Abstract
The importance of climatic change on the establishment and differentiation of high-latitude species is largely unknown. Biological effects of historic climate change can be determined from historic signals in genetic data. The rock sandpiper (Calidris ptilocnemis) is a good test case for examining these biological effects because it has a known sister species, the purple sandpiper (Calidris maritima), and it is the only endemic Beringian bird with multiple described subspecies, suggesting a process of initial establishment and subsequent differentiation in the high-latitude regions of Beringia. We sequenced 2,074 bp of mitochondrial DNA from 40 rock sandpipers from nine breeding locations and four purple sandpipers. We used phylogenetic and coalescence methods to reconstruct trees and to evaluate the population demography, migration rates, and relative times of population divergence. Phylogenetic trees show that purple and rock sandpipers are monophyletic sister species. Within the rock sandpiper, clade branching patterns and coalescence estimates suggest that there were multiple refugial populations in Beringia, which correspond loosely to different glacial cycles. Rock sandpipers show the establishment, persistence, and accumulation of partitioned genetic diversity across several glacial cycles, implicating the presence of multiple cryptic biological refugia in this region through repeated cycles of climate change.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
American Ornithologists’ Union.: 1910, Check-list of North American Birds, 3rd edn. American Ornithologists’ Union, New York.
American Ornithologists’ Union.: 1931, Check-list of North American Birds, 4th edn. American Ornithologists’ Union, Lancaster.
American Ornithologists’ Union.: 1957, Check-list of North American Birds, 5th edn. American Ornithologists’ Union, Baltimore.
Avise, J. C.: 2000, Phylogeography. Harvard University Press,Cambridge
Borowik, O. A.: 1996, Molecular Systematics and the Evolution of Mating Systems in Calidridine Sandpipers. Doctor of philosophy dissertation, University of Toronto.
Borowik, O. A. and McLennan, D. A.: 1999, ‘Phylogenetic Patterns of Parental Care in Calidridine Sandpipers’, Auk116, 1107–1117.
Congdon, B. C., Piatt, J. F., Martin, K., and Friesen, V. L.: 2000, ‘Mechanisms of Population Differentiation in Marbled Murrelets: Historical Versus Contemporary Processes’, Evolution54, 974–986.
del Hoyo, J., Elliott, A., and Sargatal, J. eds.: 1996, Handbook of the Birds of the World, Vol.3. Hoatzins to Auks. Lynx Editions, Barcelona.
Edwards, S. V. and Beerli, P.: 2000, ‘Gene Divergence, Population Divergence, and the Variance in Coalescence Time in Phylogeographic Studies’, Evolution54, 1839–1854.
Farris, J. S., Kallersjo, M., Kluge, A. G., and Bult, C.: 1995a, ‘Testing Significance of Incongruence’, Cladistics10, 315–319.
Farris, J. S., Kallersjo, M., Kluge, A. G., and Bult, C.: 1995b, ‘Constructing a Significance Test for Incongruence’, Syst. Biol.44, 570–572.
Fay, F. H. and Cade, T. J.: 1959, ‘An Ecological Analysis of the Avifauna of St. Lawrence Island, Alaska’, Univ. California Publ. Zoology63, 73–150.
Fedorov, V. B. and Stenseth, N. C.: 2002, ‘Multiple Glacial Refugia in the North American Arctic: Inference from Phylogeography of the Collared Lemming Dicrostonyxgroenlandicus’, Proc. Royal Soc. London Ser. B269 2071–2078.
Felsenstein, J.: 1985, ‘Confidence Limits on Phylogenies: an Approach Usingthe Bootstrap’, Evolution29, 783–791.
Fleischer, R. C. and McIntosh, C. E., and Tarr, C. L.: 1998, ‘Evolution on a Volcanic Conveyor Belt: Using Phylogeographic Reconstructions and K-Ar-Based Ages of the Hawaiian Islands to Estimate Molecular Evolutionary Rates’,Mol. Ecol.7, 533–545.
Gibson, D. D. and Kessel, B.: 1992, ‘Seventy-Four New Avian Taxa Documentedin Alaska 1976–1991’, Condor94, 454–467.
Gibson, D. D. and Kessel, B.: 1997, ‘Inventory of the Species and Subspecies of Alaska Birds’, West. Birds28, 45–95.
Gill, R. E., Tomkovich, P. S., and McCaffery, B. J.: 2003, ‘Rock Sandpiper’,in A. Poole and F. Gill eds., Birds of North America, No. 686, The Birds of North America Inc., Philadelphia.
Glenn, T.: 1997, Genetic Bottlenecks in Long-Lived Vertebrates: Mitochondrial and Microsatellite DNA Variation in American Alligators and Whooping Cranes. Doctor of Philosophy dissertation, University of Maryland.
Griswold, C. K. and Baker, A. J.: 2002, ‘Time to the Most Recent Common Ancestor and Divergence Times of Populations of Common Chaffinches (Fringilla coelebs) in Europe and North Africa: Insights into Pleistocene Refugia and Current Levels of Migration’, Evolution 56, 143–153.
Hackett, S. J. 1996 ‘Molecular Phylogenetics and Biogeography of Tanagers in the Genus Ramphocelus Aves’, Mol. Phylogen. Evol.5 368–382.
Hamilton, T. D., Reed, K. M., and Thorsen, R. M. 1986. Glaciation in Alaska. Alaska Geological Society, Anchorage.
Harding, R. M. 1996 ‘New Phylogenies: An Introductory Look at the Coalescent’, in Harvey, P.H. et al. eds., New Uses for New Phylogenies, Oxford University Press, pp. 15–22.
Harshman, J.: 1996, Phylogeny, Evolutionary Rates, and Ducks. Doctor of Philosophy Dissertation, University of Chicago.
Hartl, D. L. and Clark, A. G.: 1997, Principles of Population Genetics, 3rd edn., Sinauer,Sunderland.
Hasegawa, M. H., Kishino, H., and Yano, T.: 1985, ‘Dating of the Human-Ape Splitting by a Molecular Clock of Mitochondrial DNA’, J. Mol. Evol.21 160–174.
Hayman, P., Marchant, J., and Prater, T.: 1986, Shorebirds: An Identification Guide to the Waders of the World, Houghton Mifflin Co., Boston.
Hewitt, G.: 2000, ‘The Genetic Legacy of the Quaternary Ice Ages’, Nature405, 907–913.
Holder, K., Montgomerie, R., and Friesen, V. L.: 1999, ‘A Test of the Glacial Refugium Hypothesis Using Patterns of Mitochondrial and Nuclear DNA Sequence Variation in Rock Ptarmigan Lagopus mutus’, Evolution53, 1936–1950.
Hopkins, D. M.: 1967, ‘The Cenozoic History of Beringia–A Synthesis’, in D. M. Hopkins ed., The Bering Land Bridge, Stanford University Press, Stanford, pp. 451–484.
Hopkins, D. M., Matthews, J. V., Schweger, C. E., and Young, S. B.: 1982, Paleoecology of Beringia, Academic Press, New York.
Huelsenbeck, J. P. and Ronquist, F.: 2001, ‘MR-BAYES: Bayesian Inference of Phylogeny’, Bioinformatics17, 754–755.
Johnson, K. P. and Sorenson, M. D.: 1998, ‘Comparing Molecular Evolution in Two Mitochondrial Protein Coding Genes Cytochrome b and ND2 in the Dabbling Ducks Tribe: Anatini’, Mol. Phylogen. Evol.10, 82–94.
Johnson, K. P. and Clayton, D. H.: 2000, ‘A Molecular Phylogeny of the Dove Genus Zenaida: Mitochondrial and Nuclear DNA Sequences’, Condor102, 864–870.
Kimura, M.: 1983, The Neutral Theory of Molecular Evolution,Cambridge University Press, Cambridge.
Klicka, J. and Zink, R. M.: 1997, ‘The Importance of Recent ice Ages in Speciation: A Failed Paradigm’, Science277, 1666–1669.
Kornegay, J. R., Kocher, T. D., Williams, L. A., and Wilson, A. C.: 1993, ‘Pathways of Lysozyme Evolution Inferred from the Sequences of Cytochrome b in Birds’, J. Mol. Evol.37, 367–379.
Krajewski, C. and D. G. King.: 1996, ‘Molecular Divergence and Phylogeny: Rates and Patterns of Cytochrome b Evolution in Cranes’, Mol. Biol. Evol.13, 21–30.
Larget, B. and Simon, D. L.: 1999, ‘Markov Chain Monte Carlo Algorithms forthe Bayesian Analysis of Phylogenetic Trees’, Mol. Biol. Evol.16, 750–759.
Muira, G. I. and Edwards, S. V.: 2001, ‘Cryptic Differentiation and Geographic Variation in Genetic Diversity of Hall’s Babbler, Pomastostomus halli’J. Avian Biol.32, 102–110.
Murie, O. J.: 1959, Fauna of the Aleutian Islands and Alaska Peninsula, North American Fauna No. 61, US Fish and Wildlife Service, Washington DC.Murie, O. J. 1959. Fauna of the Aleutian Islands and Alaska Peninsula, North American Fauna No. 61, US Fish and Wildlife Service, Washington DC.Murie, O. J.: 1959, Fauna of the Aleutian Islands and Alaska Peninsula, North American Fauna No. 61, US Fish and Wildlife Service, Washington DC.Murie, O. J. 1959. Fauna of the Aleutian Islands and Alaska Peninsula, North American Fauna No. 61, US Fish and Wildlife Service, Washington DC.
Murphy, W. J., Eizirik, E., O’Brien, S. J., Madsen, O., Scally, M., Douady, C. J., Teeling, E., Ryder, O. A., Stanhope, M. J., de Jong, W. W., and Springer, M. S.: 2001, ‘Resolution of the Early Placental Mammal Radiation Using Bayesian Phylogenetics’, Science294, 2348–2351.
Nielsen, R. and Wakeley, J.: 2001, ‘Distinguishing Migration from Isolation:A Markov Chain Monte Carlo Approach’, Genetics158, 885–896.
Nunn, G. B., Cooper, J., Jouventin, P., Robertson, C. J. R., and G. G. Robertson.: 1996, ‘Evolutionary Relationships Among Extant Albatrosses Procellariiformes: Diomedeidae Established from Complete Cytochrome-b Gene Sequences’, Auk113, 784–801.
Peters, J. L.: 1934, Check-list of the Birds of the World, Harvard University Press, Cambridge.
Pielou, E. C.: 1991, After the Ice Age, University of Chicago Press, Chicago.
Posada, D. and Crandall, K. A.: 1998, ‘Modeltest: Testing the Model of DNA Substitution’, Bioinformatics14, 817–818.
Rand, D. M.: 1996, ‘Neutrality Tests of Molecular Markers and the Connection Between DNA Polymorphism, Demography, and Conservation Biology’, Cons. Biol10, 665–671.
Randi, E.: 1996, ‘A Mitochondrial Cytochrome b Phylogeny of the Alectoris Partridges’, Mol. Phylogen. Evol.6, 214–227.
Rannala, B. and Yang, Z.: 1996, ‘Probability Distribution of Molecular Evolutionary Trees: A New Method of Phylogenetic Inference’, J. Mol. Evol.43, 304–311.
Rogers, A. R.: 1995, ‘Genetic Evidence for a Pleistocene Population Explosion’, Evolution49, 608–615.
Rogers, A. R. and Harpending, H.: 1992, ‘Population Growth Makes Waves in the Distribution of Pairwise Genetic Distances’, Mol. Biol. Evol.9, 552–569.
Schneider, S., Kueffer, J., Roessli, D., and Excoffier, L.: 1997, Arlequin ver. 1.1: A Software for Population Genetic Data Analysis, Genetics and Biometry Laboratory, University of Geneva, Geneva.
Shields, G. F. and Wilson, A. C.: 1987, ‘Calibration of Mitochondrial DNA Evolution in Geese’, J. Mol. Evol.24, 212–217.
Sorenson, M. D., Ast, J. C., Dimcheff, D. E., Yuri, T., and Mindell, D. P.:1999, ‘Primers for a PCR-Based Approach to Mitochondrial Genome Sequencing in Birds and Other Vertebrates’, Mol. Phylogen. Evol.12, 105–114.
Stewart, J. R. and Lister, A. M.: 2001, ‘Cryptic Northern Refugia and the Origins of the Modern Biota’, Trends Ecol. Evol.16, 608–613.
Swofford, D. L.: 2001, Phylogenetic Analysis using Parsimony and other methods, ver. 4.0b10,Sinauer, Sunderland.
Taberlet, P. and Cheddadi, R.: 2002, ‘Quaternary Refugia and Persistence of Biodiversity’, Science297, 2009–2010.
Tajima, F.: 1989, ‘Statistical Method for Testing the Neutral Mutation Hypothesis of DNA Polymorphism’, Genetics123, 585–595.
Tarr, C. L. and Fleischer, R. C.: 1993, ‘Mitochondrial-DNA Variation and Evolutionary Relationships in the Amakihi Complex’, Auk110, 825–831.
Tzedakis, P. C., Lawson, I. T., Frogley, M. R., Hewitt, G. M., and Preece, R. C.: 2002, ‘Buffered Tree Population Changes in a Quaternary Refugium: Evolutionary Implications’, Science297, 2044–2047.
Williams, M., Dunkerley, D., De Deckker, P., Kershaw, P., and Chappell, J.: 1998, Quaternary Environments, 2nd edn., Arnold, London.
Zink, R. M. and Blackwell, R. C.: 1998, ‘Molecular Systematics of the Scaled Quail Complex Genus Callipepla’, Auk115, 394–403.
Zhaxybayeva, O. and Gogarten, J. P.: 2002, ‘Bootstrap, Bayesian Probability and Maximum Likelihood Mapping: Exploring New Tools for Comparative Genome Analyses’, BMC Genomics3, 4.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pruett, C.L., Winker, K. Biological Impacts of Climatic Change on a Beringian Endemic: Cryptic Refugia in the Establishment and Differentiation of the Rock Sandpiper (Calidris Ptilocnemis). Climatic Change 68, 219–240 (2005). https://doi.org/10.1007/s10584-005-1584-4
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/s10584-005-1584-4