Isolation and introgression in the Intermountain West: Contrasting gene genealogies reveal the complex biogeographic history of the American pika (Ochotona princeps)

Journal of Biogeography

Volumn 37, Issue 2, 2010, Pages 344-362

  Galbreath, Kurt E ^a,b   Hafner, David J ^c   Zamudio, Kelly R ^a   Agnew, Kelly ^d  

^a Department of Obstetrics Gynecology   (United States)

^b WESTERN WASHINGTON UNIVERSITY   (United States)

^c UNIVERSITY OF NEW MEXICO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alpine; Coalescent simulation; Glaciation; Lagomorpha; Ochotona princeps; Pleistocene; Rocky Mountains; Sierra Nevada; Statistical phylogeography

Indexed keywords

ALPINE ENVIRONMENT; BAYESIAN ANALYSIS; CLIMATE EFFECT; COLONIZATION; GENEALOGY; GLACIATION; HISTORICAL PERSPECTIVE; INTROGRESSION; ISOLATION EFFECT; LAGOMORPH; MITOCHONDRIAL DNA; PHYLOGENETICS; PLEISTOCENE; RANGE EXPANSION; SMALL MAMMAL; TAXONOMY; ZOOGEOGRAPHY;

INTERMOUNTAIN WEST; ROCKY MOUNTAINS;

LAGOMORPHA; OCHOTONA PRINCEPS; OCHOTONIDAE;

EID: 74849115408     PISSN: 03050270     EISSN: 13652699     Source Type: Journal    
DOI: 10.1111/j.1365-2699.2009.02201.x     Document Type: Article

References (104)

1. Adams, K.D. Wesnousky, S.G. (1999) The Lake Lahontan highstand: age, surficial characteristics, soil development, and regional shoreline correlation. Geomorphology, 30, 357 392.
2. Albach, D.C., Schönswetter, P. Tribsch, A. (2006) Comparative phylogeography of the Veronica alpina complex in Europe and North America. Molecular Ecology, 15, 3269 3286.
3. Arbogast, B.S. Kenagy, G.J. (2001) Comparative phylogeography as an integrative approach to historical biogeography. Journal of Biogeography, 28, 819 825.
4. Avise, J.C. (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA.
5. Beever, E.A., Brussard, P.E. Berger, J. (2003) Patterns of apparent extirpation among isolated populations of pikas (Ochotona princeps) in the Great Basin. Journal of Mammalogy, 84, 37 54.
6. Booth, D.B., Troost, K.G., Clague, J.J. Waitt, R.B. (2004) The Cordilleran ice sheet. Developments in Quaternary science 1: the Quaternary period in the United States (ed. by A.R. Gillespie, S.C. Porter B.F. Atwater pp. 17 44. Elsevier, Amsterdam.
7. Bradley, R.D., Bull, J.J., Johnson, A.D. Hillis, D.M. (1993) Origin of a novel allele in a mammalian hybrid zone. Proceedings of the National Academy of Sciences USA, 90, 8939 8941.
8. Briggs, R.W., Wesnousky, S.G. Adams, K.D. (2005) Late Pleistocene and late Holocene lake highstands in the Pyramid Lake subbasin of Lake Lahontan, Nevada, USA. Quaternary Research, 64, 257 263.
9. Brouillet, L. Whetstone, R.D. (1993) Climate and physiography. Flora of North America north of Mexico (ed. by FONAE Committee pp. 15 46. Oxford University Press, New York.
10. Brown, J.H. (1971) Mammals on mountaintops: nonequilibrium insular biogeography. The American Naturalist, 105, 467 478.
11. Brunsfeld, S.J., Sullivan, J., Soltis, D.E. Soltics, P.S. (2001) Comparative phylogeography of northwestern North America. Integrating ecological and evolutionary processes in a spatial context (ed. by J. Silvertown J. Antonovics pp. 319 339. Blackwell Science, Oxford.
12. Carstens, B.C. Knowles, L.L. (2007) Shifting distributions and speciation: species divergence during rapid climate change. Molecular Ecology, 16, 619 627.
13. Carstens, B.C. Richards, C.L. (2007) Integrating coalescent and ecological niche modeling in comparative phylogeography. Evolution, 61, 1439 1454.
14. Carstens, B.C., Brunsfeld, S.J., Demboski, J.R., Good, J.M. Sullivan, J. (2005) Investigating the evolutionary history of the Pacific Northwest mesic forest ecosystem: hypothesis testing within a comparative phylogeographic framework. Evolution, 59, 1639 1652.
15. Clement, M., Posada, D. Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657 1659.
16. DeChaine, E.G. Martin, A.P. (2004) Historic cycles of fragmentation and expansion in Parnassius smintheus (Papilionidae) inferred using mitochondrial DNA. Evolution, 58, 113 127.
17. DeChaine, E.G. Martin, A.P. (2005a) Historical biogeography of two alpine butterflies in the Rocky Mountains: broad-scale concordance and local-scale discordance. Journal of Biogeography, 32, 1943 1956.
18. DeChaine, E.G. Martin, A.P. (2005b) Marked genetic divergence among sky island populations of Sedum lanceolatum (Crassulaceae) in the Rocky Mountains. American Journal of Botany, 92, 477 486.
19. DeChaine, E.G. Martin, A.P. (2006) Using coalescent simulations to test the impact of Quaternary climate cycles on divergence in an alpine plant-insect association. Evolution, 60, 1004 1013.
20. Demboski, J.R. Cook, J.A. (2001) Phylogeography of the dusky shrew, Sorex monticolus (Insectivora, Soricidae): insight into deep and shallow history in northwestern North America. Molecular Ecology, 10, 1227 1240.
21. Dobeš, C., Mitchell-Olds, T. Koch, M.A. (2004a) Intraspecific diversification in North American Boechera stricta (=Arabis drummondii), Boechera×divaricarpa, and Boechera holboellii (Brassicaceae) inferred from nuclear and chloroplast molecular markers - an integrative approach. American Journal of Botany, 91, 2087 2101.
22. Dobeš, C.H., Mitchell-Olds, T. Koch, M.A. (2004b) Extensive chloroplast haplotype variation indicates Pleistocene hybridization and radiation of North American Arabis drummondii, A.×divaricarpa, and A. holboellii (Brassicaceae). Molecular Ecology, 13, 349 370.
23. Drummond, A.J. Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
24. Drummond, A.J., Nicholls, G.K., Rodrigo, A.G. Solomon, W. (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics, 161, 1307 1320.
25. Drummond, A.J., Rambaut, A., Shapiro, B. Pybus, O.G. (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22, 1185 1192.
26. Formozov, N.A., Grigor'eva, T.V. Surin, V.L. (2006) Molecular systematics of pikas of the subgenus Pika (Ochotona, Lagomorpha). Zoologichesky Zhurnal, 85, 1465 1473.
27. Galbreath, K.E. (2009) Of pikas and parasites: historical biogeography of an alpine host-parasite assemblage. PhD Thesis, Cornell University, Ithaca, NY.
28. Galbreath, K.E., Hafner, D.J. Zamudio, K. (2009) When cold is better: climate-driven elevation shifts yield complex patterns of diversification and demography in an alpine specialist (American pika, Ochotona princeps). Evolution doi :.
29. Godsey, H.S., Currey, D.R. Chan, M.A. (2005) New evidence for an extended occupation of the Provo shoreline and implications for regional climate change, Pleistocene Lake Bonneville, Utah, USA. Quaternary Research, 63, 212 223.
30. Good, J.M. Sullivan, J. (2001) Phylogeography of the red-tailed chipmunk (Tamias ruficaudus), a northern Rocky Mountain endemic. Molecular Ecology, 10, 2683 2695.
31. Good, J.M., Demboski, J.R., Nagorsen, D.W. Sullivan, J. (2003) Phylogeography and introgressive hybridization: chipmunks (genus Tamias) in the northern Rocky Mountains. Evolution, 57, 1900 1916.
32. Graham, R.W., Lundelius, E.L., Graham, M.A., Schroeder, E.K., Toomey, R.S., Anderson, E., Barnosky, A.D., Burns, J.A., Churcher, C.S., Grayson, D.K., Guthrie, R.D., Harington, C.R., Jefferson, G.T., Martin, L.D., McDonald, H.G., Morlan, R.E., Semken, H.A., Webb, S.D., Werdelin, L. Wilson, M.C. (1996) Spatial response of mammals to late Quaternary environmental fluctuations. Science, 272, 1601 1606.
33. Grayson, D.K. (2000) Mammalian responses to Middle Holocene climatic change in the Great Basin of the western United States. Journal of Biogeography, 27, 181 192.
34. Grayson, D.K. (2005) A brief history of Great Basin pikas. Journal of Biogeography, 32, 2103 2111.
35. Grayson, D.K. (2006) The Late Quaternary biogeographic histories of some Great Basin mammals (western USA). Quaternary Science Reviews, 25, 2964 2991.
36. Guralnick, R. (2007) Differential effects of past climate warming on mountain and flatland species distributions: a multispecies North American mammal assessment. Global Ecology and Biogeography, 16, 14 23.
37. Hafner, D.J. (1993) North American pika (Ochotona princeps) as a Late Quaternary biogeographic indicator species. Quaternary Research, 39, 373 380.
38. Hafner, D.J. (1994) Pikas and permafrost: post-Wisconsin historical zoogeography of Ochotona in the southern Rocky Mountains, USA. Arctic and Alpine Research, 26, 375 382.
39. Hafner, D.J. Riddle, B.R. (2005) Mammalian phylogeography and evolutionary history of northern Mexico's deserts. Biodiversity, ecosystems, and conservation in northern Mexico (ed. by J.-L.E. Cartron, G. Ceballos R.S. Felger pp. 225 245. Oxford University Press, New York.
40. Hafner, D.J. Sullivan, R.M. (1995) Historical and ecological biogeography of Nearctic pikas (Lagomorpha, Ochotonidae). Journal of Mammalogy, 76, 302 321.
41. Hasegawa, M., Kishino, H. Yano, T. (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, 160 174.
42. Heusser, C.J. (1983) Vegetational history of the northwestern United States including Canada. Late Quaternary environments of the United States, Vol. 1, The Late Pleistocene (ed. by S.C. Porter pp. 239 258. University of Minnesota Press, Minneapolis, MN.
43. Hey, J. Nielsen, R. (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics, 167, 747 760.
44. Hillis, D.M., Mable, B.K., Larson, A., Davis, S.K. Zimmer, E.A. (1996) Nucleic acids IV: sequencing and cloning. Molecular systematics (ed. by D.M. Hillis, C. Moritz B.K. Mable pp. 342 343. Sinauer Associates, Sunderland, MA.
45. Hoffman, S.M.G. Brown, W.M. (1995) The molecular mechanism underlying the 'rare allele phenomenon' in a subspecific hybrid zone of the California field mouse, Peromyscus californicus. Journal of Molecular Evolution, 41, 1165 1169.
46. Hoffmann, R.S. Smith, A.T. (2005) Lagomorpha. Mammal species of the world (ed. by D.E. Wilson D.M. Reeder pp. 185 211. Johns Hopkins University Press, Baltimore, MD.
47. Hudson, R.R. Kaplan, N.L. (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics, 111, 147 164.
48. Irwin, D.E. (2002) Phylogeographic breaks without geographic barriers to gene flow. Evolution, 56, 2383 2394.
49. Knowles, L.L. (2001) Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers. Molecular Ecology, 10, 691 701.
50. Knowles, L.L. (2004) The burgeoning field of statistical phylogeography. Journal of Evolutionary Biology, 17, 1 10.
51. Knowles, L.L. Maddison, W.P. (2002) Statistical phylogeography. Molecular Ecology, 11, 2623 2635.
52. Krajick, K. (2004) All downhill from here? Science, 303, 1600 1602.
53. Kumar, S., Tamura, K. Nei, M. (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics, 5, 150 163.
54. Kurtén, B. Anderson, E. (1980) Pleistocene mammals of North America. Columbia University Press, New York.
55. Lanave, C., Preparata, G., Saccone, C. Serio, G. (1984) A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution, 20, 86 93.
56. Lawlor, T.E. (1998) Biogeography of Great Basin mammals: paradigm lost? Journal of Mammalogy, 79, 1111 1130.
57. Lissovsky, A.A., Ivanova, N.V. Borisenko, A.V. (2007) Molecular phylogenetics and taxonomy of the subgenus Pika (Ochotona, Lagomorpha). Journal of Mammalogy, 88, 1195 1204.
58. MacArthur, R.A. Wang, L.C.H. (1974) Behavioral thermoregulation in the pika Ochotona princeps: a field study using radiotelemetry. Canadian Journal of Zoology, 52, 353 358.
59. Maddison, W.P. Maddison, D.R. (2008) Mesquite: a modular system for evolutionary analysis, v2.5. Available at: http://mesquiteproject.org (accessed 1 June 2008).
60. Marlowe, K. Hufford, L. (2008) Evolution of Synthyris sect. Dissecta (Plantaginaceae) on sky islands in the Northern Rocky Mountains. American Journal of Botany, 95, 381 392.
61. Martínez-Meyer, E. Peterson, A.T. (2006) Conservatism of ecological niche characteristics in North American plant species over the Pleistocene-to-Recent transition. Journal of Biogeography, 33, 1779 1789.
62. Matthee, C.A., van Vuuren, B.J., Bell, D. Robinson, T.J. (2004) A molecular supermatrix of the rabbits and hares (Leporidae) allows for the identification of five intercontinental exchanges during the Miocene. Systematic Biology, 53, 433 447.
63. Mead, J.I. (1987) Quaternary records of pika, Ochotona, in North America. Boreas, 16, 165 171.
64. Mead, J.I. Grady, F. (1996) Ochotona (Lagomorpha) from Late Quaternary cave deposits in eastern North America. Quaternary Research, 45, 93 101.
65. Merriam, C.H. (1899) Results of a biological survey of Mount Shasta, California. North American Fauna, No. 16, US Department of Agriculture, Division of Biological Survey, Washington, DC.
66. Moritz, C. (1994) Applications of mitochondrial DNA analysis in conservation: a critical review. Molecular Ecology, 3, 401 411.
67. Morrison, R.B. (ed.) (1991) Quaternary stratigraphic, hydrologic, and climate history of the Great Basin, with emphasis on Lake Lahontan, Bonneville and Tecopa. The geology of North America, Vol. K-2, Quaternary nonglacial geology; conterminous U.S., pp. 283 320. Geological Society of America, Boulder, CO.
68. Nielson, M., Lohman, K. Sullivan, J. (2001) Phylogeography of the tailed frog (Ascaphus truei): implications for the biogeography of the Pacific Northwest. Evolution, 55, 147 160.
69. Niu, Y.D., Wei, F.W., Li, M., Liu, X.M. Feng, Z.J. (2004) Phylogeny of pikas (Lagomorpha, Ochotona) inferred from mitochondrial cytochrome b sequences. Folia Zoologica, 53, 141 155. (Pubitemid 39040364)
70. O'Connor, J.E. (1993) Hydrology, hydraulics, and geomorphology of the Bonneville Flood. Special Paper 274. Geological Society of America, Boulder, CO.
71. O'Connor, J.E. Baker, V.R. (1992) Magnitudes and implications of peak discharges from glacial Lake Missoula. Geological Society of America Bulletin, 104, 267 279.
72. Oviatt, C.G. (1997) Lake Bonneville fluctuations and global climate change. Geology, 25, 155 158.
73. Peacock, M.M. (1997) Determining natal dispersal patterns in a population of North American pikas (Ochotona princeps) using direct mark-resight and indirect genetic methods. Behavioral Ecology, 8, 340 350.
74. Peterson, A.T., Soberón, J. Sánchez-Cordero, V. (1999) Conservatism of ecological niches in evolutionary time. Science, 285, 1265 1267.
75. Porter, S.C., Pierce, K.L. Hamilton, T.D. (1983) Late Wisconsin mountain glaciation in the western United States. Late Quaternary environments of the United States: Vol. 1, The Late Pleistocene (ed. by S.C. Porter pp. 71 111. University of Minnesota Press, Minneapolis, MN.
76. Posada, D. (2006) ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Research, 34, W700 W703.
77. Posada, D. Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817 818.
78. Rambaut, A. Drummond, A.J. (2004) Tracer v1.4. Available at: http://beast.bio.ed.ac.uk/Tracer (accessed 1 June 2008).
79. Rickart, E.A. (2001) Elevational diversity gradients, biogeography and the structure of montane mammal communities in the intermountain region of North America. Global Ecology and Biogeography, 10, 77 100.
80. Riddle, B.R. (1996) The molecular phylogeographic bridge between deep and shallow history in continental biotas. Trends in Ecology and Evolution, 11, 207 211.
81. Riddle, B.R. Hafner, D.J. (2006) A step-wise approach to integrating phylogeographic and phylogenetic biogeographic perspectives on the history of a core North American warm deserts biota. Journal of Arid Environments, 66, 435 461.
82. Riddle, B.R., Hafner, D.J., Alexander, L.F. Jaeger, J.R. (2000) Cryptic vicariance in the historical assembly of a Baja California Peninsular Desert biota. Proceedings of the National Academy of Sciences USA, 97, 14438 14443.
83. Rozas, J., Sánchez-DelBarrio, J.C., Messeguer, X. Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496 2497.
84. Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Lodge, D.M., Mooney, H.A., Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, B.H., Walker, M. Wall, D.H. (2000) Global biodiversity scenarios for the year 2100. Science, 287, 1770 1774.
85. Shields, G.F. Kocher, T.D. (1991) Phylogenetic relationships of North American ursids based on analysis of mitochondrial data. Evolution, 45, 218 221.
86. Slatkin, M. Maddison, W.P. (1989) A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics, 123, 603 613. (Pubitemid 19274683)
87. Smith, A.T. (1974) The distribution and dispersal of pikas: influences of behavior and climate. Ecology, 55, 1368 1376.
88. Smith, A.T. (1987) Population structure of pikas: dispersal versus philopatry. Mammalian dispersal patterns: the effects of social structure on population genetics (ed. by B.D. Chepko-Sade Z.T. Halpin pp. 128 142. University of Chicago Press, Chicago.
89. Smith, A.T. Ivins, B.L. (1983) Colonization in a pika population: dispersal vs. philopatry. Behavioral Ecology and Sociobiology, 13, 37 47.
90. Smith, A.T. Weston, M.L. (1990) Ochotona princeps. Mammalian Species, 352, 1 8.
91. Soltis, D.E., Gitzendanner, M.A., Strenge, D.D. Soltis, P.S. (1997) Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America. Plant Systematics and Evolution, 206, 353 373.
92. Somers, P. (1973) Dialects in southern Rocky Mountain pikas, Ochotona princeps (Lagomorpha). Animal Behaviour, 21, 124 137.
93. Spaulding, W.G., Leopold, E.B. Devender, T.R.V. (1983) Late Wisconsin paleoecology of the American Southwest. Late-Quaternary environments of the United States, Vol. 1, The Late Pleistocene (ed. by S.C. Porter pp. 259 293. University of Minnesota Press, Minneapolis, MN.
94. Spellman, G.M., Riddle, B. Klicka, J. (2007) Phylogeography of the mountain chickadee (Poecile gambeli): diversification, introgression, and expansion in response to Quaternary climate change. Molecular Ecology, 16, 1055 1068.
95. Stephens, M. Scheet, P. (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. American Journal of Human Genetics, 76, 449 462.
96. Stephens, M., Smith, N.J. Donnelly, P. (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978 989.
97. Swofford, D.L. (2000) PAUP*: phylogenetic analysis using parsimony (*and other methods), v4. Sinauer Associates, Sunderland, MA.
98. Thompson, J.D., Higgins, D.G. Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673 4680.
99. Waitt, R.B., Jr. (1985) Case for periodic, colossal jökulhlaups from Pleistocene glacial Lake Missoula. Geological Society of America Bulletin, 96, 1271 1286.
100. Watterson, G.A. Guess, H.A. (1977) Is the most frequent allele the oldest? Theoretical Population Biology, 11, 141 160.
101. Wiens, J.J. Graham, C.H. (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics, 36, 519 539.
102. Wilkinson, L. (1997) SYSTAT, v7. SPSS Inc., Chicago.
103. Wilson, G.M., Den Bussche, R.A., McBee, K., Johnson, L.A. Jones, C.A. (2005) Intraspecific phylogeography of red squirrels (Tamiasciurus hudsonicus) in the central Rocky Mountain region of North America. Genetica, 125, 141 154.
104. Zink, R.M. Barrowclough, G.F. (2008) Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology, 17, 2107 2121.