Skip to main content

Advertisement

SpringerLink
Log in

Nuclear genetic variation across the range of ponderosa pine (Pinus ponderosa): Phylogeographic, taxonomic and conservation implications

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Ponderosa pine (Pinus ponderosa) is among the most broadly distributed conifer species of western North America, where it possesses considerable ecological, esthetic, and commercial value. It exhibits complicated patterns of morphological and genetic variation, suggesting that it may be in the process of differentiating into distinct regional lineages. A robust analysis of genetic variation across the ponderosa pine complex is necessary to ensure the effectiveness of management and conservation efforts given the species’ large distribution, the existence of many isolated disjunct populations, and the potential susceptibility of some populations to climate change and other threats. We used highly polymorphic nuclear microsatellite markers and isozyme markers from 3113 trees in 104 populations to assess genetic variation and structure across the geographic range of ponderosa pine. The results reveal pervasive inbreeding and patterns of genetic diversity consistent with the hypothesis that ponderosa existed in small, as-yet-undetected Pleistocene glacial refugia north of southern Arizona and New Mexico. The substructuring of genetic variation within the species complex was consistent with its division into two varieties, with genetic clusters within varieties generally associated with latitudinal zones. The analyses indicate widespread gene flow and/or recent common ancestry among genetic clusters within varieties, but not between varieties. Isolated disjunct populations had lower genetic variation by some measures and greater genetic differentiation than main-range populations. These results should be useful for decision-making and conservation planning related to this widespread and important species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson RS (1989) Development of the southwestern ponderosa pine forests: What do we really know? In: Tecle A, Covington WW, Hamre RH (eds) Multiresource management of ponderosa pine forests. vol General Technical Report RM-185. United States Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station, Fort Collins, pp 15–22

    Google Scholar 

  • Anderson RS (1990) Holocene forest development and paleoclimates within the central Sierra Nevada, California. J Ecol 78(2):470–489

    Article  Google Scholar 

  • Anderson RS, Hasbargen J, Koehler PA, Feiler EJ (1999) Late Wisconsin and Holocene subalpine forests of the Markagunt Plateau of Utah, southwestern Colorado Plateau, USA. Arct Antarct Alp Res 31(4):366–378

    Article  Google Scholar 

  • Baker RG (1986) Sangamonian (questionable) and Wisconsinian paleoenvironments in Yellowstone National Park. Geol Soc Am Bull 97(6):717–736. doi:10.1130/0016-7606(1986)97<717:sawpiy>2.0.co;2

    Article  Google Scholar 

  • Barton NH, Slatkin M (1986) A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 56:409–415

    Article  PubMed  Google Scholar 

  • Betancourt JL (1990) Late Quaternary biogeography of the Colorado Plateau. In: Betancourt JL, Van Devender TR, Martin PS (eds) Packrat middens: the last 40,000 years of biotic change. The University of Arizona Press, Tucson, pp 259–292

    Google Scholar 

  • Betancourt JL, Van Devender TR, Martin PS (1990) Packrat middens: the last 40,000 years of biotic change. University of Arizona Press, Tucson

    Google Scholar 

  • Bialozyt R, Ziegenhagen B, Petit RJ (2006) Contrasting effects of long distance seed dispersal on genetic diversity during range expansion. J Evol Biol 19(1):12–20. doi:10.1111/j.1420-9101.2005.00995.x

    Article  CAS  PubMed  Google Scholar 

  • Boys J, Cherry M, Dayanandan S (2005) Microsatellite analysis reveals genetically distinct populations of red pine (Pinus resinosa Pinaceae). Am J Bot 92(5):833–841

    Article  CAS  PubMed  Google Scholar 

  • Brayshaw TC (1997) Washoe and ponderosa pines on Promontory Hill near Merritt, B.C., Canada. Ann Naturhist Mus Wien 99B:673–680

    Google Scholar 

  • Callaham RZ (2013a) Pinus ponderosa: a taxonomic review with five subspecies in the United States. U.S. Department of Agriculture Forest Service, Pacific Southwest Research Station, Albany

    Google Scholar 

  • Callaham RZ (2013b) Pinus ponderosa: geographic races and subspecies based on morphological variation. U.S. Department of Agriculture Forest Service, Pacific Southwest Research Station, Albany

    Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570

    Article  Google Scholar 

  • Chapman TB, Veblen TT, Schoennagel T (2012) Spatiotemporal patterns of mountain pine beetle activity in the southern Rocky Mountains. Ecology 93(10):2175–2185

    Article  PubMed  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24(3):621–631

    Article  CAS  PubMed  Google Scholar 

  • Cole K (1983) Late Pleistocene vegetation of Kings Canyon, Sierra Nevada, California. Quat Res 19(1):117–129. doi:10.1016/0033-5894(83)90031-5

    Article  Google Scholar 

  • Comes HP, Kadereit JW (1998) The effect of quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3(11):432–438

    Article  Google Scholar 

  • Conkle MT, Critchfield WB (1988) Genetic variation and hybridization of ponderosa pine. In: Baumgartner DM, Lotan JE (eds) Ponderosa pine: the species and its management. Washington State University Cooperative Extension, Pullman, pp 27–43

    Google Scholar 

  • Conkle MT, Hodgskiss PD, Nunnally LB, Hunter SC (1982) Starch Gel electrophoresis of conifer seeds: a laboratory manual. Pacific Southwest Forest and Range Experiment Station, United States Department of Agriculture Forest Service, Berkeley

    Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144(4):2001–2014

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10(3):556–557. doi:10.1111/j.1755-0998.2009.02801.x

    Article  PubMed  Google Scholar 

  • Critchfield WB (1984) Crossability and relationships of Washoe pine. Madrono 31(3):144–170

    Google Scholar 

  • Critchfield WB, Allenbaugh GL (1965) Washoe pine on the Bald Mountain Range, California. Madrono 18:63–64

    Google Scholar 

  • Critchfield WB, Little EL (1966) Geographic distribution of the pines of the world. United States Department of Agriculture Forest Service, Washington

    Book  Google Scholar 

  • Crookston NL, Rehfeldt GE, Dixon GE, Weiskittel AR (2010) Addressing climate change in the forest vegetation simulator to assess impacts on landscape forest dynamics. For Ecol Manag 260(7):1198–1211. doi:10.1016/j.foreco.2010.07.013

    Article  Google Scholar 

  • Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc Ser B-Methodol 39(1):1–38

    Google Scholar 

  • Dong JS, Wagner DB (1994) Paternally inherited chloroplast polymorphism in Pinus: Estimation of diversity and population subdivision, and tests of disequilibrium with a maternally inherited mitochondrial polymorphism. Genetics 136(3):1187–1194

    CAS  PubMed Central  PubMed  Google Scholar 

  • Durand E, Jay F, Gaggiotti OE, Francois O (2009) Spatial inference of admixture proportions and secondary contact zones. Mol Biol Evol 26(9):1963–1973. doi:10.1093/molbev/msp106

    Article  CAS  PubMed  Google Scholar 

  • Dvorak WS, Potter KM, Hipkins VD, Hodge GR (2009) Genetic diversity and gene exchange in Pinus oocarpa, a Mesoamerican pine with resistance to the pitch canker fungus (Fusarium circinatum). Int J Plant Sci 170(5):609–626. doi:10.1086/597780

    Article  Google Scholar 

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17(5):1170–1188

    Article  CAS  PubMed  Google Scholar 

  • Elsik CG, Williams CG (2001) Families of clustered microsatellites in a conifer genome. Mol Gen Genomics 265(3):535–542

    Article  CAS  Google Scholar 

  • Elsik CG, Minihan VT, Hall SE, Scarpa AM, Williams CG (2000) Low-copy microsatellite markers for Pinus taeda L. Genome 43(3):550–555

    Article  CAS  PubMed  Google Scholar 

  • Eriksson G, Namkoong G, Roberds JH (1993) Dynamic gene conservation for uncertain futures. For Ecol Manag 62(1–4):15–37

    Article  Google Scholar 

  • ESRI (2006) ArcMap 9.2. Environmental Systems Research Institute Inc., Redlands, California

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131(2):479–491

    CAS  PubMed Central  PubMed  Google Scholar 

  • Farjon A (1984) Pines: drawings and descriptions of the genus Pinus. E.J. Brill, Leiden

    Google Scholar 

  • Felsenstein J (2005) PHYLIP (Phylogeny Inference Package), version 3.6. Department of Genome Sciences, University of Washington, Seattle

    Google Scholar 

  • Gernandt DS, Hernandez-Leon S, Salgado-Hernandez E, de la Rosa JAP (2009) Phylogenetic relationships of Pinus subsection Ponderosae inferred from rapidly evolving cpDNA regions. Syst Bot 34(3):481–491

    Article  Google Scholar 

  • Gibson JP, Hamrick JL (1991) Genetic diversity and structure in Pinus pungens (Table Mountain pine) populations. Can J For Res-Revue Can De Rech Forestiere 21(5):635–642

    Article  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86(6):485–486

    Google Scholar 

  • Hale ML, Burg TM, Steeves TE (2012) Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population is enough to accurately estimate allele frequencies. Plos One 7(9). doi:10.1371/journal.pone.0045170

  • Haller JR (1965) The role of 2-needle fascicles in the adaptation and evolution of ponderosa pine. Brittonia 17(4):354–382

    Article  Google Scholar 

  • Hamrick JL, Blanton HM, Hamrick KJ (1989) Genetic structure of geographically marginal populations of ponderosa pine. Am J Bot 76(11):1559–1568. doi:10.2307/2444394

    Article  Google Scholar 

  • Hansen HP (1942) The influence of volcanic eruptions upon post-Pleistocene forest succession in Central Oregon. Am J Bot 29(3):214–219. doi:10.2307/2437672

    Article  Google Scholar 

  • Hansen HP (1947) Postglacial vegetation of the northern Great Basin. Am J Bot 34(3):164–171. doi:10.2307/2437371

    Article  Google Scholar 

  • Heuertz M, Hausman JF, Hardy OJ, Vendramin GG, Frascaria-Lacoste N, Vekemans X (2004) Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southeastern European populations of the common ash (Fraxinus excelsior L.). Evolution 58(5):976–988

    PubMed  Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58(3):247–276

    Article  Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405(6789):907–913

    Article  CAS  PubMed  Google Scholar 

  • Hoff RJ (1988) Susceptibility of ponderosa pine to the needle case fungus Lophodermium baculiferum. U.S. Department of Agriculture Forest Service, Intermountain Research Station, Ogden

    Google Scholar 

  • Huff DR, Peakall R, Smouse PE (1993) RAPD variation within and among natural populations of outcrossing buffalograss (Buchloe dactyloides (Nutt.) Engelm.). Theor Appl Genet 86(8):927–934. doi:10.1007/bf00211043

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291

    Article  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23(14):1801–1806. doi:10.1093/bioinformatics/btm233

    Article  CAS  PubMed  Google Scholar 

  • Jaramillo-Correa JP, Beaulieu J, Khasa DP, Bousquet J (2009) Inferring the past from the present phylogeographic structure of North American forest trees: seeing the forest for the genes. Can J For Res-Revue Can De Rech Forestiere 39(2):286–307. doi:10.1139/x08-181

    Article  Google Scholar 

  • Johansen AD, Latta RG (2003) Mitochondrial haplotype distribution, seed dispersal and patterns of postglacial expansion of ponderosa pine. Mol Ecol 12(1):293–298

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen SM, Hamrick JL (1997) Biogeography and population genetics of whitebark pine, Pinus albicaulis. Can J For Res 27(10):1574–1585

    Article  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17(18):4015–4026. doi:10.1111/j.1365-294X.2008.03887.x

    Article  PubMed  Google Scholar 

  • Kalinowski ST, Taper ML (2006) Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conserv Genet 7(6):991–995. doi:10.1007/s10592-006-9134-9

    Article  CAS  Google Scholar 

  • Karhu A, Vogl C, Moran GF, Bell JC, Savolainen O (2006) Analysis of microsatellite variation in Pinus radiata reveals effects of genetic drift but no recent bottlenecks. J Evol Biol 19(1):167–175

    Article  CAS  PubMed  Google Scholar 

  • Kitchen SG (2010) Historic Fire Regimes of Eastern Great Basin (USA) Mountains Reconstructed from Tree Rings. Ph.D. Dissertation, Brigham Young University, Provo, Utah

  • Kral R (1993) Pinus. In: Flora of North America Editorial Committee (ed) Flora of North America North of Mexico, vol Pteridophytes and Gymnosperms, Vol. 2. Oxford University Press, New York, pp 373–398

    Google Scholar 

  • La Farge T (1975) Genetic differences in stem form of ponderosa pine grown in Michigan. Silvae Genet 23:211–213

    Google Scholar 

  • Lascoux M, Palme AE, Cheddadi R, Latta RG (2004) Impact of Ice Ages on the genetic structure of trees and shrubs. Philos T Roy Soc B 359(1442):197–207. doi:10.1098/rstb.2003.1390

    Article  Google Scholar 

  • Latta RG, Mitton JB (1999) Historical separation and present gene flow through a zone of secondary contact in ponderosa pine. Evolution 53(3):769–776

    Article  Google Scholar 

  • Latta RG, Linhart YB, Fleck D, Elliot M (1998) Direct and indirect estimates of seed versus pollen movement within a population of ponderosa pine. Evolution 52(1):61–67

    Article  Google Scholar 

  • Lauria F (1997) The taxonomic status of Pinus washoensis H. Mason & Stockw. (Pinaceae). Ann Naturhist Mus Wien 99:655–671

    Google Scholar 

  • Lesser MR, Parchman TL, Buerkle CA (2012) Cross-species transferability of SSR loci developed from transciptome sequencing in lodgepole pine. Mol Ecol Resour 12(3):448–455. doi:10.1111/j.1755-0998.2011.03102.x

    Article  CAS  PubMed  Google Scholar 

  • Libiger O, Nievergelt CM, Schork NJ (2009) Comparison of genetic distance measures using human SNP genotype data. Hum Biol 81(4):389–406

    Article  PubMed  Google Scholar 

  • Liewlaksaneeyanawin C, Ritland CE, El-Kassaby YA, Ritland K (2004) Single-copy, species-transferable microsatellite markers developed from loblolly pine ESTs. Theor Appl Genet 109(2):361–369

    Article  CAS  PubMed  Google Scholar 

  • Littell JS, McKenzie D, Peterson DL, Westerling AL (2009) Climate and wildfire area burned in western U. S. ecoprovinces, 1916–2003. Ecol Appl 19(4):1003–1021. doi:10.1890/07-1183.1

    Article  PubMed  Google Scholar 

  • Little EL (1971) Atlas of United States Trees. Volume 1. Conifers and Important Hardwoods. Washington, D.C

  • Little EL (1979) Checklist of United States Trees (Native and Naturalized). United States Department of Agriculture, Washington

    Google Scholar 

  • Lorenz TJ, Aubry C, Shoal R (2008) A review of the literature on seed fate in whitebark pine and the life history traits of Clark’s nutcracker and pine squirrels. United States Department of Agriculture Forest Service, Pacific Northwest Research Station, Portland

    Google Scholar 

  • MacDonald GM, Cwynar LC, Whitlock C (1998) The late quaternary dynamics of pines in northern North America. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 122–136

    Google Scholar 

  • McLachlan JS, Clark JS, Manos PS (2005) Molecular indicators of tree migration capacity under rapid climate change. Ecology 86(8):2088–2098

    Article  Google Scholar 

  • Meddens AJH, Hicke JA, Ferguson CA (2012) Spatiotemporal patterns of observed bark beetle-caused tree mortality in British Columbia and the western United States. Ecol Appl 22(7):1876–1891

    Article  PubMed  Google Scholar 

  • Mitton JB, Ferrenberg SM (2012) Mountain pine beetle develops an unprecedented summer generation in response to climate warming. Am Nat 179(5):E163–E171. doi:10.1086/665007

    Article  PubMed  Google Scholar 

  • Moritz C (1994) Defining evolutionarily significant units for conservation. Trends Ecol Evol 9(10):373–375

    Article  CAS  PubMed  Google Scholar 

  • Neale DB, Sederoff RR (1989) Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor Appl Genet 77(2):212–216

    Article  CAS  PubMed  Google Scholar 

  • Niebling CR, Conkle MT (1990) Diversity of Washoe pine and comparisons with allozymes of ponderosa pine races. Can J For Res-Revue Can De Rech Forestiere 20(3):298–308. doi:10.1139/x90-044

    Article  Google Scholar 

  • Norris JR, Jackson ST, Betancourt JL (2006) Classification tree and minimum-volume ellipsoid analyses of the distribution of ponderosa pine in the western USA. J Biogeogr 33(2):342–360

    Article  Google Scholar 

  • O’Connell LM, Ritland K, Thompson SL (2008) Patterns of post-glacial colonization by western redcedar (Thuja plicata, Cupressaceae) as revealed by microsatellite markers. Botany 86(2):194–203. doi:10.1139/b07-124

    Article  Google Scholar 

  • Oliver WW, Ryker RA (1990) Ponderosa Pine. In: Burns RM, Honkala BH (eds) Silvics of North America: 1. Conifers, vol 1. Agricultural Handbook 654. U.S. Department of Agriculture Forest Service, Washington

    Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295. doi:10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  • Pearson RG (2006) Climate change and the migration capacity of species. Trends Ecol Evol 21(3):111–113. doi:10.1016/j.tree.2005.11.022

    Article  PubMed  Google Scholar 

  • Peloquin RL (1984) The identification of three-species hybrids in the ponderosa pine complex. Southw Nat 29(1):115–122. doi:10.2307/3670776

    Article  Google Scholar 

  • Perry JP (1991) The Pines of Mexico and Central America. Timber Press, Portland

    Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90(4):502–503

    Article  Google Scholar 

  • Pitel JA, Cheliak WM (1984) Effect of extraction buffers on characterization of isoenzymes from vegetative tissues of five conifer species: a user’s manual. Agriculture Canada, Canadian Forestry Service, Petawawa National Forestry Institute, Chalk River

    Google Scholar 

  • Porter SC (1989) Some geological implications of average quaternary glacial conditions. Quat Res 32(3):245–261. doi:10.1016/0033-5894(89)90092-6

    Article  Google Scholar 

  • Potter KM, Jetton RM, Dvorak WS, Hipkins VD, Rhea R, Whittier WA (2012) Widespread inbreeding and unexpected geographic patterns of genetic variation in eastern hemlock (Tsuga canadensis), an imperiled North American conifer. Conserv Genet 13(2):475–498. doi:10.1007/s10592-011-0301-2

    Article  Google Scholar 

  • Potter KM, Hipkins VD, Mahalovich MF, Means RE (2013) Mitochondrial DNA haplotype distribution patterns in Pinus ponderosa (Pinaceae): range-wide evolutionary history and implications for conservation. Am J Bot 100(8):1562–1579. doi:10.3732/ajb.1300039

    Article  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23(10):564–571. doi:10.1016/j.tree.2008.06.010

    Article  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) Genepop (version-1.2): population genetics software for exact tests and ecumenicism. J Hered 86(3):248–249

    Google Scholar 

  • Read RA (1980) Genetic variation in seedling progeny of ponderosa pine provenances vol Forest Science Monograph 23. Society of American Foresters, Washington

    Google Scholar 

  • Read RA (1983) Ten-year performance of ponderosa pine provenances in the great plains of North America. U.S. Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station, Fort Collins

    Book  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17(1):230–237

    Article  Google Scholar 

  • Rehfeldt GE (1990) Genetic differentiation among populations of Pinus ponderosa from the upper Colorado River basin. Bot Gaz 151(1):125–137

    Article  Google Scholar 

  • Rehfeldt GE (1991) A model of genetic variation for Pinus ponderosa in the Inland Northwest (U.S.A.): applications in gene resource management. Can J For Res 21(10):1491–1500

    Article  Google Scholar 

  • Rehfeldt GE (1993) Genetic variation in the Ponderosae of the Southwest. Am J Bot 80(3):330–343

    Article  Google Scholar 

  • Rehfeldt GE (1999a) Systematics and genetic structure of Ponderosae taxa (Pinaceae) inhabiting the mountain islands of the Southwest. Am J Bot 86(5):741–752

    Article  CAS  PubMed  Google Scholar 

  • Rehfeldt GE (1999b) Systematics and genetic structure of Washoe pine: applications in conservation genetics. Silvae Genet 48(3–4):167–173

    Google Scholar 

  • Rehfeldt GE, Wilson BC, Wells SP, Jeffers RM (1996) Phytogeographic, taxonomic, and genetic implications of phenotypic variation in the Ponderosae of the Southwest. Southwest Nat 41(4):409–418

    Google Scholar 

  • Rehfeldt GE, Crookston NL, Warwell MV, Evans JS (2006) Empirical analyses of plant-climate relationships for the western United States. Int J Plant Sci 167(6):1123–1150

    Article  Google Scholar 

  • Rehfeldt GE, Leites LP, St Clair JB, Jaquish BC, Saenz-Romero C, Lopez-Upton J, Joyce DG (2014a) Comparative responses to climate in the varieties of Pinus ponderosa and Pseudotsuga menziesii: clines in growth potential. For Ecol Manag 324:138–146

    Article  Google Scholar 

  • Rehfeldt GE, Leites LP, St Clair JB, Jaquish BC, Saenz-Romero C, Lopez-Upton J, Joyce DG (2014b) Comparative responses to climate in the varieties of Pinus ponderosa and Pseudotsuga menziesii: realized climate niches. For Ecol Manag 324:126–137

    Article  Google Scholar 

  • Rehfeldt GE, Leites LP, St Clair JB, Jaquish BC, Saenz-Romero C, Lopez-Upton J, Joyce DG (2014c) Comparative responses to climate in the varieties of Pinus ponderosa and Pseudotsuga menziesii: reforestation. For Ecol Manag 324:147–157

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  PubMed  Google Scholar 

  • SAS Institute Inc. (2008) The SAS System for Windows, Version 9.2. Cary, North Carolina

  • Sawyer JO (2007) Why are the Klamath Mountains and adjacent North Coast floristically diverse? Fremontia 35(3):3–11

    Google Scholar 

  • Schaberg PG, DeHayes DH, Hawley GJ, Nijensohn SE (2008) Anthropogenic alterations of genetic diversity within tree populations: implications for forest ecosystem resilience. For Ecol Manag 256(5):855–862. doi:10.1016/j.foreco.2008.06.038

    Article  Google Scholar 

  • Schmidtling RC, Hipkins VD (1998) Genetic diversity in longleaf pine (Pinus palustris): influence of historical and prehistorical events. Can J For Res-Revue Can De Rech Forestiere 28(8):1135–1145. doi:10.1139/cjfr-28-8-1135

    Article  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236(4803):787–792

    Article  CAS  PubMed  Google Scholar 

  • Smith RH (1977) Monoterpenes of ponderosa pine xylem resin in western United States. U.S. Department of Agriculture, Forest Service, Washington

    Google Scholar 

  • Smith RH, Peloquin RL, Passof PC (1969) Local and regional variation in the monoterpenes of ponderosa pine wood oleoresin. U.S. Department of Agriculture, Forest Service, Pacific Southwest Forest and Range Experiment Station, Berkeley

    Google Scholar 

  • Squillace AE, Silen RR (1962) Racial variation in ponderosa pine. For Sci Monogr 2(2):1–27

    Google Scholar 

  • Sturgeon KB (1979) Monoterpene variation in ponderosa pine xylem resin related to western pine beetle predation. Evolution 33(3):803–814. doi:10.2307/2407647

    Article  CAS  Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7(4):453–464

    Article  CAS  PubMed  Google Scholar 

  • Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144(1):389–399

    CAS  PubMed Central  PubMed  Google Scholar 

  • United States Department of Agriculture Forest Service (2012) National Forest Genetics Laboratory, Standard Operating Procedures. National Forest Genetics Laboratory, United States Department of Agriculture Forest Service, Placerville, California

  • Van Devender TR (1990) Late Quaternary vegetation and climate of the Chihuahuan desert, United States and Mexico. In: Betancourt JL, Van Devender TR, Martin PS (eds) Packrat middens: the last 40,000 years of biotic change. The University of Arizona Press, Tucson, pp 104–132

    Google Scholar 

  • Van Devender TR, Spaulding WG (1979) Development of vegegation and climate in the southwestern United States. Science 204(4394):701–710. doi:10.1126/science.204.4394.701

    Article  PubMed  Google Scholar 

  • Van Devender TR, Betancourt JL, Wimberly M (1984) Biogeographic implications of a packrat midden sequence from the Sacramento Mountains, south-central New Mexico. Quat Res 22(3):344–360. doi:10.1016/0033-5894(84)90028-0

    Article  Google Scholar 

  • Van Devender TR, Thompson RS, Betancourt JL (1987) Vegetation history of the deserts of southwestern North America: the nature and timing of the late Wisconsin-Holocene transition. In: Ruddiman WF, Wright HE Jr (eds) North America and adjacent oceans during the last deglaciation, vol the geology of north america, v. K-3. Geological Society of America, Boulder, pp 323–352

    Chapter  Google Scholar 

  • Van Haverbeke DF (1986) Genetic variation in ponderosa pine: a 15-year test of provenances in the great plains. U.S. Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station, Fort Collins

    Book  Google Scholar 

  • Wang C-W (1977) Genetics of ponderosa pine. U.S. Department of Agriculture, Forest Service, Washington

    Book  Google Scholar 

  • Weidman RH (1939) Evidences of racial influence in a 25-year test of ponderosa pine. J Agric Res 59:0855–0887

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370

    Article  Google Scholar 

  • Wells OO (1964) Geographic variation in ponderosa pine: I. The ecotypes and their distribution. Silvae Genet 13(4):89–103

    Google Scholar 

  • Whitlock C, Shafer SL, Marlon J (2003) The role of climate and vegetation change in shaping past and future fire regimes in the northwestern US and the implications for ecosystem management. For Ecol Manag 178(1–2):5–21. doi:10.1016/s0378-1127(03)00051-3

    Article  Google Scholar 

  • Willi Y, Van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Evol Syst 37:433–458

    Article  Google Scholar 

  • Willyard A, Cronn R, Liston A (2009) Reticulate evolution and incomplete lineage sorting among the ponderosa pines. Mol Phylogenet Evol 52(2):498–511. doi:10.1016/j.ympev.2009.02.011

    Article  CAS  PubMed  Google Scholar 

  • Wofford AM, Finch K, Bigott A, Willyard A (2014) A set of plastid loci for use in multiplex fragment length genotyping for intraspecific variation in Pinus (Pinaceace). Appl Plant Sci 2(5):XXX

  • Wright JW, Lemmien WA, Bright JN (1969) Early growth of ponderosa pine ecotypes in Michigan. For Sci 15(2):121–129

    Google Scholar 

Download references

Acknowledgments

The authors thank the natural resource specialists from government agencies who assisted with the identification and collection of samples. The authors thank Doug Page, Connie Millar, and David Charlet for multiple collections; Jody Mello, Rosanna Hanson, Ricardo Hernandez, Pat Guge, Suellen Carroll, Kristin Motz, Courtney Owens, and Sara Trujillo for laboratory analyses; Mark Lesser for sharing the Pinus contorta primer sequences; and Julie Canavin for manuscript preparation assistance. This project was a cooperative effort between the Bureau of Land Management Wyoming and the National Forest Genetics Laboratory of the United States Department of Agriculture (USDA) Forest Service, Forest Management Staff. It was supported in part through Research Joint Venture Agreement 10-JV-11330146-049 between the Southern Research Station of the USDA Forest Service and North Carolina State University. Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the USDA and does not imply its approval to the exclusion or other products or vendors that also may be suitable.

Data Archiving Statement

Microsatellite and isozyme genotypes at all loci for all samples, as well as population names and coordinates, are archived at TreeGenes (http://dendrome.ucdavis.edu/treegenes/) as TGDR035.

Author information

Authors and Affiliations

  1. Department of Forestry and Environmental Resources, North Carolina State University, Research Triangle Park, NC, 27709, USA

    Kevin M. Potter

  2. National Forest Genetics Laboratory, USDA Forest Service, Placerville, CA, 95667, USA

    Valerie D. Hipkins

  3. Genetic Resource Program, Northern, Rocky Mountain, Southwestern and Intermountain Regions, USDA Forest Service, Moscow, ID, 83843, USA

    Mary F. Mahalovich

  4. Bureau of Land Management Wyoming, Cheyenne, WY, 82009, USA

    Robert E. Means

Authors
  1. Kevin M. Potter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Valerie D. Hipkins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mary F. Mahalovich
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert E. Means
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kevin M. Potter.

Additional information

Communicated by S. N. Aitken

This article is part of the Topical Collection on Gene Conservation

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 18 kb)

ESM 2

(DOCX 856 kb)

ESM 3

(DOCX 23 kb)

ESM 4

(DOCX 40 kb)

ESM 5

(DOCX 39 kb)

ESM 6

(DOCX 626 kb)

ESM 7

(DOCX 21 kb)

ESM 8

(DOCX 17 kb)

ESM 9

(DOCX 351 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Potter, K.M., Hipkins, V.D., Mahalovich, M.F. et al. Nuclear genetic variation across the range of ponderosa pine (Pinus ponderosa): Phylogeographic, taxonomic and conservation implications. Tree Genetics & Genomes 11, 38 (2015). https://doi.org/10.1007/s11295-015-0865-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-015-0865-y

Keywords

Search

Navigation