-492. doi:10.2193/0022-541X(2006) 70[485:AHIWPU]2.0.CO;2.
52. Lenormand, T. 2002. Gene flow and the limits to natural selection. Trends Ecol. Evol. 17: 183-189. doi:10.1016/S0169-5347(02)02497-7.
53. Leonard, W.P., McAllister, K.R., and Friesz, R.C. 1999. Survey and assessment of northern leopard frog (Rana pipiens) populations in Washington State. Northwest. Nat. 80: 51-60. doi:10.2307/3536929.
54. Lode, T., Holveck, M.J., and Lesbarreres, D. 2005. Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina. Biol. J. Linn. Soc. 86: 191-200. doi:10.1111/j.1095-8312.2005.00521.x.
55. Merrell, D.J. 1968. A comparison of the estimated and the effective size of breeding populations of the leopard frog. Evolution, 22: 274-283. doi:10.2307/2406526.
56. Merrell, D.J. 1977. Life history of the leopard frog, Rana pipiens, in Minnesota. Occas. Pap. 15. Bell Museum of Natural History, University of Minnesota, Minneapolis.
57. Metts, B.S., Hopkins, W.A., and Nestor, J.P. 2005. Interaction of an insecticide with larval density in pond-breeding salamanders (Ambystoma). Freshw. Biol. 50: 685-696. doi:10.1111/j.1365-2427.2005.01342.x.
58. Monsen, K.J., and Blouin, M.S. 2003. Genetic structure in a montane ranid frog: restricted gene flow and nuclear-mitochondrial discordance. Mol. Ecol. 12: 3275-3286. doi:10.1046/j.1365-294X.2003.02001.x. PMID:14629345.
59. Monsen, K.J., and Blouin, M.S. 2004. Extreme isolation by distance in a montane frog Rana cascadae. Conserv. Genet. 5: 827-835. doi:10.1007/s10592-004-1981-z.
60. Newman, R.A., and Squire, T. 2001. Microsatellite variation and fine-scale population structure in the wood frog (Rana sylvatica). Mol. Ecol. 10: 1087-1100. doi:10.1046/j.1365-294X.2001.01255.x. PMID:11380868.
61. Packer, C., Pusey, A.E., Rowley, H., Gilbert, D.A., Martenson, J., and O'Brien, S.J. 1991. Case study of a population bottleneck - lions of the Ngorongoro Crater. Conserv. Biol. 5: 219-230. doi:10.1111/j.1523-1739. 1991.tb00127.x.
62. Palkovacs, E.P., Oppenheimer, A.J., Gladyshev, E., Toepfer, J.E., Amato, G., Chase, T., and Caccone, A. 2004. Genetic evaluation of a proposed introduction: the case of the greater prairie chicken and the extinct heath hen. Mol. Ecol. 13: 1759-1769. doi:10.1111/j.1365-294X.2004.02181.x. PMID:15189201.
63. Peakall, R., and Smouse, P.E. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes, 6: 288-295. doi:10.1111/j.1471-8286.2005.01155.x.
64. Petit, R.J., El Mousadik, A., and Pons, O. 1998. Identifying populations for conservation on the basis of genetic markers. Conserv. Biol. 12: 844-855. doi:10.1046/j.1523-1739.1998.96489.x.
65. Pritchard, J.K., Stephens, M., and Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics, 155: 945-959 PMID:10835412.
66. Raymond, M., and Rousset, F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249.
67. Reed, D.H., and Frankham, R. 2003. Correlation between fitness and genetic diversity. Conserv. Biol. 17: 230-237. doi:10.1046/j.1523-1739. 2003.01236.x.
68. Rhymer, J.M., and Simberloff, D. 1996. Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst. 27: 83-109. doi:10.1146/annurev. ecolsys.27.1.83.
69. Rice, W.R. 1989. Analyzing tables of statistical tests. Evolution, 43: 223-225. doi:10.2307/2409177.
70. Roberts, W.E. 1981. What happened to the leopard frog? Alta. Nat. 11: 1-4.
71. Roberts, W.E. 1987. The northern leopard frog - endangered in Alberta. In Proceedings of the Workshop on Endangered Species in the Prairie Provinces. Edited by G.L. Holroyd, W.B. McGillivray, P.H.R. Stepney, D.M. Ealey, G.C. Trottier, and K.E. Ederhart. Occas. Pap. 9. Provincial Museum of Alberta Natural History, Edmonton. pp. 137-138.
72. Roelke, M.E., Martenson, J.S., and O'Brien, S.J. 1993. The consequences of demographic reduction and genetic depletion in the endangered Florida Panther. Curr. Biol. 3: 340-350. doi:10. 1016/0960-9822(93)90197-V. PMID:15335727.
73. Romanchuk, K.A., and Quinlan, R.W. 2006. Magrath northern leopard frog reintroduction project: final report. Alberta species at risk report No. 104. Alberta Sustainable Resource Development, Fish and Wildlife Division, Edmonton.
74. Rowe, G., and Beebee, T.J.C. 2007. Defining population boundaries: use of three Bayesian approaches with microsatellite data from British natterjack toads (Bufo calamita). Mol. Ecol. 16: 785-796. doi:10.1111/j.1365-294X.2006.03188.x. PMID:17284211.
75. Russell, W.C., Thorne, E.T., Oakleaf, R., and Ballou, J.D. 1994. The genetic basis of black-footed ferret reintroduction. Conserv. Biol. 8: 263-266. doi:10.1046/j.1523-1739.1994.08010263.x.
76. Saccheri, I., Kuussaari, M., Kankare, M., Vikman, P., Fortelius, W., and Hanski, I. 1998. Inbreeding and extinction in a butterfly metapopulation. Nature (London), 392: 491-494. doi:10.1038/33136.
77. Sarrazin, F., and Legendre, S. 2000. Demographic approach to releasing adults versus young in reintroductions. Conserv. Biol. 14: 488-500. doi:10.1046/j.1523-1739.2000.97305.x.
78. Scribner, K.T., Arntzen, J.W., and Burke, T. 1997. Effective number of breeding adults in Bufo bufo estimated from age-specific variation at minisatellite loci. Mol. Ecol. 6: 701-712. doi:10.1046/j.1365-294X.1997. 00238.x. PMID:9262012.
79. Seburn, C.N.L., and Seburn, D.C. 1998. COSEWIC status report on the northern leopard frog, Rana pipiens, in Canada (western population). Committee on the Status of Endangered Wildlife in Canada, Ottawa, Ont.
80. Seburn, C.N.L., Seburn, D.C., and Paszkowski, C.A. 1997. Northern leopard frog (Rana pipiens) dispersal in relation to habitat. In Amphibians in decline: Canadian studies of a global problem. Edited by D.M. Green. Herpetological conservation. Vol. 1. Society for the Study of Amphibians and Reptiles, St. Louis, Mo. pp. 64-72.
81. Seddon, P.J., Armstrong, D.P., and Maloney, R.F. 2007. Developing the science of reintroduction biology. Conserv. Biol. 21: 303-312. doi:10.1111/j.1523-1739.2006.00627.x. PMID:17391180.
82. Seppa, P., and Laurila, A. 1999. Genetic structure of island populations of the anurans Rana temporaria and Bufo bufo. Heredity, 82: 309-317. doi:10.1038/sj.hdy.6884900. PMID:10336706.
83. Shaffer, G., Fellers, G.M., Magee, A., and Voss, R. 2000. The genetics of amphibian declines: population substructure and molecular differentiation in the Yosemite toad, Bufo canorus (Anura, Bufonidae) based on single-strand conformation polymorphism analysis (SSCP) and mitochondrial DNA sequence data. Mol. Ecol. 9: 245-257. doi:10.1046/j.1365-294x.2000.00835.x. PMID:10736023.
84. Soule, M. 1987. Viable populations for conservation. Cambridge University Press, Cambridge, U.K.
85. Squire, T., and Newman, R.A. 2002. Fine-scale population structure in the wood frog (Rana sylvatica) in a northern woodland. Herpetologica, 58: 119-130. doi:10.1655/0018-0831(2002)058[0119:FPSITW]2.0.CO;2.
86. Stuart, S.N., Chanson, J.S., Cox, N.A., Young, B.E., Rodrigues, A.S.L., Fischman, D.L., and Waller, R.W. 2004. Status and trends of amphibian declines and extinctions worldwide. Science (Washington, D.C.), 306: 1783-1786. doi:10.1126/science.1103538. PMID:15486254.
87. Swofford, D.L. 2003. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Inc., Sunderland, Mass.
88. Vieites, D.R., Nieto-Roman, S., Barluenga, M., Palanca, A., Vences, M., and Meyer, A. 2004. Post-mating clutch piracy in an amphibian. Nature (London), 431: 305-308. doi:10.1038/nature02879. PMID:15372032.
89. Vredenburg, V.T. 2004. Reversing introduced species effects: experimental removal of introduced fish leads to rapid recovery of a declining frog. Proc. Natl. Acad. Sci. U.S.A. 101: 7646-7650. doi:10.1073/pnas.0402321101. PMID:15136741.
90. Wagner, G. 1997. Status of the northern leopard frog in Alberta. Alberta Environmental Protection, Wildlife Management Division, Edmonton.
91. Waples, R.S. 1991. Genetic interactions between hatchery and wild salmonids: lessons from the Pacific Northwest. Can. J. Fish. Aquat. Sci. 48(Suppl. 1): 124-133. doi:10.1139/f91-311.
92. Weir, B.S., and Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38: 1358-1370. doi:10.2307/2408641.
93. Werner, J.K. 2003. Status of the northern leopard frog Rana pipiens in western Montana. Northwest. Nat. 84: 24-30. doi:10.2307/3536719.
94. Wilson, G.A., Fulton, T.L., Kendell, K., Schock, D.M., Paszkowski, C.A., and Coltman, D.W. 2008. Genetic evidence for single season polygyny in the northern leopard frog (Rana pipiens). Herpetol. Rev. 39: 46-50.
95. Wolf, C.M., Griffith, B., Reed, C., and Temple, S.A. 1996. Avian and mammalian translocations: update and reanalysis of 1987 survey data. Conserv. Biol. 10: 1142-1154. doi:10.1046/j.1523-1739.1996.10041142.x.
96. Wright, S. 1978. Evolution and the genetics of populations. Volume 4: variability within and among natural populations. University of Chicago Press, Chicago.