Contrasting patterns of genetic diversity across the ranges of Pinus monticola and P. strobus: A comparison between eastern and western North American postglacial colonization histories

American Journal of Botany

Volumn 102, Issue 8, 2015, Pages 1342-1355

  Nadeau, Simon ^a,b   Godbout, Julie ^b   Lamothe, Manuel ^b   Gros Louis, Marie Claude ^b   Isabel, Nathalie ^b   Ritland, Kermit ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b LAURENTIAN FORESTRY CENTRE   (Canada)

Author keywords

cryptic refugium; glacial refugium; landscape genetics; long distance dispersal; phylogeography; Pinaceae; Pinus monticola; Pinus strobus; population structure; postglacial colonization

Indexed keywords

MONTICOLA; PINACEAE; PINUS MONTICOLA; PINUS STROBUS; STROBUS;

VEGETABLE PROTEIN;

CANADA; CLIMATE CHANGE; GENETIC VARIATION; GENETICS; METABOLISM; PHYSIOLOGY; PINE; PLANT DISPERSAL; SINGLE NUCLEOTIDE POLYMORPHISM; UNITED STATES;

CANADA; CLIMATE CHANGE; GENETIC VARIATION; PINUS; PLANT DISPERSAL; PLANT PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; UNITED STATES;

EID: 84947102216     PISSN: 00029122     EISSN: 15372197     Source Type: Journal    
DOI: 10.3732/ajb.1500160     Document Type: Article

References (103)

1. Barnosky, C. W. 1981. A record of late Quaternary vegetation from Davis Lake, southern Puget Lowland, Washington. Quaternary Research 16: 221–239.
2. Barnosky, C. W. 1985. Late Quaternary vegetation near Battle Ground Lake, southern Puget Trough, Washington. Geological Society of America Bulletin 96: 263–271.
3. Beatty, G. E., and J. Provan. 2011. Phylogeographic analysis of North American populations of the parasitic herbaceous plant Monotropa hypopitys L. reveals a complex history of range expansion from multiple late glacial refugia. Journal of Biogeography 38: 1585–1599.
4. Beaulieu, J., and J.-P. Simon. 1994. Genetic structure and variability in Pinus strobus in Quebec. Canadian Journal of Forest Research 24: 1726–1733.
5. Beaulieu, J., and J.-P. Simon. 1995. Mating system in natural populations of eastern white pine in Quebec. Canadian Journal of Forest Research 25: 1697–1703.
6. Bialozyt, R., B. Ziegenhagen, and R. J. Petit. 2006. Contrasting effects of long distance seed dispersal on genetic diversity during range expansion. Journal of Evolutionary Biology 19: 12–20.
7. Bohrerova, Z., G. Bohrer, K. D. Cho, M. A. Bolch, and K. G. Linden. 2009. Determining the viability response of pine pollen to atmospheric conditions during long-distance dispersal. Ecological Applications 19: 656–667.
8. Brunsfeld, S. J., T. R. Miller, and B. C. Carstens. 2007. Insights into the biogeography of the Pacific Northwest of North America: Evidence from the phylogeography of Salix melanopsis. Systematic Botany 32: 129–139.
9. Brunsfeld, S. J., J. Sullivan, D. E. Soltis, and P. S. Soltis. 2001. Comparative phylogeography of north- western North America: a synthesis. In J. Silvertown and J. Antonovics [eds.], Integrating ecological and evolutionary processes in a spatial context, 319–339. Blackwell, Oxford, UK.
10. Clark, P. U., A. S. Dyke, J. D. Shakun, A. E. Carlson, J. Clark, B. Wohlfarth, and J. X. Mitrovica et al. 2009. The Last Glacial Maximum. Science 325: 710–714.
11. Critchfield, W. B., and E. L. Little. 1966. Geographic distribution of the pines of the world. Miscellaneous Publication 991. USDA Forest Service, Washington, D.C., USA.
12. Cwynar, L. C. 1987. Fire and the forest history of the North Cascade Range. Ecology 68: 791–802.
13. Cwynar, L. C., and G. M. MacDonald. 1987. Geographical variation of lodgepole pine in relation to population history. American Naturalist 129: 463–469.
14. Davis, M. B. 1983. Quaternary history of deciduous forests of eastern North America and Europe. Annals of the Missouri Botanical Garden 70: 550–563.
15. Dyke, A. S., A. Moore, and L. Robertson. 2003. Deglaciation of North America. Open File 1574. Geological Survey of Canada, Ottawa, Ontario, Canada.
16. Earl, D. A., and B. M. VonHoldt. 2012. STRUCTURE HARVESTER: A website and program for visualizing structure output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.
17. Eckert, A. J., A. D. Bower, S. C. González-Martínez, J. L. Wegrzyn, G. Coop, and D. B. Neale. 2010a. Back to nature: Ecological genomics of loblolly pine (Pinus taeda, Pinaceae). Molecular Ecology 19: 3789–3805.
18. Eckert, A. J., A. D. Bower, K. D. Jermstad, J. L. Wegrzyn, B. J. Knaus, J. V. Syring, and D. B. Neale. 2013. Multilocus analyses reveal little evidence for lineage-wide adaptive evolution within major clades of soft pines (Pinus subgenus Strobus). Molecular Ecology 22: 5635–5650.
19. Eckert, A. J., van Heerwaarden J., J. L. Wegrzyn, C. D. Nelson, J. Ross-Ibarra, S. C. González-Martínez, and D. B. Neale 2010b. Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda L., Pinaceae). Genetics 185: 969–982.
20. Eckert, A. J., J. L. Wegrzyn, B. Pande, K. D. Jermstad, J. M. Lee, J. D. Liechty, and B. R. Tearse et al. 2009. Multilocus patterns of nucleotide diversity and divergence reveal positive selection at candidate genes related to cold hardiness in coastal Douglas fir (Pseudotsuga menziesii var. menziesii). Genetics 183: 289–298.
21. El-Kassaby, Y. A., M. D. Meagher, and R. Davidson. 1993. Temporal variation in the outcrossing rate in a natural stand of western white pine. Silvae Genetica 42: 131–135.
22. Evanno, G., S. Regnaut, and J. Goudet. 2005. Detecting the number of clusters of individuals using the software structure: A simulation study. Molecular Ecology 14: 2611–2620.
23. Eveno, E., C. Collada, M. A. Guevara, V. Léger, A. Soto, L. Díaz, and P. Léger et al. 2008. Contrasting patterns of selection at Pinus pinaster Ait. Drought stress candidate genes as revealed by genetic differentiation analyses. Molecular Biology and Evolution 25: 417–437.
24. Excoffier, L., M. Foll, and R. J. Petit. 2009. Genetic consequences of range expansions. Annual Review of Ecology, Evolution and Systematics 40: 481–501.
25. Excoffier, L., and H. E. L. Lischer. 2010. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.
26. 14C dates on pristine corals. Quaternary Science Reviews 24: 1781–1796.
27. Falush, D., M. Stephens, and J. K. Pritchard. 2003. Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164: 1567–1587.
28. Fayard, J., E. K. Klein, and F. Lefèvre. 2009. Long distance dispersal and the fate of a gene from the colonization front. Journal of Evolutionary Biology 22: 2171–2182.
29. Gernandt, D. S., S. Magallón, G. Geada López, O. Zerón Flores, A. Willyard, and A. Liston. 2008. Use of simultaneous analyses to guide fossil-based calibrations of Pinaceae phylogeny. International Journal of Plant Sciences 169: 1086–1099.
30. Godbout, J., A. Fazekas, C. H. Newton, F. C. Yeh, and J. Bousquet. 2008. Glacial vicariance in the Pacific Northwest: Evidence from a lodgepole pine mitochondrial DNA minisatellite for multiple genetically distinct and widely separated refugia. Molecular Ecology 17: 2463–2475.
31. Godbout, J., J. P. Jaramillo-Correa, J. Beaulieu, and J. Bousquet. 2005. A mitochondrial DNA minisatellite reveals the postglacial history of jack pine (Pinus banksiana), a broad-range North American conifer. Molecular Ecology 14: 3497–3512.
32. Graham, R. T. 1990. Pinus monticola Dougl. ex D. Don, western white pine. In R. M. Burns and B. H. Honkala [technical coordinators], Silvics of North America, vol. 1, 385–394. Agriculture Handbook 654. USDA Forest Service, Washington, D.C., USA.
33. Gray, L. K., and A. Hamann. 2013. Tracking suitable habitat for tree populations under climate change in western North America. Climatic Change 117: 289–303.
34. Grigg, L. D., and C. Whitlock. 1998. Late-glacial vegetation and climate change in western Oregon. Quaternary Research 49: 287–298.
35. Grivet, D., F. Sebastiani, R. Alía, T. Bataillon, S. Torre, M. Zabal-Aguirre, G. G. Vendramin, and S. C. González-Martínez 2011. Molecular footprints of local adaptation in two Mediterranean conifers. Molecular Biology and Evolution 28: 101–116.
36. Hampe, A., and R. J. Petit. 2005. Conserving biodiversity under climate change: The rear edge matters. Ecology Letters 8: 461–467.
37. Hewitt, G. M. 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society 58: 247–276.
38. Hewitt, G. M. 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907–913.
39. Hoban, S. M., D. S. Borkowski, S. L. Brosi, T. S. McCleary, L. M. Thompson, J. S. McLachlan, and M. A. Pereira et al. 2010. Range-wide distribution of genetic diversity in the North American tree Juglans cinerea: A product of range shifts, not ecological marginality or recent population decline. Molecular Ecology 19: 4876–4891.
40. Hoban, S., and S. Schlarbaum. 2014. Optimal sampling of seeds from plant populations for ex-situ conservation of genetic biodiversity, considering realistic population structure. Biological Conservation 177: 90–99.
41. Holliday, V. T., J. C. Knox, Running G. L. IV, R. D. Mandel, and C. R. Ferring. 2002. The Central Lowlands and Great Plains. In A. Orme [ed.], The physical geography of North America, 335–362. Oxford University Press, Oxford, UK.
42. Hubisz, M. J., D. Falush, M. Stephens, and J. K. Pritchard. 2009. Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9: 1322–1332.
43. Ibrahim, K. M., R. A. Nichols, and G. M. Hewitt. 1996. Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77: 282–291.
44. Isabel, N., J. Beaulieu, P. Thériault, and J. Bousquet. 1999. Direct evidence for biased gene diversity estimates from dominant random amplified polymorphic DNA (RAPD) fingerprints. Molecular Ecology 8: 477–483.
45. Jackson, S. T., J. T. Overpeck, Webb T. III, S. E. Keattch, and K. H. Anderson. 1997. Mapped plant-macrofossil and pollen records of late quaternary vegetation change in eastern North America. Quaternary Science Reviews 16: 1–70.
46. Jackson, S. T., R. S. Webb, K. H. Anderson, J. T. Overpeck, Webb T. III, J. W. Williams, and B. C. S. Hansen. 2000. Vegetation and environment in Eastern North America during the last glacial maximum. Quaternary Science Reviews 19: 489–508.
47. Jacobson, G. L., and A. Dieffenbacher-Krall. 1995. White pine and climate change—Insights from the past. Journal of Forestry 93: 39–42.
48. Jaramillo-Correa, J. P., J. Beaulieu, and J. Bousquet. 2004. Variation in mitochondrial DNA reveals multiple distant glacial refugia in black spruce (Picea mariana), a transcontinental North American conifer. Molecular Ecology 13: 2735–2747.
49. Jaramillo-Correa, J. P., J. Beaulieu, D. P. Khasa, and J. Bousquet. 2009. Inferring the past from the present phylogeographic structure of North American forest trees: Seeing the forest for the genes. Canadian Journal of Forest Research 39: 286–307.
50. Jermstad, K. D., A. J. Eckert, J. L. Wegrzyn, A. Delfino-Mix, D. A. Davis, D. C. Burton, and D. B. Neale. 2011. Comparative mapping in Pinus: Sugar pine (Pinus lambertiana Dougl.) and loblolly pine (Pinus taeda L.). Tree Genetics & Genomes 7: 457–468.
51. Joyce, D. G., and G. E. Rehfeldt. 2013. Climatic niche, ecological genetics, and impact of climate change on eastern white pine (Pinus strobus L.): Guidelines for land managers. Forest Ecology and Management 295: 173–192.
52. Keir, K. R., J. B. Bemmels, and S. N. Aitken. 2011. Low genetic diversity, moderate local adaptation, and phylogeographic insights in Cornus nuttallii (Cornaceae). American Journal of Botany 98: 1327–1336.
53. Kim, M.-S., B. A. Richardson, G. I. McDonald, and N. B. Klopfenstein. 2011. Genetic diversity and structure of western white pine (Pinus monticola) in North America: A baseline study for conservation, restoration, and addressing impacts of climate change. Tree Genetics & Genomes 7: 11–21.
54. Kremer, A., O. Ronce, J. J. Robledo-Arnuncio, F. Guillaume, G. Bohrer, R. Nathan, and J. R. Bridle et al. 2012. Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecology Letters 15: 378–392.
55. Liston, A., M. Parker-Defeniks, J. V. Syring, A. Willyard, and R. Cronn. 2007. Interspecific phylogenetic analysis enhances intraspecific phylogeographical inference: A case study in Pinus lambertiana. Molecular Ecology 16: 3926–3937.
56. Lorenz, T. J., K. A. Sullivan, A. V. Bakian, and C. A. Aubry. 2011. Cache-site selection in Clark's Nutcracker (Nucifraga columbiana). American Ornithologists' Union 128: 237–247.
57. MacDonald, G. M., L. C. Cwynar, and C. Whitlock. 1998. The late Quaternary dynamics of pines in northern North America. In D. M. Richardson [ed.], Ecology and biogeography of Pinus, 122–136. Cambridge University Press, Cambridge, UK.
58. Mandák, B., V. Hadincová, V. Mahelka, and R. Wildová 2013. European invasion of North American Pinus strobus at large and fine scales: High genetic diversity and fine-scale genetic clustering over time in the adventive range. PLoS One 8: e68514.
59. McLachlan, J. S., J. S. Clark, and P. S. Manos. 2005. Molecular indicators of tree migration capacity under rapid climate change. Ecology 86: 2088–2098.
60. Mee, J. A., and J.-S. Moore. 2014. The ecological and evolutionary implications of microrefugia. Journal of Biogeography 41: 837–841.
61. Mehes, M. S., K. K. Nkongolo, and P. Michael. 2007. Genetic analysis of Pinus strobus and Pinus monticola populations from Canada using ISSR and RAPD markers: Development of genome-specific SCAR markers. Plant Systematics and Evolution 267: 47–63.
62. Mehes, M., K. K. Nkongolo, and P. Michael. 2009. Assessing genetic diversity and structure of fragmented populations of eastern white pine (Pinus strobus) and western white pine (P. monticola) for conservation management. Journal of Plant Ecology 2: 143–151.
63. Miller, M. P. 2005. Alleles in Space (AIS): Computer software for the joint analysis of interindividual spatial and genetic information. Journal of Heredity 96: 722–724.
64. Naydenov, K., S. Senneville, J. Beaulieu, F. Tremblay, and J. Bousquet. 2007. Glacial vicariance in Eurasia: Mitochondrial DNA evidence from Scots pine for a complex heritage involving genetically distinct refugia at mid-northern latitudes and in Asia Minor. BMC Evolutionary Biology 7: 233.
65. Newton, A. C., T. R. Allnutt, A. C. M. Gillies, A. J. Lowe, and R. A. Ennos. 1999. Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends in Ecology & Evolution 14: 140–145.
66. Noss, R. F. 2001. Beyond Kyoto: Forest management in a time of rapid climate change. Conservation Biology 15: 578–590.
67. Pavy, N., J. Laroche, P. Rigault, N. Isabel, and J. Bousquet. 2012. A spruce gene map indicates ancient plant genome reshuffling and slow evolution in the gymnosperm lineage leading to extant conifers. BMC Biology 10: 84.
68. Petit, R. J., I. Aguinagalde, de Beaulieu J.-L., C. Bittkau, S. Brewer, R. Cheddadi, and R. Ennos et al. 2003. Glacial refugia: Hotspots but not melting pots of genetic diversity. Science 300: 1563–1565.
69. Petit, R. J., U. M. Csaikl, S. Bordács, K. Burg, E. Coart, J. Cottrell, van Dam B. et al. 2002. Chloroplast DNA variation in European white oaks: Phylogeography and patterns of diversity based on data from over 2600 populations. Forest Ecology and Management 156: 5–26.
70. Petit, R. J., F. S. Hu, and C. W. Dick. 2008. Forests of the past: A window to future changes. Science 320: 1450–1452.
71. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.
72. Provan, J., and K. D. Bennett. 2008. Phylogeographic insights into cryptic glacial refugia. Trends in Ecology & Evolution 23: 564–571.
73. R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
74. Rajora, O. P., L. DeVerno, A. Mosseler, and D. J. Innes. 1998. Genetic diversity and population structure of disjunct Newfoundland and central Ontario populations of eastern white pine (Pinus strobus). Canadian Journal of Botany 76: 500–508.
75. Ray, N., and L. Excoffier. 2010. A first step towards inferring levels of long-distance dispersal during past expansions. Molecular Ecology Resources 10: 902–914.
76. Raymond, M., and F. Rousset. 1995. GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248–249.
77. Rehfeldt, G. E., R. J. Hoff, and R. J. Steinhoff. 1984. Geographic patterns of genetic variation in Pinus monticola. Botanical Gazette 145: 229–239.
78. Remington, C. L. 1968. Suture-zones of hybrid interaction between recently joined biotas. In T. Dobzhansky, M. K. Hecht, and W. C. Steere [eds.], Evolutionary biology, 321–428. Springer, New York, New York, USA.
79. Richardson, B. A., S. J. Brunsfeld, and N. B. Klopfenstein. 2002. DNA from bird-dispersed seed and wind-disseminated pollen provides insights into postglacial colonization and population genetic structure of whitebark pine (Pinus albicaulis). Molecular Ecology 11: 215–227.
80. Richardson, B. A., G. E. Rehfeldt, and M.-S. Kim. 2009. Congruent climate-related genecological responses from molecular markers and quantitative traits for western white pine (Pinus monticola). International Journal of Plant Sciences 170: 1120–1131.
81. Roberts, D. R., and A. Hamann. 2015. Glacial refugia and modern genetic diversity of 22 western North American tree species. Proceedings of the Royal Society, B, Biological Sciences 282: 20142903.
82. Robledo-Arnuncio, J. J. 2011. Wind pollination over mesoscale distances: an investigation with Scots pine. New Phytologist 190: 222–233.
83. Rousset, F. 2008. genepop’007: A complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources 8: 103–106.
84. Shafer, A. B. A., C. I. Cullingham, S. D. Côté, and D. W. Coltman. 2010. Of glaciers and refugia: A decade of study sheds new light on the phylogeography of northwestern North America. Molecular Ecology 19: 4589–4621.
85. Soltis, D. E., M. A. Gitzendanner, D. D. Strenge, and P. S. Soltis. 1997. Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America. Plant Systematics and Evolution 206: 353–373.
86. Soltis, D. E., A. B. Morris, J. S. McLachlan, P. S. Manos, and P. S. Soltis. 2006. Comparative phylogeography of unglaciated eastern North America. Molecular Ecology 15: 4261–4293.
87. Steinhoff, R. J., D. G. Joyce, and L. Fins. 1983. Isozyme variation in Pinus monticola. Canadian Journal of Forest Research 13: 1122–1132.
88. Storey, J. D. 2002. A direct approach to false discovery rates. Journal of the Royal Statistical Society, B, Statistical Methodology 64: 479–498.
89. Storey, J. D., and R. Tibshirani. 2003. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences, USA 100: 9440–9445.
90. Svenning, J.-C., and F. Skov. 2007. Ice age legacies in the geographical distribution of tree species richness in Europe. Global Ecology and Biogeography 16: 234–245.
91. Swenson, N. G., and D. J. Howard. 2005. Clustering of contact zones, hybrid zones, and phylogeographic breaks in North America. American Naturalist 166: 581–591.
92. Thayer, T. C., and S. B. Vander Wall. 2005. Interactions between Steller's Jays and yellow pine chipmunks over scatter-hoarded sugar pine seeds. Journal of Animal Ecology 74: 365–374.
93. Vander Wall, S. B., and R. P. Balda. 1977. Co-adaptations of Clark's Nutcracker and pinon pine for efficient seed harvest and dispersal. Ecological Monographs 47: 89–111.
94. Vander Wall, S. B., and R. P. Balda. 1981. Ecology and evolution of food storing behavior in conifer-seed-caching corvids. Zeitschrift für Tierpsychologie 56: 217–242.
95. Varis, S., A. Pakkanen, A. Galofré, and P. Pulkkinen. 2009. The extent of south–north pollen transfer in Finnish Scots pine. Silva Fennica 43: 717–726.
96. Wainman, N., and R. W. Mathewes. 1987. Forest history of the last 12,000 years based on plant macrofossil analysis of sediment from Marion Lake, southwestern British Columbia. Canadian Journal of Botany 65: 2179–2187.
97. Walter, R., and B. K. Epperson. 2005. Geographic pattern of genetic diversity in Pinus resinosa: Contact zone between descendants of glacial refugia. American Journal of Botany 92: 92–100.
98. Wang, T., E. M. Campbell, G. A. O'Neill, and S. N. Aitken. 2012. Projecting future distributions of ecosystem climate niches: Uncertainties and management applications. Forest Ecology and Management 279: 128–140.
99. Warnes, G., G. Gorjanc, L. Friedrich, and M. Man. 2013. Genetics: Population genetics. R package version 1.3.8.1. R Foundation for Statistical Computing, Vienna, Austria. Website https://cran.r-project.org/web/packages/genetics/index.html.
100. Weir, B. S., and C. C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.
101. Wellner, C. A. 1965. Silvics of western white pine (Pinus monticola Dougl.). In H. A. Fowells [comp.], Silvics of forest trees of the United States, 478–487. Agriculture Handbook 271. USDA Forest Service, Washington, D.C., USA.
102. Wendel, G. W., and H. C. Smith. 1990. Pinus strobus L., eastern white pine. In R. M. Burns, and B. H. Honkala [eds.], Silvics of North America, vol. 1, 476–488. Agriculture Handbook 654. USDA Forest Service, Washington, D.C., USA.
103. Williams, J. W. 2003. Variations in tree cover in North America since the last glacial maximum. Global and Planetary Change 35: 1–23.