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Conservation Genetics

, Volume 7, Issue 5, pp 735–751 | Cite as

Re-examination of the historical range of the greater prairie chicken using provenance data and DNA analysis of museum collections

  • Jeremy D. Ross
  • Allan D. Arndt
  • Roger F. C. Smith
  • Jeff A. Johnson
  • Juan L. Bouzat
Article

Abstract

The extent to which a species has declined within its historical range is commonly used as an important criterion in categorizing the conservation status of wild populations. The greater prairie chicken (Tympanuchus cupido) has been extirpated from much of the area it once inhabited. However, within a large part of this area the species is not considered to be native, warranting no recovery effort or special protection. Demographic analysis based on provenance data from 238 specimens from museum collections in addition to genetic analyses of 100 mtDNA sequences suggest this species was native to the northern prairies, extending from central Minnesota to Alberta, Canada. Provenance data from 1879 to 1935 indicate that T. cupido would have required colonization and establishment of populations on an average 11,905 km2 every year, with an estimated per capita growth rate of 8.9% per year. These rates seem unrealistic given the limited dispersal and high mortality rates reported for this species. A survey of mtDNA sequences from “original” and “expanded” ranges revealed no differences in levels of sequence diversity within ranges (π=0.018; SE=0.004) but significant levels of genetic differentiation (F ST=0.034; P=0.013), which suggest that these populations have been relatively isolated for significant evolutionary time periods. DNA mismatch distributions fit a sudden expansion model consistent with a post-Pleistocene expansion of the species, which coincides with the expansion of prairies into the Canadian plains about 9000 years before present. This study demonstrates the value of museum collections as stores of ecological and genetic information fundamental for the conservation of natural populations, and suggests that the current status of the greater prairie chicken should be re-evaluated within all areas where this species may occur, but is now considered non-native.

Key words

Tympanuchus cupido range expansion historical DNA analysis mitochondrial DNA mismatch distributions 

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Notes

Acknowledgements

This work was supported by Department of Biological Sciences at Bowling Green State University, the Brandon University Research Committee, and the H. Stewart Perdue Award. We thank Christopher Tracey for technical assistance on GIS mapping, and Karen V. Root, Scott Mills, Ken N. Paige and three anonymous reviewers for helpful comments on the manuscript. The following museums provided access for specimen sampling: American Museum of Natural History (New York, NY), B.J. Hales Museum of Natural History (Brandon, MB), Canadian Museum of Nature (Ottawa, ON), Field Museum of Natural History (Chicago, IL), Manitoba Museum of Man and Nature (Winnipeg, MB), Museum of Vertebrate Zoology (Berkeley, CA), National Museum of Natural History (Washington, DC), Royal Ontario Museum (Toronto, ON), Royal Saskatchewan Museum (Regina, SK), and the U. of Alberta Museum of Zoology (Edmonton, AB). The following institutions provided T. cupido provenance data: Academy of Natural Sciences (Philadelphia, PA), Delaware Museum of Natural History (Wilmington, DE), Denver Museum of Nature and Science (CO), Dickey Collection – UCLA (Los Angeles, CA), Florida Museum of Natural History (Gainesville, FL), Milwaukee Public Museum (Milwaukee, WI), Museum of Comparative Zoology at Harvard (Cambridge, MA), New York State Museum (Albany, NY), Ohio State University Museum of Biological Diversity (Columbus, OH), Peabody Museum at Yale (New Haven, CT), Provincial Museum of Alberta (Edmonton, AB), San Diego Natural History Museum (San Diego, CA), Sam Noble Oklahoma Museum of Natural History (Norman, OK), The Natural History Museum (London, UK), U. of Michigan Museum of Zoology (Ann Arbor, MI), U. of Nevada (Reno, NV), and Western Foundation of Vertebrate Zoology (Camarillo, CA).

References

  1. Andow D, Kareiva P, Levin SA, Okubo A (1993). Spread of invading organisms: patterns of spread. In: Kim KC, (eds). Evolution of Insect Pests: The Pattern of Variations. Wiley, New York, pp. 219–242Google Scholar
  2. Applegate RD, Horak GJ (1999) Status and management of the greater prairie chicken in Kansas. In: The Greater Prairie Chicken: A National Look (eds. Svedarsky WD et al.), pp. 113–121. Minnesota Agricultural Experiment Station publication 99–1999, University of Minnesota, Saint Paul, MinnesotaGoogle Scholar
  3. Arndt AD, Van Neer W, Hellemans B, Robben J, Volckaert F, Waelkens M (2003). Roman trade relationships at Sagalassos (Turkey) elucidated by ancient DNA from fish remains. J. Archaeol. Sci. 30: 1095–1105CrossRefGoogle Scholar
  4. Audubon MR (1960). Audubon and His Journals. Dover Publications, New YorkGoogle Scholar
  5. Avise JC, Walker D (1998). Pleistocene phylogeographic effects on avian populations and the speciation process. Proc. Royal Soc. London Ser. B-Biol. Sci. 265: 457–463CrossRefGoogle Scholar
  6. Ballard JWO, Whitlock MC (2004). The incomplete natural history of mitochondria. Mol. Ecol. 13: 729–744CrossRefPubMedGoogle Scholar
  7. Bouzat JL (2001). The importance of control populations for the identification and management of genetic diversity. Genetica 110: 109–115CrossRefGoogle Scholar
  8. Bouzat JL, Lewin HA, Paige KN (1998). The ghost of genetic diversity past: historical DNA analysis of the Greater Prairie Chicken. Am. Nat. 152: 1–6CrossRefGoogle Scholar
  9. Bouzat JL, Johnson K (2004). Genetic structure among closely-spaced leks in a peripheral population of lesser prairie-chickens. Mol. Ecol. 13: 499–505CrossRefPubMedGoogle Scholar
  10. Bowman TJ, Robel RJ (1977). Brood break-up, dispersal, mobility, and mortality of juvenile prairie chickens. J. Wildlife Manage. 41: 27–34Google Scholar
  11. Charlesworth B, Charlesworth D, Barton NH (2003). The effects of genetic and geographic structure on neutral variation. Ann. Rev. Ecol., Evol. Syst. 34: 99–125CrossRefGoogle Scholar
  12. Coffin B, Pfannmuller L (1988). Minnesota’s Endangered Flora and Fauna. University of Minnesota Press, MinneapolisGoogle Scholar
  13. Collins SL (2001) Long-term research and the dynamics of bird populations and communities. Auk 118: 583–588CrossRefGoogle Scholar
  14. Cooke W (1888). Report on Bird Migration in the Mississippi Valley in the Years 1884 and 1885. Department of Agriculture Ornithology Bulletin 2. U.S. Government Printing Office, Washington, D.CGoogle Scholar
  15. Coues E (1874). Birds of the Northwest. U.S. Government Print Office, Washington, D.CGoogle Scholar
  16. Dimcheff DE, Drovetski SV, Mindell DP (2002). Phylogeny of Tetraoninae and other galliform birds using mitochondrial 12S and ND2 genes. Mol. Phylogenet. Evol. 24: 203–215CrossRefPubMedGoogle Scholar
  17. DNR-Minnesota (2005). 2005 Minnesota Hunting Regulations. St. Paul, MinnesotaGoogle Scholar
  18. Douglas D (1829). Observations on some species of the genera Tetrao and Ortyx, natives of North America, with descriptions of four new species of the former, and two of the latter genus. Trans. Linn. Soc. London 16: 133–149Google Scholar
  19. Drovetski SV (2002) Molecular Phylogeny of grouse: individual and combined performance of W-linked autosomal, and mitochondrial loci Syst.Biol., 51 930–945PubMedGoogle Scholar
  20. Drovetski SV, Ronquist F (2003). Plio-Pleistocene climatic oscilations, Holarctic biogeography and speciation in an avian subfamily. J. Biogeogr. 30: 1173–1181CrossRefGoogle Scholar
  21. Dunn PO, Braun CE (1985). Natal dispersal and lek fidelity of sage grouse. Auk 102: 621–627Google Scholar
  22. García-Ramos G, Rodríguez D (2002). Evolutionary speed of species invasions. Evolution 56: 661–668PubMedCrossRefGoogle Scholar
  23. Hamerstrom F, Hamerstrom F (1973). The prairie chicken in Wisconsin: highlights of a 22-year study of counts, behavior, movements, turnover and habitat. Technical Bulletin 64, Department of Natural Resources, Madison, WisconsinGoogle Scholar
  24. Hansson B, Bensch S, Hasselquist D, Lillandt BG, Wennerberg L, Von Schantz T (2000). Increase of genetic variation over time in a recently founded population of great red warblers (Acrocephalus arundinaceus) revealed by microsatellites and DNA fingerprinting. Mol. Ecol. 9: 1529–1538CrossRefPubMedGoogle Scholar
  25. Hind HY (1860) Narrative of the Canadian Red River Exploring Expedition of 1857; and of the Assinniboine and Saskatchewan Exploring Expedition of 1858. Longman, Green, Longman and Roberts, LondonGoogle Scholar
  26. Hjertaas D, Brechtel S, Jones R, Edwards R, Schroeder C (1993). National Recovery Plan for the Greater Prairie-Chicken. Report No. 5. Recovery of Nationally Endangered Wildlife Committee, OttawaGoogle Scholar
  27. Hooge PN, Eichenlaub B (2000). Animal Movement Extension to Arcview. Alaska Science Center - Biological Science Office, U.S. Geological Survey, Anchorage, AKGoogle Scholar
  28. Houston CS (2002). Spread and disappearance of the greater prairie-chicken, Tympanuchus cupido, on the Canadian prairies and adjacent areas. Can. Field-Nat. 116: 1–21Google Scholar
  29. Hubbard JP (1973). Avian evolution in the arid-lands of North America. Living Bird 12: 155–196Google Scholar
  30. Hutchison DW (2003). Testing the central/peripheral model: analysis of microsatellite variability in the eastern collared lizard. Am. Midland Nat. 149: 148–162CrossRefGoogle Scholar
  31. IUCN (2001). IUCN Red List categories, v. 3. 1. International Union for the Conservation of Nature (IUCN), Gland, SwitzerlandGoogle Scholar
  32. Johnsgard PA (1983). The Grouse of the World. University of Nebraska Press, LincolnGoogle Scholar
  33. Johnson JA, Dunn PO (2006) Low genetic variation in the Heath Hen prior to extinction and implications for the conservation of prairie-chicken populations. Conserv. Genet. (in press)Google Scholar
  34. 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: 3335–3348CrossRefPubMedGoogle Scholar
  35. Johnson JA, Bellinger MR, Toepfer JE, Dunn PO (2004). Temporal changes in allele frequencies and low effective population size in greater prairie-chickens. Mol. Ecol. 13: 2617–2630CrossRefPubMedGoogle Scholar
  36. King WR (1866). The Sportsman and Naturalist in Canada. Hurst and Blackett, LondonGoogle Scholar
  37. Kirsch LM, Kruse AD (1972) Prairie fires and wildlife. pp. 289–303. Annual Tall Timbers Fire Ecology Conference. Northern Prairie Wildlife Research Center, Bureau of Sport Fisheries and WildlifeGoogle Scholar
  38. Kobriger JD (1999) Status and management of the greater prairie chicken in North Dakota. In The Greater Prairie Chicken: A National Look (eds. Svedarsky WD et al.), pp. 63–74. Minnesota Agricultural Experiment Station publication 99–1999, University of Minnesota, Saint Paul, MinnesotaGoogle Scholar
  39. Kumar S, Tamura K, Jakobsen IB, Nei M (2001). MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17: 1244–1245PubMedCrossRefGoogle Scholar
  40. Lambert DM, Ritchie PA, Millar CD, Holland B, Drummond AJ, Baroni C (2002). Rates of evolution in ancient DNA from Adélie penguins. Science 295: 2270–2273CrossRefPubMedGoogle Scholar
  41. Lavery S, Moritz C, Fielder DR (1996) Genetic patterns suggest exponential population growth in a declining species. Mol. Biol. Evol. 12: 1106–1113Google Scholar
  42. Lessa EP, Cook JA, Patton JL (2003). Genetic footprints of demographic expansion in North America, but not Amazonia, during the Late Quaternary. Proc. Natl. Acad. Sci. USA 100: 10331–10334CrossRefPubMedGoogle Scholar
  43. Lieberman BS (2000). Palaeobiogeography: Using Fossils to Study Global Change, Plate Tectonics, and Evolution. Plenum Press/Kluwer Academic Publishers, New YorkGoogle Scholar
  44. Lucchini V, Hoglund J, Klaus S, Swenson J, Randi E (2001). Historical biogeography and a mitochondrial DNA phylogeny of grouse and ptarmigan. Mol. Phylogenet. Evol. 20: 149–162CrossRefPubMedGoogle Scholar
  45. Mundinger PC, Hope S (1982). Expansion of the winter range of the house finch: 1947–1979. Am. Birds 36: 347–353Google Scholar
  46. Nei M, Kumar S (2000). Mol. Evol. Phylogenet. Oxford University Press, New York, NY, USAGoogle Scholar
  47. Okubo A (1988). Diffusion-type models for avian range expansion. In: Ouellet H, (eds). Acta XIX Congress Internationalis Ornithologici. National Museum of Natural Sciences, University of Ottawa Press, Ottawa, pp. 1038–1049Google Scholar
  48. Pergams ORW, Barnes WM, Nyberg D (2003). Mammalian microevolution: rapid change in mouse mitochondrial DNA. Nature 423:397CrossRefPubMedGoogle Scholar
  49. Posada D, Crandall KA (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  50. Quinn TW (1992). The genetic legacy of Mother Goose: phylogeographic patterns of lesser snow goose Chen caerulescens caerulescens maternal lineages. Mol. Ecol. 1:105–117PubMedGoogle Scholar
  51. Quinn TW, Wilson AC (1993). Sequence evolution in and around the control region in birds. J. Mol. Evol. 37:417–425CrossRefPubMedGoogle Scholar
  52. Roberts TS (1932). The Birds of Minnesota. University of Minnesota Press, MinneapolisGoogle Scholar
  53. Rogers AR (1992). Error introduced by the infinite-sites model. Mol. Biol. Evol. 9:1181–1184PubMedGoogle Scholar
  54. Rogers AR (1995). Genetic-evidence for a Pleistocene population explosion. Evolution 49:608–615CrossRefGoogle Scholar
  55. Rogers AR, Harpending H (1992). Population-growth makes waves in the distribution of pairwise genetic-differences. Mol. Biol. Evol. 9:552–569PubMedGoogle Scholar
  56. Rowe KC, Heske EJ, Brown PW, Paige KN (2004). Surviving the ice: Northern refugia and postglacial colonization. Proc. Natl. Acad. Sci. USA 101:10355–10359CrossRefPubMedGoogle Scholar
  57. Rozas J, Rozas R (1999). DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175PubMedCrossRefGoogle Scholar
  58. Sambrook J, Fritsch EF, Maniatis T (1989). Molecular Cloning. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  59. Schneider S, Excoffier L (1999). Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates very among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedGoogle Scholar
  60. Schneider S, Roessli D, Excoffier L (2000) Arlequin, Version 2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  61. Schroeder MA, Braun CE (1993). Partial migration in a population of greater prairie-chickens in Northeastern Colorado. Auk 110:21–28Google Scholar
  62. Shaffer HB, Fisher RN, Davidson C (1998). The role of natural history collections in documenting species declines. Trends Ecol. Evol. 13:27–30CrossRefGoogle Scholar
  63. Slatkin M, Hudson RR (1991). Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedGoogle Scholar
  64. Svedarsky WD, Hier RH, Silvy NJ, eds. (1999a) The greater prairie chicken: a national look. Minnesota Agricultural Experimentation Station publication 99–1999, University of Minnesota, St. Paul, MinnesotaGoogle Scholar
  65. Svedarsky WD, Wolfe TJ, Toepfer JE (1999b) Status and management of the greater prairie chicken in Minnesota. In: The Greater Prairie Chicken: A National Look (eds. Svedarsky WD et al.), pp. 25–38. Minnesota Agricultural Experiment Station publication 99–1999, University of Minnesota, Saint Paul, MinnesotaGoogle Scholar
  66. Tajima F (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  67. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 24:4876–4882CrossRefGoogle Scholar
  68. Trippe TM (1871). Some differences between western and eastern birds. Am. Nat. 5:632–636CrossRefGoogle Scholar
  69. Toepfer JE (2003). Prairie Chickens and Grasslands: 2000 and Beyond. Society of Tympanuchus Cupido Pinnatus Ltd., Elm Grove, WisconsinGoogle Scholar
  70. Williams JW, Shuman BN, Webb T, Bartlein PJ, Leduc PL (2004). Late Quaternary vegetation dynamics in North America: scaling from taxa to biomes. Ecol. Monogr. 74:309–334Google Scholar
  71. Wisdom MJ, Mills LS (1997). Sensitivity analysis to guide population recovery: prairie-chickens as an example. J. Wildlife Manage. 61:302–312Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Jeremy D. Ross
    • 1
  • Allan D. Arndt
    • 2
    • 4
  • Roger F. C. Smith
    • 2
  • Jeff A. Johnson
    • 3
  • Juan L. Bouzat
    • 1
  1. 1.Department of Biological SciencesBowling Green State UniversityBowling GreenUSA
  2. 2.Department of ZoologyBrandon UniversityManitobaCanada
  3. 3.Museum of ZoologyUniversity of MichiganAnn ArborUSA
  4. 4.University College of Fraser ValleyAbbotsfordCanada

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