Appraisal of the consequences of the DDT-induced bottleneck on the level and geographic distribution of neutral genetic variation in Canadian peregrine falcons, Falco peregrinus

Molecular Ecology

Volumn 16, Issue 2, 2007, Pages 327-343

  Brown, Joseph W ^a,c   Van Coeverden De Groot, Peter J ^a   Birt, Tim P ^a   Seutin, Gilles ^b   Boag, Peter T ^a   Friesen, Vicki L ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b PARKS CANADA   (Canada)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Genetic bottleneck; Microsatellite DNA; Mitochondrial DNA; Museum specimens; Peregrine falcons; Systematics

Indexed keywords

CHLORPHENOTANE; MICROSATELLITE DNA; MITOCHONDRIAL DNA; PESTICIDE; PRIMER DNA;

ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CANADA; CLASSIFICATION; CLUSTER ANALYSIS; COMPARATIVE STUDY; DNA SEQUENCE; DRUG EFFECT; ENVIRONMENTAL PROTECTION; FALCONIFORMES; GENETIC VARIABILITY; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POPULATION DYNAMICS; POPULATION GENETICS;

ANIMALS; BASE SEQUENCE; BAYES THEOREM; CANADA; CLUSTER ANALYSIS; CONSERVATION OF NATURAL RESOURCES; DDT; DNA PRIMERS; DNA, MITOCHONDRIAL; FALCONIFORMES; GENETICS, POPULATION; MICROSATELLITE REPEATS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PESTICIDES; POPULATION DYNAMICS; SEQUENCE ANALYSIS, DNA; VARIATION (GENETICS);

FALCO PEREGRINUS; FALCO PEREGRINUS ANATUM; FALCO PEREGRINUS PEALEI; FALCO PEREGRINUS TUNDRIUS;

EID: 33846039231     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2007.03151.x     Document Type: Article

References (108)

1. Barrowclough GF (1982) Geographic variation, predictiveness, and subspecies. Auk, 99, 601-603.
2. Beebe FL (1960) The marine peregrines of the northwest Pacific coast. Condor, 62, 145-189.
3. Beerli P, Felsenstein J (1999) Maximum likelihood estimation of migration rates and population numbers of two populations using a coalescent approach. Genetics, 152, 763-773.
4. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proceedings of the National Academy of Sciences, USA, 98, 4563-4568.
5. Bellinger MR, Johnson JA, Toepfer J, Dunn P (2003) Loss of genetic variation in greater prairie chickens following a population bottleneck in Wisconsin, USA. Conservation Biology, 17, 717-724.
6. Bollmer JL, Kimball RT, Whiteman NK, Sarasola JH, Parker PG (2006) Phylogeography of the Galápagos hawk (Buteo galapagoensis): a recent arrival to the Galápagos Islands. Molecular Phylogenetics and Evolution, 39, 237-247.
7. Bouzat JL (2000) The importance of control populations for the identification and management of genetic diversity. Genetica, 110, 109-115.
8. Brown JW, van Coeverden de Groot PJ, Birt TP, Seutin G, Friesen VL (in review) Comparing temporal estimates of effective population size in a population of peregrine falcons from arctic Canada. Submitted to Conservation Genetics.
9. Burg TM, Gaston AJ, Winkers K, Friesen VL (2005) Rapid divergence and postglacial colonization in western North American Steller's jays (Cyanocitta stelleri). Molecular Ecology, 14, 3745-3755.
10. Burns EL, Eldridge MBD, Houlden BA (2004) Microsatellite variation and population structure in a declining Australian Hylid Litoria aurea. Molecular Ecology, 13, 1745-1757.
11. Byun SA, Koop BF, Reimchen TE (1997) North American black bear mtDNA phylogeography: implications for morphology and the Haida Gwaii glacial refugium controversy. Evolution, 51, 1647-1653.
12. Byun SA, Koop BF, Reimchen TE (1999) Coastal refugia and postglacial recolonization routes: a reply to Demboski, Stone, and Cook. Evolution, 53, 2013-2015.
13. Cade TJ, Enderson JH, Thelander CG, White CM (eds) (1988) Peregrine Falcon Populations: Their Management and Recovery. The Peregrine Fund, Boise,Idaho.
14. Cade TJ, Enderson JH, Kiff LF, White CM (1997) Are there enough good data to justify de-listing the American peregrine falcon? Wilson Bulletin, 25, 730-738.
15. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics, 19, 233-257.
16. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001-2014.
17. Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics, 153, 1989-2000.
18. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution, 15, 290-295.
19. Demboski JR, Stone KD, Cook JA (1999) Further perspectives on the Haida Gwaii glacial refugium. Evolution, 53, 2008-2012.
20. Dinerstein E, McCracken GF (1990) Endangered greater one-horned rhinoceros carry high levels of genetic variation. Conservation Biology, 4, 417-422.
21. Elliott JE, Miller MJ, Wilson LK (2005) Assessing breeding potential of peregrine falcons based on chlorinated hydrocarbon concentrations in prey. Environmental Pollution, 134, 353-361.
22. England PR, Osler GHR, Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (2003) Effects of intense versus diffuse population bottlenecks on microsatellite genetic diversity and evolutionary potential. Conservation Genetics, 4, 595-604.
23. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131, 479-491.
24. Falush D, Stephens M, Pritchard J (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567-1587.
25. Fleming MA, Cook JA (2002) Phylogeography of endemic ermine (Mustela erminea) in southeast Alaska. Molecular Ecology, 11, 795-807.
26. Frankham R (1995) Inbreeding and extinction: a threshold effect. Conservation Biology, 9, 792-799.
27. Frankham R (1998) Inbreeding and extinction: island populations. Conservation Biology, 12, 665-675.
28. Friesen VL, Congdon BC, Walsh HE, Birt TP (1997) Intron variation in marbled murrelets detected using analyses of single-stranded conformational polymorphisms. Molecular Ecology, 6, 1047-1058.
29. Fyfe RW (1969) The peregrine falcon in northern Canada. In: Peregrine Falcon Populations: Their Biology and Decline (ed. Hickey JJ), pp. 101-114. University of Wisconsin press, Madison, Wisconsin.
30. Fyfe RW, Temple SA, Cade TJ (1976) The 1975 North American peregrine falcon survey. Canadian Field Naturalist, 90, 228-273.
31. Fyfe RW, Banasch U, Benavides V, Hilgert de Benavides N, Luscombe A, Sanchez J (1990) Organochlorine residues in potential prey of peregrine falcons, Falco peregrinus, in Latin America. Canadian Field Naturalist, 104, 285-292.
32. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Molecular Ecology, 10, 305-318.
33. Glenn TC, Stephan W, Braun MJ (1999) Effects of a population bottleneck on whooping crane mitochondrial DNA variation. Conservation Biology, 13, 1097-1107.
34. Goudet J, Raymond M, de-Meeus T, Rousset F (1995) Testing differentiation in diploid populations. Genetics, 144, 1933-1940.
35. Groombridge JJ, Jones CG, Bruford MW, Nichols RA (2000) 'Ghost' alleles of the Mauritius kestrel. Nature, 403, 616.
36. Hailer F, Helander B, Folkestad AO et al. (2006) Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biology Letters DOI: 10.1098/rsbl.2006.0453.
37. Harris ML, Wilson LK, Elliott JE, Bishop CA, Tomlin AD, Henning KV (2000) Transfer of DDT and metabolites from fruit orchard soils to American robins (Turdus migratorius) twenty years after agricultural use of DDT in Canada. Archives of Environmental Contamination and Toxicology, 39, 205-220.
38. Hedrick P (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution, 53, 3131-3318.
39. Hickey JJ (ed.) (1969) Peregrine Falcon Populations: Their Biology and Decline. University of Wisconsin press, Madison, Wisconsin.
40. Ibarguchi G, Birt TP, Warheit KI, Boag PT, Friesen VL (2000) Microsatellite loci from common and thick-billed murres, Uria aalge and U. lomvia. Molecular Ecology, 9, 638-639.
41. James FC (1983) Environmental component of morphological differentiation in birds. Science, 221, 184-186.
42. Johnson JA, Toepfer JE, Dunn PO (2003) Contrasting patterns of mitochondrial and microsatellite population structure in fragmented populations of greater prairie-chickens. Molecular Ecology, 12, 3335-3347.
43. Johnson JA, Bellinger MR, Toepfer JE, Dunn P (2004) Temporal changes in allele frequencies and low effective population size in greater prairie-chickens. Molecular Ecology, 13, 2617-2630.
44. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes, 5, 187-189.
45. Langella O (2002) POPULATIONS 1.2.28. Population Genetic Software (Individuals or Populations Distances, Phylogenetic Trees). Available from http://www.cnrs-gif.fr/pge/bioinfo/populations/.
46. Lewis P, Zaykin D (2000) Genetic Data Analysis: Computer Program for the Analysis of Allelic Data, Version 1.0. Available from http://hydrodictyon.eeb.uconn.edu/people/plewis/software.php.
47. Lifjeld JT, Bjørnstad G, Steen OF, Nesje M (2002) Reduced genetic variation in Norwegian peregrine falcons Falco peregrinus indicated by minisatellite DNA fingerprinting. Ibis, 144, E19-E26.
48. Martínez-Cruz B, Godoy JA, Negro JJ (2004) Population genetics after fragmentation: the case of the endangered Spanish imperial eagle (Aquila adalberti). Molecular Ecology, 13, 2243-2255.
49. Maruyama T, Fuerst PA (1984) Population bottlenecks and nonequilibrium models in population genetics. I. Allele numbers when populations evolve from zero variability. Genetics, 108, 745-763.
50. Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics, 111, 675-689.
51. Matocq MD, Villablanca FX (2001) Low genetic diversity in an endangered species: recent or historical pattern? Biological Conservation, 98, 61-68.
52. Mayr E (1982) Of what use are subspecies? Auk, 99, 593-595.
53. McCusker MR, Parkinson E, Taylor EB (2000) Mitochondrial DNA variation in rainbow trout (Oncorhynchus mykiss) across its native range: testing biogeographical hypotheses and their relevance to conservation. Molecular Ecology, 9, 2089-2108.
54. Mesta R (1999) Endangered and threatened wildlife and plants; final rule to remove the American peregrine falcon from the federal list of endangered and threatened wildlife, and to remove the similarity of appearance provision for free-flying Peregrines in the coterminous United States. Federal Register, 64, 46542-46558.
55. Mills LS, Smouse PE (1994) Demographic consequences of inbreeding in remnant populations. American Naturalist, 144, 412-431.
56. Millsap BA, Kennedy PL, Byrd MA, Court G, Enderson JH, Rosenfield RN (1998) Review of the proposal to de-list the American peregrine falcon. Wilson Bulletin, 26, 522-538.
57. Mindell DP, Sorenson MD, Dimcheff DE, Hasegawa M, Ast JC, Yuri T (1999) Interordinal relationships of birds and other reptiles based on whole mitochondrial genomes. Systematic Biology, 48, 138-152.
58. Mora M, Skiles R, McKinney B et al. (2002) Environmental contaminants in prey and tissues of the peregrine falcon in the Big Bend region, Texas, USA. Environmental Pollution, 116, 169-176.
59. Mundy NI, Winchell CS, Burr T, Woodruff DS (1997) Microsatellite variation and microevolution in the critically endangered San Clemente Island loggerhead shrike (Lanius ludovicianus mearnsi). Proceedings of the Royal Society of London. Series B, Biological Sciences, 264, 869-875.
60. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution, 29, 1-10.
61. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. Journal of Molecular Evolution, 19, 153-170.
62. Nesje M, Røed KH, Bell DA, Lindberg P, Lifjeld JT (2000a) Microsatellite analysis of population structure and genetic variability in peregrine falcons (Falco peregrinus). Animal Conservation, 3, 267-275.
63. Nesje M, Røed KH, Lifjeld JT, Lindberg P, Steen OF (2000b) Genetic relationships in the peregrine falcon (Falco peregrinus) analysed by microsatellite DNA markers. Molecular Ecology, 9, 53-60.
64. Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution, 51, 354-362.
65. Nichols RA, Freeman KLM (2004) Using molecular markers with high mutation rates to obtain estimates of relative population size and to distinguish the effects of gene flow and mutation: a demonstration using data from endemic Mauritian skinks. Molecular Ecology, 14, 775-787.
66. Nichols RA, Bruford MW, Groombridge JJ (2001) Sustaining genetic variation in a small population: evidence from the Mauritius kestrel. Molecular Ecology, 10, 593-602.
67. Pagel JE, Bell DA (1997) Reply to Cade et al. regarding de-listing the American peregrine falcon. Wilson Bulletin, 25, 739-742.
68. Pagel JE, Bell DA, Norton BE (1996) De-listing the American peregrine falcon: is it premature? Wilson Bulletin, 24, 429-435.
69. Paxinos EE, James HF, Olson SL, Ballou JD, Leonard JA, Fleischer RC (2002) Prehistoric decline of genetic diversity in the nene. Science, 296, 1827.
70. Phillimore AB, Owens IPF (2006) Are subspecies useful in evolutionary and conservation biology? Proceedings of the Royal Society of London. Series B, Biological Sciences, 273, 1049-1053.
71. Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. Journal of Heredity, 90, 502-503.
72. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. Journal of Heredity, 95, 536-539.
73. Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
74. Purvis A, Gittleman JL, Cowlishaw G, Mace GM (2000) Predicting extinction risk in declining species. Proceedings of the Royal Society of London. Series B, Biological Sciences, 267, 1947-1952.
75. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences, USA, 94, 9197-9201.
76. Ratcliffe D (1967) Decreases in eggshell weight in certain birds of prey. Nature, 215, 208-210.
77. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution, 49, 1280-1283.
78. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conservation Biology, 17, 230-237.
79. Reed JM, Doerr PD, Walters JR (1986) Determining minimum population size for birds and mammals. Wildlife Society Bulletin, 14, 244-261.
80. Rice W (1989) Analyzing tables of statistical tests. Evolution, 43, 223-225.
81. Risebrough RW, Peakall DB (1988) The relative importance of the several organochlorines in the decline of peregrine falcon populations. In: Peregrine Falcon Populations: Their Management and Recovery (eds Cade TJ, Enderson JH, Thelander CG, White CM), pp. 449-462. The Peregrine Fund, Boise, Idaho.
82. Rogers RA, Rogers LA, Hoffmann RS, Martin LD (1991) Native American biological diversity and the biogeographic influence of ice age refugia. Journal of Biogeography, 18, 623-630.
83. Roques S, Negro JJ (2005) mtDNA genetic diversity and population history of a dwindling raptorial bird, the red kite (Milvus milvus). Biological Conservation, 126, 41-50.
84. Rosenberg N (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137-138.
85. Rowell P, Holroyd GL, Banasch U (2003) The 2000 Canadian peregrine falcon survey. Journal of Raptor Research, 37, 98-116.
86. Rozas J, Rozas R (1999) DNASP (version 3): an integrated program for molecular population genetics and molecular evolutionary analysis. Bioinformatics, 15, 174-175.
87. Saccheri I, Kuussaari M, Kanhare M, Vikman P, Fortelius W, Hanksi I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature, 392, 491-494.
88. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406-425.
89. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York.
90. Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN: A Software Package for Population Genetics Data Analysis, Version 2.0. Genetics and Biometry Laboratory, Department of Anthropology, University of Geneva, Switzerland. Available from http://anthro.unige.ch/arlequin/.
91. Schönhuth S, Luikart G, Doadrio I (2003) Effects of a founder event and supplementary introductions on genetic variation in a captive breeding population of the endangered Spanish killifish. Journal of Fish Biology, 63, 1538-1551.
92. Smith CT, Nelson RJ, Wood CC, Koop BF (2001) Glacial biogeography of North American coho salmon (Oncorhynchus kisutch). Molecular Ecology, 10, 2775-2785.
93. Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact. Proceedings of the National Academy of Sciences, USA, 101, 15261-15264.
94. Spong G, Hellborg L (2002) A near-extinction event in lynx: do microsatellites tell the tale? Conservation Ecology, 6, 15.
95. Sunnucks P, Wilson ACC, Beheregaray LB, Zenger K, French J, Taylor AC (2000) SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. Molecular Ecology, 9, 1699-1710.
96. Swem T (1994) Endangered and threatened wildlife and plants; removal of Arctic peregrine falcon from the list of endangered and threatened wildlife. Federal Register, 59, 50796-50805.
97. Tajima J (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
98. Tordoff HB, Redig PT (2001) Role of genetic background in the success of reintroduced peregrine falcons. Conservation Biology, 15, 528-532.
99. Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics, 163, 429-446.
100. Warner BG, Mathewes RF, Clague JJ (1982) Ice-free conditions on the Queen Charlotte Islands, British Columbia, at the height of the late Wisconsin glaciation. Science, 218, 675-677.
101. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
102. Westemeier RL, Brawn JD, Simpson SA et al. (1998) Tracking the long-term decline and recovery of an isolated population. Science, 282, 1695-1698.
103. White CM (1968) Diagnosis and relationships of the North American tundra-inhabiting peregrine falcons. Auk, 85, 179-191.
104. White CM, Boyce DA Jr (1988) An overview of peregrine falcon subspecies. In: Peregrine Falcon Populations: Their Management and Recovery (eds Cade TJ, Enderson JH, Thelander CG, White CM), pp. 789-810. The Peregrine Fund, Boise, Idaho.
105. White CM, Clum NJ, Cade TJ, Hunt WG (2002) Peregrine falcon (Falco peregrinus). In: The Birds of North America, no. 660 (eds Poole A, Gill F). The Birds of North America, Inc, Philadelphia.
106. Wilson EO, Brown WL Jr (1953) The subspecies concept and its taxonomic application. Systematic Zoology, 2, 97-111.
107. Zink RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proceedings of the Royal Society of London. Series B, Biological Sciences, 271, 561-564.
108. Zink RM, Dittmann DL (1993) Gene flow, refugia, and evolution of geographic variation in the song sparrow (Melospiza melodia). Evolution, 47, 717-729.