Conservation Genetics

, Volume 9, Issue 3, pp 495–505 | Cite as

High genetic diversity in the blue-listed British Columbia population of the purple martin maintained by multiple sources of immigrants

  • Allan J. BakerEmail author
  • Annette D. Greenslade
  • Laura M. Darling
  • J. Cam Finlay
Research Article


To assess genetic diversity in the blue-listed purple martin (Progne subis) population in British Columbia, we analysed mitochondrial control region sequences of 93 individuals from British Columbia and 121 individuals collected from seven localities of the western and eastern North American subspecies P. s. arboricola and P. s. subis, respectively. Of the 47 haplotypes we detected, 34 were found exclusively in western populations, and 12 were found only in eastern populations. The most common eastern haplotype (25) was also found in three nestlings in British Columbia and one in Washington. Another British Columbia nestling had a haplotype (35) that differed by a C to T transition from haplotype 25. Coalescent analysis indicated that these five nestlings are probably descendents of recent immigrants dispersing from east to the west, because populations were estimated to have diverged about 200,000–400,000 ybp, making ancestral polymorphism a less likely explanation. Maximum likelihood estimates of gene flow among all populations detected asymmetrical gene flow into British Columbia not only of rare migrants from the eastern subspecies in Alberta but also a substantial number of migrants from the adjacent Washington population, and progressively lower numbers from Oregon in an isolation-by distance pattern. The influx of migrants from different populations is consistent with the migrant-pool model of recolonization which has maintained high genetic diversity in the small recovering population in British Columbia. Thus, the risk to this population is not from genetic erosion or inbreeding following a severe population crash, but from demographic stochasticity and extinction in small populations.


Genetic diversity Migrant-pool recolonization Blue-listed population Purple martin Nest box recovery 



The research was made possible by grants and sponsorship from NSERC, the Rocky Point Bird Observatory, British Columbia Ministry of Environment, Lands and Parks, Canada Department of National Defense, Washington Department of Fish and Wildlife, British Columbia Habitat Conservation Trust Fund, Toronto Dominion Friends of the Environment Foundation, and the Purple Martin Conservation Association. We gratefully acknowledge our many volunteer partners who assisted collecting blood samples: California: Dan Airola, Thomas Leeman, Stan Kostka, Stan Wright; Oregon: Bruce Campbell, Kat Beal, Terry Farrell, Marnie Albritten, Wayne Burns; Washington: Michelle Tirhi, Kevin Li; Pennsylvania: James R. Hill III, Eugene Morton, Bridget Stutchbury, Tony Salvadori; Manitoba: Ernie Didur; Ontario, Bill Petrie; Alberta: Hardy Pletz, Pamela Gordy; British Columbia: Tom Gillespie, Michael Setterington. Laboratory work was conducted by O. Haddrath (OH) and A. Greenslade (ADG), and statistical analysis of the DNA data was performed by ADG and AJB. O. Haddrath, Royal Ontario Museum, designed a martin-specific primer and assisted with data collection and experiment design. We thank Bruce Cousens who provided essential input to the data collection and natural history aspects of this paper, and carefully checked the manuscript.


  1. Ardern SL, Lambert DM, Rodrigo AG, McLean IG (1997) The effects of population bottlenecks on multilocus DNA variation in robins. J Heredity 88:79–186Google Scholar
  2. Baker AJ, Marshall HD (1997) Mitochondrial control region sequences as tools for understanding evolution. In: Mindell DP (ed) Avian molecular evolution and systematics. Academic Press, San DiegoGoogle Scholar
  3. Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744 PubMedCrossRefGoogle Scholar
  4. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedGoogle Scholar
  5. Barton NH, Whitlock MC (1997) The evolution of metapopulations. In: Hanski IA, Gilpin ME (eds) Metapopulation biology: ecology, genetics, and evolution. Academic Press, San DiegoGoogle Scholar
  6. Beerli P (2004) Migrate: documentation and program, part of LAMARC. Version 2.0. Revised December 23, 2004. Distributed over the Internet, Scholar
  7. Beerli P, Felsenstein J (1999) Maximum likelihood estimation of migration rates and population numbers of two populations using a coalescent approach. Genetics 152:763–773PubMedGoogle Scholar
  8. 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 Natl Acad Sci USA 98:4563–4568PubMedCrossRefGoogle Scholar
  9. Behle WH (1968) A new race of the purple martin from Utah. Condor 70:166–169CrossRefGoogle Scholar
  10. Brito PH (2005) The influence of Pleistocene glacial refugia on tawny owl genetic diversity and phylogeography in western Europe. Mol Ecol 14:3077–3094PubMedCrossRefGoogle Scholar
  11. Brown CR (1997) Purple martin (Progne subis). In: Poole A, Gill F (eds) The birds of North America, No. 287. Academy of natural sciences, Philadelphia, PA, and American Ornithologists Union, Washington, DCGoogle Scholar
  12. Cabot E (1997) XESEE 3.1, Eyeball Sequencer EditorGoogle Scholar
  13. Campbell RW, Dawe NK, McTaggart-Cowan I, Cooper JM, Kaiser GW, McNall MC, Smith GE (1997) The birds of British Columbia. Vol.3. Passerines: flycatchers through vireos. UBC Press, Vancouver, British ColumbiaGoogle Scholar
  14. Clegg SM, Degnan SD, Kikkawa J, Moritz C, Estoup A, Owens IPF (2002) Genetic consequences of sequential founder events by an island-colonizing bird. Proc Natl Acad Sci USA 99:8127–8132PubMedCrossRefGoogle Scholar
  15. Copley D, Fraser D, Finlay JC (1999) Purple martin, Progne subis: a British Columbia success story. Can Field Nat 113:226–229Google Scholar
  16. Cousens B, Lee JC, Darling LM, Finlay JC, Gillespie TW (2005a) Two Decades of Purple martin stewardship and recovery in British Columbia—successes and challenges. Proceedings of the 2005 Puget Sound Georgia Basin research conference, 29–31 March 2005. Seattle, WashingtonGoogle Scholar
  17. Cousens B, Lee JC, Kostka S, Darling LM, Tirhi M, Finlay JC, Gillespie TW (2005b) Recovery of the Western Purple martin bordering the ‘Salish Sea’—the Georgia Basin of British Columbia and Puget Sound, Washington. Proceedings of the 2005 Puget Sound Georgia Basin research conference, 29–31 March 2005. Seattle, WashingtonGoogle Scholar
  18. Dean AD, Greenwald JE (1995) Use of filtered pipet tips to elute DNA from agarose gels. Biotechniques 18:980PubMedGoogle Scholar
  19. Fraser DF, Copley D, Finlay JC (2000) The return of the purple martin in British Columbia. In: Darling LM (ed) Proceedings of a conference on the biology and management of species and habitats at risk, vol 1, Kamloops BC 15–19 Feb (1999), B. C. Ministry of Environment, Lands and Parks, Victoria, B. C. and University College of the Cariboo, Kamloops, B. CGoogle Scholar
  20. Fraser DF, Siddle C, Copley D, Walters E (1997) Status of the purple martin in British Columbia. Wildlife Status Report Number WR-89. B. C. Ministry of Environment, Lands and Parks. Wildlife BranchGoogle Scholar
  21. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  22. Fu Y-X, W-H Li (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedGoogle Scholar
  23. Giles BE, Goudet J (1997) A case study of genetic structure in a plant metapopulation. In: Hanski IA, Gilpin ME (eds) Metapopulation biology: ecology, genetics, and evolution. Academic Press, San DiegoGoogle Scholar
  24. Hill JR III, Dellinger TB (1997) Purple martin recoveries south of the border. Purple Martin Update 8:28–29 Google Scholar
  25. Klicka J, RM Zink (1997) The importance of recent ice ages in speciation: a failed paradigm. Science 277:1666–1669CrossRefGoogle Scholar
  26. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, NY, USAGoogle Scholar
  27. Nei M, Maruyama T, Chakraborthy R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  28. Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov Chain Monte Carlo approach. Genetics 158:885–896PubMedGoogle Scholar
  29. Pereira SL, AJ Baker (2006) A mitogenomics timescale for birds detects variable phylogenetic rates of molecular evolution and refutes the standard molecular clock. Mol Biol Evol 23:1731–1740PubMedCrossRefGoogle Scholar
  30. Plath T (1994) Purple martin (Progne subis) nest box program—first recorded nesting in 22 years for BC Mainland. Vancouver Natl History Soc Discover 23:143–145Google Scholar
  31. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  32. Pridgeon S (1997) Wildlife at risk in British Columbia: purple martin. B. C. Ministry of Environment, Lands and Parks, Victoria, B.CGoogle Scholar
  33. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  34. Rozas J, Sanchez-DelBarrio JC, Messequer X, Rozas R (2003) DNAsp, DNA polymorhism analysis by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  35. Sæther B, Lande R, Engen S, Weimerskirch H, Lillegård M, Altwegg R, Becker PH, Bregnoballe T, Brommer JE, McCleery RH, Merilä J, Nyholm E, Rendell W, Robertson RR, Tryjanowski P, Visser ME (2005) Generation time and temporal scaling of bird population dynamics. Nature 436:99–102PubMedCrossRefGoogle Scholar
  36. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. Cold Spring Harbor Laboratory, Cold Spring Harbor, New YorkGoogle Scholar
  37. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000 : a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  38. Slatkin M (1977) Gene flow and genetic drift in a species subject to frequent local extinctions. Theoret Pop Biol 12:253–262CrossRefGoogle Scholar
  39. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  40. 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
  41. Tarr CL (1995) Primers for amplification and determination of mitochondrial control-region sequences in oscine passerines. Mol Ecol 4:527–529PubMedCrossRefGoogle Scholar
  42. Tarr CL, Conant S, Fleischer RC (1998) Founder events and variation at microsatellite loci in an insular passerine bird, the Laysan finch (Telespiza cantans). Mol Ecol 7:719–731CrossRefGoogle Scholar
  43. Whitlock MC, McCauley DE (1990) Some population genetic consequences of colony formation and extinction: genetic correlations within founding groups. Evolution 44:1717–1724CrossRefGoogle Scholar
  44. Zink RM (2005) Natural selection on mitochondrial DNA in Parus and its relevance for phylogeographic studies. Proc Roy Soc B 272:71–78CrossRefGoogle Scholar
  45. Zink RM, Drovetski SV, Rohwer S (2006) Selective neutrality of mitochondrial ND2 sequences, phylogeography and species limits in Sitta europea. Mol Phylogenet Evol 40:679–686PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Allan J. Baker
    • 1
    Email author
  • Annette D. Greenslade
    • 1
  • Laura M. Darling
    • 2
  • J. Cam Finlay
    • 3
  1. 1.Department of Natural HistoryRoyal Ontario MuseumTorontoCanada
  2. 2.B.C. Ministry of EnvironmentVictoriaCanada
  3. 3.VictoriaCanada

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