Advertisement

Conservation Genetics

, Volume 8, Issue 6, pp 1287–1309 | Cite as

Conservation genetics of snowy plovers (Charadrius alexandrinus) in the Western Hemisphere: population genetic structure and delineation of subspecies

  • W. Chris Funk
  • Thomas D. Mullins
  • Susan M. Haig
Research Article

Abstract

We examined the genetic structure of snowy plovers (Charadrius alexandrinus) in North America, the Caribbean, and the west coast of South America to quantify variation within and among breeding areas and to test the validity of three previously recognized subspecies. Sequences (676 bp) from domains I and II of the mitochondrial control region were analyzed for 166 snowy plovers from 20 breeding areas. Variation was also examined at 10 microsatellite loci for 144 snowy plovers from 14 breeding areas. The mtDNA and microsatellite data provided strong evidence that the Puerto Rican breeding group is genetically divergent from sites in the continental U.S. (net sequence divergence = 0.38%; F ST for microsatellites = 0.190). Our data also revealed high levels of differentiation between sites from South America and North America (net sequence divergence = 0.81%; F ST for microsatellites = 0.253). In contrast, there was little genetic structure among breeding sites within the continental U.S. Our results suggest that snowy plovers in Florida should be considered part of C. a. nivosus (rather than part of C. a. tenuirostris, where they are currently placed), whereas snowy plovers from Puerto Rico should be considered part of C. a. tenuirostris. Snowy plovers in South America should remain a separate subspecies (C. a. occidentalis). Although U.S. Pacific and Gulf Coast breeding areas were not genetically distinct from other continental U.S. sites, demographic isolation, unique coastal habitats, and recent population declines suggest they warrant special concern.

Keywords

Snowy plover Microsatellites MtDNA Subspecies Population structure 

Notes

Acknowledgements

We thank A. Archuleta, K. Brennan, S. Cardiff, K. Castelein, M. Colwell, B. Cosler, D. Dittmann, R. Estelle, K. Fahy, J. Gerwin, L. Gorman, S. Hackett, C. Hallet, L. Hanauska, D. Lauten, A. Musche, M.P. Nieto, G. Page, A. Powell, P. Sanzenbacher, M. Stern, R. Swift, O. Taft, J. Van Remsen, J. Whittier, and D. Wilson for collecting tissue samples. Logistical support was provided by Cabo Rojo, Lower Rio Grande Valley, Quivira, and Willapa Bay National Wildlife Refuges, Florida Game and Fresh Water Fish Commission, Florida Division of Recreation and Parks, Gulf Island National Seashore, Eglin Air Force Base, Louisiana Museum of Natural History, Texas Parks and Wildlife Division, Inland Sea Shorebird Reserve, Bureau of Land Management Salt Lake District Office, Utah Division of Wildlife Resources, and Summer Lake Wildlife Area. We are grateful to C. Küpper for sharing primer sequences; B. Bowen, E. Elliott-Smith, S. Oyler-McCance, S. Talbot, and two anonymous reviewers for providing comments on earlier drafts of this paper; P. Martin for discussions regarding subspecies issues; and USFWS (regions 1 and 4), USGS Forest and Rangeland Ecosystem Science Center, and the USGS Science Support Program for providing funding for this work. Views expressed in this paper are the authors’ and do not necessarily reflect the view of the USGS.

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automatic Control 19:716–723CrossRefGoogle Scholar
  2. Amadon D (1949) The seventy-five percent rule for subspecies. Condor 51:250–258CrossRefGoogle Scholar
  3. American Ornithologists’ Union (1957) Check-list of North American birds, 5th edn. American Ornithologists’ Union, Washington, DCGoogle Scholar
  4. Ball RM, Avise JC (1992) Mitochondrial DNA phylogeographic differentiation among avian populations and the evolutionary significance of subspecies. Auk 109:626–636Google Scholar
  5. Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744PubMedCrossRefGoogle Scholar
  6. Barrowclough TG, Vogler AP (2000) Detecting the geographical pattern of speciation from species-level phylogenies. Am Nat 155:419–434CrossRefGoogle Scholar
  7. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Nat Acad Sci USA 98:4563–4568PubMedCrossRefGoogle Scholar
  8. Benedict NG, Oyler-McCance SJ, Taylor SE, Braun CE, Quinn TW (2003) Evaluation of the eastern (Centrocercus u. urophasianus) and western (Centrocercus urophasianus phaios) subspecies of sage-grouse using mitochondrial control-region sequence data. Conserv Gen 4:301–310CrossRefGoogle Scholar
  9. Bhagabati NK, Brown JL, Bowen BS (2004) Geographic variation in Mexican Jays (Aphelocoma ultramarina): local differentiation, polyphyly, or hybridization? Mol Ecol 13:2721–2734PubMedCrossRefGoogle Scholar
  10. Binford LC (1989) A distributional survey of the birds of the Mexican state of Oaxaca. Ornithol Monogr 43:1–418Google Scholar
  11. Blake ER (1977) Manual of neotropical birds, vol 1. Univ. of Chicago Press, ChicagoGoogle Scholar
  12. Caizergues A, Bernard-Laurent A, Brenot J-F, Ellison L, Rasplus JY (2003) Population genetics structure of rock ptarmigan Lagopus mutus in northern and western Europe. Mol Ecol 12:2267–2274PubMedCrossRefGoogle Scholar
  13. Chan Y, Arcese P (2002) Subspecific differentiation and conservation of song sparrows (Melospiza melodia) in the San Francisco Bay region inferred by microsatellite loci analysis. Auk 119:641–657CrossRefGoogle Scholar
  14. Chase CA III, Gore JA (1989) Snowy plover breeding distribution. Florida Game and Fresh Water Fish Commission, TallahasseeGoogle Scholar
  15. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  16. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  17. Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland, MassachusettsGoogle Scholar
  18. Cramp S, Simmons KEL (1983) Handbook of the birds of Europe, the Middle East and North Africa, vol 3. Oxford Univ. Press, New YorkGoogle Scholar
  19. Darwin C (1868) The variation of animals and plants under domestication. Murray, LondonGoogle Scholar
  20. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  21. Draheim HM (2006) Phylogeography and population structure of least terns (Sterna antillarum). Masters thesis, Oregon State University, Corvallis, Oregon, USAGoogle Scholar
  22. Eggert LS, Mundy NI, WoodRuff DS (2004) Population structure of loggerhead shrikes in the California Channel Islands. Mol Ecol 13:2121–2133PubMedCrossRefGoogle Scholar
  23. El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839CrossRefGoogle Scholar
  24. Endler JA (1977) Geographic variation, speciation, and clines. Princeton Univ. Press, Princeton, New JerseyGoogle Scholar
  25. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  26. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  27. Frankham R (1997) Do island populations have lower genetic variation than mainland populations? Heredity 78:311–327PubMedCrossRefGoogle Scholar
  28. Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675CrossRefGoogle Scholar
  29. Frankham R, Ballou JD, Briscoe DA (2002) Resolving taxonomic uncertainties and defining management units. In: Frankham R, Ballou JD, Briscoe DA (eds) Introduction to conservation genetics. Cambridge Univ. Press, United Kingdom, pp 365–392Google Scholar
  30. Fry AJ, Zink RM (1998) Geographic analysis of nucleotide diversity and song sparrow (Aves: Emberizidae) population history. Mol Ecol 7:1303–1313PubMedCrossRefGoogle Scholar
  31. Futuyma DJ (1998) Evolutionary biology, 3rd edn. Sinauer, Sunderland, MassachusettsGoogle Scholar
  32. Gaunt AS, Oring LW (1997) Guidelines to the use of wild birds in research. The Ornithological Council, Washington, DCGoogle Scholar
  33. Gay L, Defos Du Rau P, Mondain-Monval J-Y, Crochet P-A (2004) Phylogeography of a game species: the red-crested pochard (Netta rufina) and consequences for its management. Mol Ecol 13:1035–1045PubMedCrossRefGoogle Scholar
  34. Given AD, Mills A, Baker AJ (2002). Isolation of polymorphic microsatellite loci from the red-billed gull (Larus novaehollandiae scopulinus) and amplification in related species. Mol Ecol Notes 2:416–418CrossRefGoogle Scholar
  35. Gore J (1996) Cuban snowy plover. In: Rodgers H, Kale W, Smith KT (eds) Rare and endangered biota of Florida. V. Birds. University Press of Florida, Gainesville, Florida, pp 61–72Google Scholar
  36. Gorman LR (2000) Population differentiation among snowy plovers (Charadrius alexandrinus) in North America. Masters thesis, Oregon State University, Corvallis, Oregon, USAGoogle Scholar
  37. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.htmlGoogle Scholar
  38. Haig SM, Forsman ED, Mullins TD (2004) Subspecies relationships and genetic structure in the spotted owl. Conserv Genet 5:683–705CrossRefGoogle Scholar
  39. Haig SM, Beever EA, Chambers SM, Draheim HM, Dugger BD, Dunham S, Elliott-Smith E, Fontaine JB, Kesler DC, Knaus BJ, Lopes IF, Loschl P, Mullins TD, Sheffield LM (2006) Taxonomic considerations in listing subspecies under the U.S. Endangered Species Act. Conserv Biol 20:1584–1594PubMedCrossRefGoogle Scholar
  40. Haldane JBS (1931) A mathematical theory of natural selection. VI. Isolation. Trans Camb Phil Soc 26:220–230CrossRefGoogle Scholar
  41. Hayman P, Marchant J, Prater T (1986) Shorebirds: an identification guide to the waders of the world. Houghton Mifflin Co., BostonGoogle Scholar
  42. Hill LA, Talent LO (1990) Effects of capture, handling, banding, and radio-marking on breeding least terns and snowy plovers. J Field Ornithol 61:310–319Google Scholar
  43. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  44. Idaghdour Y, Broderick D, Korrida A, Chbel F (2004) Mitochondrial control region diversity of the Houbara bustard Chlamydotis undulata complex and genetic structure along the Atlantic seaboard of North Africa. Mol Ecol 13:43–54PubMedCrossRefGoogle Scholar
  45. Johnson JA, Toepfer JE, Dunn PO (2003) Contrasting patterns of mitochondrial and microsatellite population structure in fragmented populations of greater prairie chickens. Mol Ecol 12:3335–3347PubMedCrossRefGoogle Scholar
  46. Jones KL, Krapu GL, Brandt DA, Ashley MV (2005) Population genetic structure in migratory sandhill cranes and the role of Pleistocene glaciations. Mol Ecol 14:2645–2657PubMedCrossRefGoogle Scholar
  47. Joseph L, Lessa EP, Christidis L (1999) Phylogeny and biogeography in the evolution of migration: shorebirds of the Charadrius complex. J Biogeogr 26:329–342CrossRefGoogle Scholar
  48. Kalinowski ST (2002) How many alleles per locus should be used to estimate genetic distances? Heredity 88:62–65PubMedCrossRefGoogle Scholar
  49. Küpper C, Horsburgh GJ, Dawson DA, Ffrench-Constant R, Székely T, Burke T (2007) Characterization of 36 polymorphic microsatellite loci in the Kentish plover (Charadrius alexandrinus) including two sex-linked loci and their amplification in four other Charadrius species. Mol Ecol Notes 7:35–39CrossRefGoogle Scholar
  50. Lafferty KD (2001) Disturbance to wintering western snowy plovers. Biol Conserv 101:315–325CrossRefGoogle Scholar
  51. Lee GC (1989) Breeding ecology and habitat use patterns of snowy and Wilson’s plovers at the Cabo Rojo salt flats, Puerto Rico. Master’s thesis, Clemson Univ., Clemson SCGoogle Scholar
  52. Lewontin R, Krakauer J (1975) Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74:175–195Google Scholar
  53. Lian C, Zhou Z, Hogetsu T (2001) A simple method for developing microsatellite markers using amplified fragments of inter-simple sequence repeat (ISSR). J Plant Res 114:381–385CrossRefGoogle Scholar
  54. Maddison DR, Maddison WP (2000) MacClade 4: analysis of phylogeny and character evolution. Ver 40. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  55. Mayr E (1942) Systematics and the origin of species. Columbia Univ. Press, New YorkGoogle Scholar
  56. Mayr E (1963) Animal species and evolution. Harvard Univ. Press, Cambridge, MassachusettsGoogle Scholar
  57. McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291CrossRefGoogle Scholar
  58. Miller MP (2005) Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96:722–724PubMedCrossRefGoogle Scholar
  59. Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518CrossRefGoogle Scholar
  60. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. J Mol Evol 19:153–170PubMedCrossRefGoogle Scholar
  61. Oyler-McCance SJ, St. John J, Knopf FL, Quinn TW (2005) Population genetic analysis of mountain plover using mitochondrial DNA sequence data. Condor 107:353–362CrossRefGoogle Scholar
  62. Page GW (2004) Evidence supporting the Pacific coastal population of the western snowy plover as a distinct population segment qualifying for threatened status under the Endangered Species Act. Unpubl. report to the U.S. Fish and Wildlife Service. Point Reyes Bird Observatory Conservation Science, Stinson Beach, CaliforniaGoogle Scholar
  63. Page GW, Stenzel LE, Shuford WD, Bruce CR (1991) Distribution and abundance of the snowy plover on its western North American breeding grounds. J Field Ornithol 62:245–255Google Scholar
  64. Page GW, JS Warriner, JC Warriner, Paton PWC (1995) Snowy plover (Charadrius alexandrinus). In: Poole A, Gill F (eds) The birds of North America, vol 154. The Academy of Natural Sciences, Philadelphia, and The American Ornithologists’ Union, Washington, DCGoogle Scholar
  65. Patten MA, Unitt P (2002) Diagnosability versus mean differences of sage sparrow subspecies. Auk 119:26–35CrossRefGoogle Scholar
  66. Paton PWC, Edwards TC Jr (1996) Factors affecting interannual movements of snowy plovers. Auk 113:534–543Google Scholar
  67. Phillimore AB, Owens IPF (2006) Are subspecies useful in evolutionary and conservation biology. Proc Roy Soc Lond B 273:1049–1053CrossRefGoogle Scholar
  68. Pitra C, D’Aloia M-A, Lieckfeldt D, Combreau O (2004) Genetic variation across the current range of the Asian Houbara bustard (Chlamydotis undulata macqueenii). Conserv Gen 5:205–215CrossRefGoogle Scholar
  69. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  70. Primmer CR, Moller AP, Ellegren H (1995) Resolving genetic relationships with microsatellite markers: a parentage testing system for the swallow Hirundo rustica. Mol Ecol 4:493–498PubMedGoogle Scholar
  71. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  72. Randi E, Tabarroni C, Rimoni S, Lucchini V, Sfougaris A (2003) Phylogeography of the rock partridge (Alectoris graeca). Mol Ecol 12:2201–2214PubMedCrossRefGoogle Scholar
  73. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 83:248–249Google Scholar
  74. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  75. Ruhlen TD, Abbott S, Stenzel LE, Page GW (2003) Evidence that human disturbance reduces snowy plover chick survival. J Field Ornithol 74:300–304Google Scholar
  76. Sibley CG, Monroe BL Jr (1990) Distribution and taxonomy of birds of the world. Yale Univ. Press, LondonGoogle Scholar
  77. Slatkin M (1985) Gene flow in natural populations. Ann Rev Ecol Syst 16:393–430CrossRefGoogle Scholar
  78. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792PubMedCrossRefGoogle Scholar
  79. Solorzano S, Baker AJ, Oyama K (2004) Conservation priorities for resplendent quetzals based on analysis of mitochondrial DNA control region sequences. Condor 106:449–456CrossRefGoogle Scholar
  80. Sorenson MD, Ast JC, Dimcheff DE, Yuri T, Mindell DP (1999) Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol Phylogenet Evol 12:105–114PubMedCrossRefGoogle Scholar
  81. Sprandel GL, Gore JA, Cobb DT (1997) Winter shorebird survey. Final performance report. Florida Game and Freshwater Fish Commission, Talahassee, FloridaGoogle Scholar
  82. Stenzel LE, Warriner JC, Warriner JS, Wilson KS, Bidstrup FC, Page GW (1994) Long-distance breeding dispersal of Snowy Plovers in western North America. J Anim Ecol 63:887–902CrossRefGoogle Scholar
  83. Stroud DA, Davidson NC, West R, Scott DA, Haanstra L, Thorup O, Ganter B, Delany S (2004) Status of migratory wader populations in Africa and western Eurasia in the 1990s. Int Wader Stud 15:1–259Google Scholar
  84. Sullivan J, Abdo Z, Joyce P, Swofford DL (2005) Comparing successive approximations and simultaneous optimization approaches to maximum likelihood estimation of phylogeny from DNA sequences. Mol Biol Evol 22:1386–1392PubMedCrossRefGoogle Scholar
  85. Swofford DL (2000) PAUP*: phylogenetic analysis using parsimony (* and other methods). Sinauer, Sunderland, MassachusettsGoogle Scholar
  86. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  87. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  88. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins D (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  89. USFWS (US Fish and Wildlife Service) (1978) Determination that 11 plant taxa are endangered species and two plant taxa are threatened species. Federal Register 43:17910–17916Google Scholar
  90. USFWS (U.S. Fish and Wildlife Service) (1993) Determination of threatened status for the Pacific Coast population of the western snowy plover. Federal Register 58:12864–12874Google Scholar
  91. USFWS (U.S. Fish and Wildlife Service) and NMFS (National Marine Fisheries Service) (1996) Policy regarding the recognition of distinct vertebrate population segments under the Endangered Species Act. Federal Register 61:4721–4725Google Scholar
  92. Valliantoes M, Lougheed SC, Boag PT (2002) Conservation genetic of the loggerhead shrike (Lanius ludovicianus) in central and eastern North America. Conserv Gen 3:1–13CrossRefGoogle Scholar
  93. Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439PubMedCrossRefGoogle Scholar
  94. Warriner JS, Warriner JC, Page GW, Stenzel LE (1986) Mating system and reproductive success of a small population of polygamous Snowy Plovers. Wilson Bull 98:15–37Google Scholar
  95. Wenink PW, Baker AJ, Tilanus GJ (1994). Mitochondrial control-region sequences in two shorebird species, the turnstone and the dunlin, and their utility in population genetic studies. Mol Biol Evol 11:22–31PubMedGoogle Scholar
  96. Wilson-Jacobs R, Meslow EC (1984) Distribution, abundance, and nesting characteristics of snowy plovers on the Oregon coast. Northwest Sci 58:40–48Google Scholar
  97. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–259PubMedGoogle Scholar
  98. Zink RM (1989) The study of geographic variation. Auk 106:157–160Google Scholar
  99. Zink RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proc R Soc Lond B 271:561–564CrossRefGoogle Scholar
  100. Zink RM, Barrowclough GF, Atwood JL, Blackwell-Rago RC (2000) Genetics, taxonomy, and conservation of the threatened California gnatcatcher. Conserv Biol 14:1394–1405CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • W. Chris Funk
    • 1
  • Thomas D. Mullins
    • 1
  • Susan M. Haig
    • 1
  1. 1.USGS Forest and Rangeland Ecosystem Science CenterCorvallisUSA

Personalised recommendations