Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
Skip to main content

Advertisement

Population genetic structure of Picea engelmannii, P. glauca and their previously unrecognized hybrids in the central Rocky Mountains

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

Abstract

Areas of geographic overlap between potentially hybridizing species provide the opportunity to study interspecific gene flow and reproductive barriers. Here we identified hybrids between Picea engelmannii and P. glauca by their genetic composition at 17 microsatellite markers, and determined the broad-scale geographic distribution of hybrids in the central Rocky Mountains of North America, a geographic region where hybrids and isolation between species had not previously been studied. Parameter estimates from admixture models revealed considerable variation in ancestry within and among collection sites, suggesting that within this area of geographic overlap, the interaction of the two species varies extensively. The results document a previously unrecognized patchy distribution of hybrids between P. engelmannii and P. glauca, including locations where hybrids were not known or expected to exist. Further, the ancestry of many hybrids was consistent with multiple generations of hybridization, with probable directional backcrossing to P. engelmannii, suggesting a relatively porous species boundary. The identification and characterization of hybridization between these spruce in this region raises the question of what factors maintain barriers to gene flow in these long-lived forest trees. The current research lays the groundwork for future study of the ecological and evolutionary contexts of their hybridization, as well as of differential introgression and permeability of species boundaries.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adams WT, Griffin AR, Moran GF (1992) Using paternity analysis to measure effective pollen dispersal in plant populations. Am Nat 140(5):762–780

    Article  PubMed  CAS  Google Scholar 

  • Aldridge G (2005) Variation in frequency of hybrids and spatial structure among Ipomopsis (Polemoniaceae) contact sites. New Phytol 167(1):279–288

    Article  PubMed  Google Scholar 

  • Aldridge G, Campbell D (2009) Genetic and morphological patterns show variation in frequency of hybrids between Ipomopsis (Polemoniaceae) zones of sympatry. Heredity 102:257–265

    Article  PubMed  CAS  Google Scholar 

  • Anderson E, Hubricht L (1938) Hybridization in Tradescantia. III. The evidence for introgressive hybridization. Am J Bot 25:396–402

    Article  Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York

    Google Scholar 

  • Barton NH (2000) Estimating multilocus linkage disequilibria . Heredity 84:373–389

    Article  PubMed  CAS  Google Scholar 

  • Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10(3):551–568

    Article  PubMed  CAS  Google Scholar 

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Ann Rev Ecolog Syst 16:113–148

    Article  Google Scholar 

  • Barton NH, Hewitt GM (1989) Adaptation, speciation and hybrid zones. Nature 341:497–503

    Article  PubMed  CAS  Google Scholar 

  • Bennuah S, Wang T, Aitken S (2004) Genetic analysis of the Picea sitchensis x glauca introgression zone in British Columbia. For Ecol Manag 197(1–3):65–77

    Article  Google Scholar 

  • Berch SM, Brockley RP, Battigelli J, Hagerman S (2009) Impacts of repeated fertilization on fine roots, mycorrhizas, mesofauna, and soil chemistry under young interior spruce in central British Columbia. Can J For Res 39(5):889–896

    Article  CAS  Google Scholar 

  • Bonnicksen TM (2000) America’s ancient forests: from the ice age to the age of discovery. Wiley-Blackwell Publishing, Inc.

  • Bousquet J, Isabel N, Pelgas B, Cottrell J, Rungis D, Ritland K (2007) Spruce. In: Kole C (ed)Forest trees. Genome mapping and molecular breeding in plants, vol 7. Springer, Berlin Heidelberg, pp 93–114

    Google Scholar 

  • Boutin-Ganache I, Raposo M, Raymond M, Deschepper C (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. BioTechniques 31(1):24

    PubMed  CAS  Google Scholar 

  • Bower AD, Aitken SN (2008) Ecological genetics and seed transfer guidelines for Pinus albicaulis (Pinaceae). Am J Bot 95(1): 66–76

    Article  PubMed  Google Scholar 

  • Bridle JR, Vass-De-Zomba J, Butlin RK (2002) Fine-scale ecological and genetic variation in a Chorthippus grasshopper hybrid zone. Ecol Entomol 27(4):499–504

    Article  Google Scholar 

  • Buerkle CA (2005) Maximum-likelihood estimation of a hybrid index based on molecular markers. Mol Ecol Notes 5:684–687

    Article  CAS  Google Scholar 

  • Buerkle CA, Lexer C (2008) Admixture as the basis for genetic mapping. Trends Ecol Evol 23(12):686–694

    Article  PubMed  Google Scholar 

  • Burgarella C, Lorenzo Z, Jabbour-Zahab R, Lumaret R, Guichoux E, Petit RJ, Soto A, Gil L (2009) Detection of hybrids in nature: application to oaks (Quercus suber and Q. ilex). Heredity 102(5):442–452

    Article  PubMed  CAS  Google Scholar 

  • Carlsson J (2008) Effects of microsatellite null alleles on assignment testing. J Heredity 99(6):616–623

    Article  CAS  Google Scholar 

  • Coates K, Haeussler S, Lindeburgh S, Pojar R, Stock A (1994) Ecology and siliviculture of interior spruce in British Columbia. FRDA report 220, Canada-British Columbia Partnership Agreement on Forest Resource Development

  • Cullings K (1992) Design and testing of a plant-specific PCR primer for ecological and evolutionary studies. Mol Ecol 1:233–240

    Article  CAS  Google Scholar 

  • Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509

    Article  PubMed  CAS  Google Scholar 

  • Daubenmire R (1968) Some geographic variations in Picea sitchensis and their ecological interpretation. Can J Bot 46:787–798

    Article  Google Scholar 

  • Daubenmire R (1974) Taxonomic and ecologic relationships between Picea glauca and Picea engelmannii. Can J Bot 52(7):1545– 1560

    Article  Google Scholar 

  • Doyle JJ, Doyle J (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Everitt B, Hothorn T (2011a) Multidimensional scaling. Springer, New York, pp 105–134

    Google Scholar 

  • Everitt B, Hothorn T (2011b) Principal components analysis. Springer, New York, pp 61–103

    Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Field DL, Ayre DJ, Whelan RJ, Young AG (2008) Relative frequency of sympatric species influences rates of interspecific hybridization, seed production and seedling performance in the uncommon Eucalyptus aggregata. J Ecol 96(6):1198–1210

    Article  Google Scholar 

  • Field DL, Ayre DJ, Whelan RJ, Young AG (2011) The importance of pre-mating barriers and the local demographic context for contemporary mating patterns in hybrid zones of Eucalyptus aggregata and Eucalyptus rubida. Mol Ecol 20(11):2367–2379

    Article  PubMed  Google Scholar 

  • Fowler D, Roche L (1977) Genetics of Engelmann spruce. Research paper WO–30, U.S. Department of Agriculture Forest Service

  • Gay L, Crochet PA, Bell DA, Lenormand T (2008) Comparing clines on molecular and phenotypic traits in hybrid zones: a window on tension zone models. Evolution 62(11):2789–2806

    Article  PubMed  Google Scholar 

  • Gompert Z, Lucas LK, Nice CC, Fordyce JA, Forister ML, Buerkle CA (2012) Genomic regions with a history of divergent selection affect fitness of hybrids between two butterfly species. Evolution 66(7):2167–2181

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Griffin A, Burgess I, Wolf L (1988) Patterns of natural and manipulated hybridisation in the genus Eucalyptus. Aust J Bot 36(1):41–66

    Article  Google Scholar 

  • Guillot G (2005) GENELAND: a computer package for landscape genetics. Contributed R package

  • Guillot G, Santos F, Estoup A (2008) Analysing georeferenced population genetics data with GENELAND: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24(11):1406–1407

    Article  PubMed  CAS  Google Scholar 

  • Habeck JR, Weaver TW (1969) A chemosystematic analysis of some hybrid spruce (Picea) populations in Montana. Can J Bot 47(10):1565–1570

    Article  CAS  Google Scholar 

  • Hamilton JA, Lexer C, Aitken SN (2012) Genomic and phenotypic architecture of a spruce hybrid zone (Picea sitchensis x P. glauca). Molecular Ecology p. Early View

  • Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8(5):461–467

    Article  PubMed  Google Scholar 

  • Harrison RG (1986) Pattern and process in a narrow hybrid zone. Heredity 56:337–349

    Article  Google Scholar 

  • Harrison RG (1990) Hybrid zones: windows on evolutionary process. Oxf Surv Evol Biol 7:69–128

    Google Scholar 

  • Harrison RG (1993) Hybrids and hybrid zones: historical perspective, chap 1. Oxford University Press, New York, pp 3–12

    Google Scholar 

  • Heuertz M, De Paoli E, Källma T, Larsson H, Jurma I, Morgante M, Lascoux M, Gyllenstrand N (2006) Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of norway spruce [Picea abies (l.) karst]. Genetics 174(4):2095–2105

    Article  PubMed  CAS  Google Scholar 

  • Hewitt GM (1988) Hybrid zones—natural laboratories for evolution studies. Trends Ecol Evol 3:158–166

    Article  PubMed  CAS  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9(5):1322–1332

    Article  Google Scholar 

  • Jaramillo-Correa JP, Beaulieu J, Bousquet J (2001) Contrasting evolutionary forces driving population structure at expressed sequence tag polymorphisms, allozymes and quantitative traits in white spruce. Mol Ecol 10(11):2729–2740

    Article  PubMed  CAS  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 39(2):286–307

    Article  Google Scholar 

  • Khasa P, Dancik B (1996) Rapid identification of White-Engelmann spruce species by RAPD markers. Theor Appl Genet 92(1): 46–52

    Article  CAS  Google Scholar 

  • Krutovskii KV, Bergmann F (1995) Introgressive hybridization and phylogenetic relationships between Norway, Picea abies (L.) Karst., and Siberian, P. obovata Ledeb., spruce species studied by isozyme loci. Heredity 74:464–480

    Article  CAS  Google Scholar 

  • Lanner RM, Phillips AMI (1992) Natural hybridization and introgression of pinyon pines in northwestern Arizona. Int J Plant Sci 153(2):250–257

    Article  Google Scholar 

  • Lavergne S, Mouquet N, Thuiller W, Ronce O (2010) Biodiversity and climate change: integrating evolutionary and ecological responses of species and communities. Annu Rev Ecol Evol System 41(1):321–350

    Article  Google Scholar 

  • Ledig FT, Hodgskiss PD, Johnson DR (2006) The structure of genetic diversity in Engelmann spruce and a comparison with blue spruce. Can J Bot 84(12):1806–1828

    Article  CAS  Google Scholar 

  • Ledig TF, Hodgskiss PD, Krutovskii KV, Neale DB, Eguiluz-Piedra T (2004) Relationships among the spruces (Picea, Pinaceae) of Southwestern North America. Syst Bot 29(2):275–295

    Article  Google Scholar 

  • Lepais O, Petit R, Guichoux E, Lavabre J, Alberto F, Kremer A, Gerber S (2009) Species relative abundance and direction of introgression in oaks. Mol Ecol 18:2228–2242

    Article  PubMed  CAS  Google Scholar 

  • Lexer C, Fay MF, Joseph JA, Nica MS, Heinze B (2005a) Barrier to gene flow between two ecological divergent Populus species, P. alba (white poplar) and P. tremula (European aspen): the role of ecology and life history in gene introgression. Mol Ecol 14:1045–1057

    Article  CAS  Google Scholar 

  • Lexer C, Heinze B, Alia R, Rieseberg LH (2004) Hybrid zones as a tool for identifying adaptive genetic variation in outbreeding forest trees: lessons from wild annual sunflowers (Helianthus spp.)For Ecol Manag 197:49–64

    Article  Google Scholar 

  • Lexer C, Joseph JA, van Loo M, Barbará T, Heinze B, Bartha D, Castiglione S, Fay MF, Buerkle CA (2010) Genomic admixture analysis in European Populus spp. reveals unexpected patterns of reproductive isolation and mating. Genetics 186(2): 699–712

    Article  PubMed  CAS  Google Scholar 

  • Lexer C, Rosenthal DM, Raymond O, Donovan LA, Rieseberg LH (2005b) Genetics of species differences in the wild annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 169:2225–2239

    Article  CAS  Google Scholar 

  • Lindtke D, Buerkle CA, Barbará T, Heinze B, Castiglione S, Bartha D, Lexer C (2012) Recombinant hybrids retain heterozygosity at many loci: new insights into the genomics of reproductive isolation in Populus. Mol Ecol 21(20):5042– 5058

    Article  PubMed  CAS  Google Scholar 

  • Major JE, Mosseler A, Johnsen KH, Rajora OP, Barsi DC, Kim KH, Park JM, Campbell M (2005) Reproductive barriers and hybridity in two spruces, Picea rubens and Picea mariana, sympatric in Eastern North America. Can J Bot 83:163–175

    Article  Google Scholar 

  • Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20(5):229–237

    Article  PubMed  Google Scholar 

  • Martinsen GD, Whitham TG, Turek RJ, Keim P (2001) Hybrid populations selectively filter introgression between species. Evolution 55:1325–1335

    PubMed  CAS  Google Scholar 

  • Meirmans P, Tienderen PV (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Minder AM, Rothenbuehler C, Widmer A (2007) Genetic structure of hybrid zones between Silene latifolia and Silene dioica (Caryophyllaceae): evidence for introgressive hybridization. Mol Ecol 16:2504–2516

    Article  PubMed  CAS  Google Scholar 

  • Mir C, Toumi L, Jarne P, Sarda V, Di Giusto F, Lumaret R (2006) Endemic North African Quercus afares Pomel originates from hybridisation between two genetically very distant oak species (Q. suber L. and Q. canariensis Willd.): evidence from nuclear and cytoplasmic markers. Heredity 96:175–184

    Article  PubMed  CAS  Google Scholar 

  • Moore WS (1977) An evaluation of narrow hybrid zones in vertebrates. Q Rev Biol 52:263–267

    Article  Google Scholar 

  • Morgenstern EK (1996) Geographic variation in forest trees: genetic basis and application of knowledge in silviculture. UBC Press, Vancouver

    Google Scholar 

  • Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9(7):325–330

    Article  PubMed  CAS  Google Scholar 

  • Nkongolo K, Michael P, Demers T (2005) Application of ISSR, RAPD, and cytological markers to the certification of Picea mariana, P. glauca, and P. engelmannii trees, and their putative hybrids. Genome 48(2):302–311

    Article  PubMed  CAS  Google Scholar 

  • Novembre J, Stephens M (2008) Interpreting principal component analyses of spatial population genetic variation. Nat Genet 40:646–649

    Article  PubMed  CAS  Google Scholar 

  • Owens JN, Molder M (1977) Bud development in Picea glauca. II. Cone differentiation and early development. Can J Bot 55(21):2746–2760

    Article  Google Scholar 

  • Owens JN, Molder M (1984) The reproductive cycle of interior spruce. Tech. rep., Ministry of Forests, British Columbia

    Google Scholar 

  • Owens JN, Simpson SJ, Caron GE (1987) The pollination mechanism of Engelmann spruce (Picea engelmannii). Can J Bot 65(7):1439–1450

    Article  Google Scholar 

  • Pavy N, Namroud MC, Gagon F, Isabel N, Bousquet J (2012) The heterogeneous levels of linkage disequilibrium in white spruce genes and comparative analysis with other conifers. Heredity 108: 273–284

    Article  PubMed  CAS  Google Scholar 

  • Pelgas B, Beauseigle S, Achere V, Jeandroz S, Bousquet J, Isabel N (2006) Comparative genome mapping among Picea glauca, P. mariana x P. rubens and P. abies and correspondence with other Pinaceae. Theor Appl Genet 113(8):1371–1393

    Article  PubMed  CAS  Google Scholar 

  • Perron M, Bousquet J (1997) Natural hybridization between black spruce and red spruce. Mol Ecol 6(8):725–734

    Article  Google Scholar 

  • Perry D, Bousquet J (1998) Sequence-tagged-site (STS) markers of arbitrary genes: development, characterization and analysis of linkage in black spruce. Genetics 149(2):1089–1098

    PubMed  CAS  Google Scholar 

  • Pfeiffer A, Olivieri A, Morgante M (1997) Identification and characterization of microsatellites in Norway spruce (Picea abies k). Genome 40(4):411–419

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0

    Google Scholar 

  • Rajora O, Dancik B (2000) Population genetic variation, structure, and evolution in Engelmann spruce, white spruce, and their natural hybrid complex in Alberta. Can J Bot 78(6):768–780

    Google Scholar 

  • Rajora OP, Mann IK, Shi YZ (2005) Genetic diversity and population structure of boreal white spruce (Picea glauca) in pristine conifer-dominated and mixedwood forest stands. Can J Bot 83(9):1096–1105

    Article  CAS  Google Scholar 

  • Ran JH, Wei XX, Wang XQ (2006) Molecular phylogeny and biogeography of Picea (Pinaceae): implications for phylogeographical studies using cytoplasmic haplotypes. Mol Phylogenet Evol 41(2):405–419

    Article  PubMed  CAS  Google Scholar 

  • Rehfeldt G (1994) Adaptation of Picea engelmannii populations to the heterogeneous environments of the intermountain west. Can J Bot 72(8):1197–1208

    Article  Google Scholar 

  • Rehfeldt G (2004) Interspecific and intraspecific variation in Picea engelmannii and its congeneric cohorts: biosystematics, genecology and climate change. General Technical Report RMRS-GTR-134, U.S. Department of Agriculture, Forest Service, Rocky Mountain Research.Fort Collins, CO

    Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Ann Rev Ecolog Syst 27:83–109

    Article  Google Scholar 

  • Rieseberg LH (1995) The role of hybridization in evolution: old wine in new skins. Am J Bot 82(7):944–953

    Article  Google Scholar 

  • Roche L (1969) A genecological study of genus Picea in British Columbia. New Phytol 68(2):505–554

    Article  Google Scholar 

  • Ross CL, Harrison RG (2002) A fine-scale spatial analysis of the mosaic hybrid zone between Gryllus firmus and Gryllus pennsylvanicus. Evolution 56(11):2296–2312

    PubMed  Google Scholar 

  • Rungis D, Berube Y, Zhang J, Ralph S, Ritland C, Ellis B, Douglas C, Bohlmann J, Ritland K (2004) Robust simple sequence repeat markers for spruce (Picea spp.) from expressed sequence tags. Theor Appl Genet 109(6):1283–1294

    Article  PubMed  CAS  Google Scholar 

  • Schaid DJ (2004) Linkage disequilibrium testing when linkage phase is unknown. Genetics 166(1):505–512

    Article  PubMed  Google Scholar 

  • Schubert R, Mueller-Starck G, Riegel R (2001) Development of EST-PCR markers and monitoring their intrapopulational genetic variation in Picea abies (l.) karst. Theor Appl Genet 103(8): 1223–1231

    Article  CAS  Google Scholar 

  • Scotti I, Magni F, Fink R, Powell W, Binelli G, Hedley P (2000) Microsatellite repeats are not randomly distributed within Norway spruce (Picea abies K.) expressed sequences. Genome 43(1):41–46

    PubMed  CAS  Google Scholar 

  • Scotti I, Magni F, Paglia G, Morgante M (2002a) Trinucleotide microsatellites in Norway spruce (Picea abies): their features and the development of molecular markers. Theor Appl Genet 106(1):40–50

    CAS  Google Scholar 

  • Scotti I, Paglia G, Magni F, Morgante M (2002b) Efficient development of dinucleotide microsatellite markers in Norway spruce (Picea abies Karst.) through dot-blot selection. Theor Appl Genet 104(6–7):1035–1041

    CAS  Google Scholar 

  • Strong WL, Hills LV (2006) Taxonomy and origin of present-day morphometric variation in Picea glauca (x engelmannii) seed-cone scales in North America. Can J Bot 84:1129–1141

    Article  Google Scholar 

  • Sutton BCS, Pritchard SC, Gawley JR, Newton CH, Kiss GK (1994) Analysis of Sitka spruce–interior spruce introgression in British Columbia using cytoplasmic and nuclear DNA probes. Can J For Res 24(2):278–285

    Article  Google Scholar 

  • Swenson NG, Howard DJ (2005) Clustering of contact zones, hybrid zones, and phylogeographic breaks in North America. Am Nat 166(5):581–591

    Article  PubMed  Google Scholar 

  • Szymura JM, Barton NH (1986) Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and B. variegata, near Cracow in southern Poland. Evolution 40:1141– 1159

    Article  Google Scholar 

  • Talbot P, Thompson SL, Schroeder W, Isabel N (2011) An efficient single nucleotide polymorphism assay to diagnose the genomic identity of poplar species and hybrids on the Canadian prairies. Can J For Res 41(5):1102–1111

    Article  Google Scholar 

  • Taylor T (1959) The taxonomic relationship between Picea glauca (Moench) Voss and P. engelmannii Parry. Madroño 15(4):111– 115

    Google Scholar 

  • Temesgen B, Brown G, Harry D, Kinlaw C, Sewell M, Neale D (2001) Genetic mapping of expressed sequence tag polymorphism (ESTP) markers in Loblolly pine (Pinus taeda L.)Theor Appl Genet 102(5):664–675

    Article  CAS  Google Scholar 

  • Thomas DT, Ahedor AR, Williams CF, dePamphilis C, Crawford DJ, Xiang QJ (2008) Genetic analysis of a broad hybrid zone in Aesculus (Sapindaceae): is there evidence of long distance pollen dispersal?Int J Plant Sci 169(5):647–657

    Article  Google Scholar 

  • Thompson SL, Lamothe M, Meirmans PG, Périnet P, Isabel N (2010) Repeated unidirectional introgression towards Populus balsamifera in contact zones of exotic and native poplars. Mol Ecol 19(1):132–145

    Article  PubMed  CAS  Google Scholar 

  • Valbuena-Carabana M, Gonzalez-Martinez S (2005) Gene flow and hybridisation in a mixed oak forest (Quercus pyrenaica willd. and Quercus petraea (matts.) liebl.) in Central Spain. Heredity 95:457–465

    Article  PubMed  CAS  Google Scholar 

  • van Loo M, Joseph J, Heinze B, Fay M, Lexer C (2008) Clonality and spatial genetic structure in Populus \(\times \) canescens and its sympatric backcross parent P. alba in a Central European hybrid zone. New Phytol 177:506–516

    PubMed  Google Scholar 

  • Wang XR, Szmidt AE (1990) Evolutionary analysis of Pinus densata (Masters), a putative Tertiary hybrid. Theor Appl Genet 80(5):641–647

    CAS  Google Scholar 

  • Weir BS (1979) Inferences about linkage disequilibrium. Biometrics 35:235–254

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Weng C, Jackson S (2000) Species differentiation of North American spruce (Picea) based on morphological and anatomical characteristics of needles. Can J Bot 78:1367–1383

    Google Scholar 

  • Whitham T (1989) Plant hybrid zones as sinks for pests. Science 244:1490–1493

    Article  Google Scholar 

  • Whittemore AT, Schaal BA (1991) Interspecific gene flow in sympatric oaks. Proc Natl Acad Sci 88(6):2540–2544

    Article  PubMed  CAS  Google Scholar 

  • Yansa CH (2006) The timing and nature of late quaternary vegetation changes in the northern great plains, USA and Canada: a re-assessment of the spruce phase. Quat Sci Rev 25(3–4):263–281

    Article  Google Scholar 

  • Zaykin DV, Pudovkin A, Weir BS (2008) Correlation-based inference for linkage disequilibrium with multiple alleles. Genetics 180(1):533–545

    Article  PubMed  Google Scholar 

  • Zeng YF, Liao WJ, Petit RJ, Zhang DY (2011) Geographic variation in the structure of oak hybrid zones provides insights into the dynamics of speciation. Mol Ecol 20(23):4995–5011

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank P. Haselhorst for assisting in the field, C. Wilcox (Coronado National Forest), P. Stankowski and W. Parker (Lakehead University, Ontario, Canada), D. Wolf and N. Takebayashi (University of Alaska–Fairbanks) for collecting needles from parental populations, Z. Gompert for assistance with statistical analyses, the Buerkle lab, three anonymous reviewers and Associate Editor S. Aitken for valuable comments on the manuscript, and the Nevada Genomics Center at the University of Nevada for providing high quality and rapid genotyping services. This research was funded by the Wyoming Native Plant Society, John W. Marr Memorial Fund, Shoshone National Forest, H. T. Northen Summer Fellowship in Botany, and UW-NPS Research Center.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Monia S. H. Haselhorst.

Additional information

Communicated by S. Aitken

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

(PDF 79.6 KB)

Data archiving statement

Data archiving statement

Allele sizes for each locus per individual and population, and detailed marker and primer information can be accessed online at datadryad.org. Dryad accession number: 10.5061/dryad.C5C1q.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haselhorst, M.S.H., Buerkle, C.A. Population genetic structure of Picea engelmannii, P. glauca and their previously unrecognized hybrids in the central Rocky Mountains. Tree Genetics & Genomes 9, 669–681 (2013). https://doi.org/10.1007/s11295-012-0583-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-012-0583-7

Keywords