Skip to main content
Log in

Genetic analysis of admixture and patterns of introgression in foundation cottonwood trees (Salicaceae) in southwestern Colorado, USA

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

Abstract

Cottonwoods are well known as foundation riparian trees that support diverse communities and drive ecosystem processes. Although hybridization naturally occurs when the distributions of two or more cottonwood species overlap, few cottonwood hybrid zones have been genetically characterized. We use genetic and genomic analyses to characterize patterns of admixture and introgression for a newly described hybrid zone at the intersection of three species (Populus L. Salicaceae—Populus deltoides, Populus fremontii, and Populus angustifolia) in southwestern Colorado, USA. Analysis of nuclear and chloroplast microsatellite marker data detected substantial genetic variation among individuals, revealing that (1) hybridization is occurring between two, not three, species (P. deltoides and P. angustifolia); (2) gene flow is bidirectional; (3) hybrids are not abundant (admixture detected in only 34 of 270 trees), with most being early-generation F1 hybrids; (4) cytonuclear disequilibria exists and F1 hybrids tend to retain P. deltoides—like chloroplasts; and (5) roughly 30 % of the nuclear markers deviated from a neutral pattern of introgression, suggesting that selection may play a role in shaping the genetic structure of the hybrid zone in this region. Overall, our results show that despite strong selection maintaining species divergence, transfer of allelic variants across species boundaries can occur. Our study assesses the fine-scale genetic structure of hybridization between P. angustifolia and P. deltoides and lays the foundation for examining how geographic differences in hybrid zone dynamics arise and may influence subsequent ecological and evolutionary processes.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Reference

  • Abernathy K (1994) The establishment of a hybrid zone between red and sika deer (genus Cervus). Mol Ecol 3:551–562

    Google Scholar 

  • Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arnold ML (1992) Natural hybridization as an evolutionary process. Annu Rev Ecol Syst 23:237–261

    Google Scholar 

  • Arnold J (1993) Cytonuclear disequilibria in hybrid zones. Annu Rev Ecol Syst 24:521–554

    Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford Series in Ecology and Evolution. Oxford University Press, Oxford

    Google Scholar 

  • Arnold ML, Martin NH (2009) Adaptation by introgression. J Biol 8:82–85

    PubMed Central  PubMed  Google Scholar 

  • Asmussen MA (1989) The effects of assortative mating and migration on cytonuclear associations in hybrid zones. Genetics 122:923–934

    CAS  PubMed Central  PubMed  Google Scholar 

  • Asmussen MA, Basten CJ (1994) Sampling theory for cytonuclear disequilibria. Genetics 138:1351–1363

    CAS  PubMed Central  PubMed  Google Scholar 

  • Asmussen MA, Arnold J, Avise JC (1987) Definitions and properties of disequilibrium statistics for associations between nuclear and cytoplasmic genotypes. Genetics 115:755–768

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baird SJE (1995) A simulation study of multilocus clines. Evolution 49:1038–1045

    Google Scholar 

  • Balatinecz JJ, Kretschmann DE (2001) Properties and utilization of poplar wood. In: Dickmann D, Isebrands JG, Eckenwalder JE, Richardson J (eds) Poplar culture in North America. NRC, Ottawa, ON, pp 277–290

    Google Scholar 

  • Barton NH, Gale KS (1993) Genetic analysis of hybrid zones. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, Oxford, pp 13–45

    Google Scholar 

  • Barton NH, Hewitt GM (1981) Hybrid zones and speciation. In: Atchley WR, Woodruff D (eds) Evolution and speciation. Cambridge University Press, Cambridge, pp 109–145

    Google Scholar 

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

    Google Scholar 

  • Baskett ML, Gomulkiewicz R (2011) Introgressive hybridization as a mechanism for species rescue. Theor Ecol 4:223–229

    Google Scholar 

  • Bernhardsson C, Robinson KM, Abreu IN, Jansson S, Albrectsen BR, Ingvarsson PK (2013) Geographic structure in metabolome and herbivore community co-occurs with genetic structure in plant defence genes. Ecol Lett 16:791–798

    PubMed  Google Scholar 

  • Bradshaw HD, Stettler RF (1993) Molecular genetics of growth and development in Populus. I. Triploidy in hybrid poplars. Theor Appl Genet 86:301–307

    PubMed  Google Scholar 

  • Broeck AV, Villar M, Van Bockstaele E, Van Slycken J (2005) Natural hybridization between cultivated poplars and their wild relatives: evidence and consequences for native poplar populations. Ann For Sci 62:601–613

    Google Scholar 

  • Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9:49–56

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Buggs RJA (2007) Empirical study of hybrid zone movement. Heredity 99:301–302

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Chatfield MWH, Kiozak KH, Fitzpatrick BM, Tucker PK (2010) Patterns of differential introgression in a salamander hybrid zone: inferences from genetic data and ecological niche modelling. Mol Ecol 19:4265–4282

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Google Scholar 

  • Conkle MT, Critchfield WB (1988) Genetic variation and hybridization of Ponderosa pine. Ponderosa pine: the species and its management. Symposium Proceedings, Washington State University Pullman, WA

  • Coyne JA, Orr AH (2004) Speciation. Sinauer Associates, Sunderland

    Google Scholar 

  • Cruzan MB, Arnold ML (1993) Ecological and genetic associations in an Iris hybrid zone. Evolution 47:1432–1445

    Google Scholar 

  • Cullingham CI, James PMA, Cooke JEK, Coltman DW (2012) Characterizing the physical and genetic structure of the lodgepole pine × jack pine hybrid zone: mosaic structure and differential introgression. Evol Appl 5:879–891

    PubMed Central  PubMed  Google Scholar 

  • Dayton PK (1972) Toward an understanding of community resilience and the potential effects of enrichments to the benthos at McMurdo Sound, Antarctica. Proceedings of the Colloquium on Conservation Problems in Antarctica. Allen Press, Lawrence

    Google Scholar 

  • Devitt TJ, Baird SJE, Moritz C (2011) Asymmetric reproductive isolation between terminal forms of the salamander ring species Ensatina eschscholtzii revealed by fine-scale genetic analysis of a hybrid zone. BMC Evol Biol 11:1–15

    Google Scholar 

  • Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellie data sets. Mol Ecol Notes 3:167–169

    CAS  Google Scholar 

  • DiFazio SP, Slavov GT, Joshi CP (2011) Populus: a premier pioneer system for plant genomics. In: Joshi CP, DiFazio SP, Kole C (eds) Genetics, genomics and breeding of poplar. Science Publishers, Enfield, pp 1–28

    Google Scholar 

  • Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS (1991) ‘Touchdown’ PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19:4008

    CAS  PubMed Central  PubMed  Google Scholar 

  • Eckenwalder JE (1984a) Natural intersectional hybridization between North American species of Populus (Salicaceae) in sections Aigeiros and Tacamahaca. II. Taxonomy. Can J Bot 62:325–335

    Google Scholar 

  • Eckenwalder JE (1984b) Natural intersectional hybridization between North American species of Populus (Salicaceae) in sections Aigeiros and Tacamahaca. III. Paleobotany and evolution. Can J Bot 62:336–342

    Google Scholar 

  • Eckenwalder JE (1996) Systematics and evolution of Populus. In: Stettler RF, Bradshaw HD, Heilman PE, Hinckley TM (eds) Biology of Populus, and its implications for management and conservation. NRC Research Press, Ottawa

    Google Scholar 

  • Ellison AM, Bank SM, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel BD, Knoepp JD, Lovett GM, Mohan J, Orwig DA, Rodenhouse NL, Sobczak WV, Stinson KA, Stone JK, Swan CM, Thompson J, Holle BV, Webster JR (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Evans LM, Allan GJ, Shuster SM, Woolbright SA, Whitham TG (2008) Tree hybridization and genotypic variation drive cryptic speciation of a specialized mite herbivore. Evolution 62:3027–3040

    PubMed  Google Scholar 

  • Evans LM, Allan GJ, Whitham TG (2012) Populus hybrid hosts drive divergence in the herbivorous mite, Aceria parapopuli: implications for conservation of plant hybrid zones as essential habitat. Conserv Genet 13:1601–1609

    Google Scholar 

  • Evans LM, Allan GJ, Meneses N, Max TL, Whitham TG (2013) Herbivore host-associated genetic differentiation depends on the scale of plant genetic variation examined. Evol Ecol 27:65–68

    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 131:479–491

    CAS  PubMed Central  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    CAS  PubMed Central  PubMed  Google Scholar 

  • Field DL, Ayre DJ, Whelan RJ, Young AG (2011) Patterns of hybridization and asymmetrical gene flow in hybrid zones of the rare Eucalyptus aggregata and common E. rubida. Heredity 106(5):841–853

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fitzpatrick BM, Johnson JR, Kump DK, Shaffer B, Smith JJ, Voss SR (2009) Rapid fixation of non-native alleles revealed by genome-wide SNP analysis of hybrid tiger salamanders. BMC Evol Biol 9:176–187

    PubMed Central  PubMed  Google Scholar 

  • Fritz RS, Moulia C, Newcombe G (1999) Resistance of hybrid plants and animals to herbivores, pathogens, and parasites. Annu Rev Ecol Syst 30:565–591

    Google Scholar 

  • Gavrilets S (1997) Hybrid zones with Dobzhansky-type epistatic interactions. Evolution 51:1027–1035

    Google Scholar 

  • Gompert Z, Buerkle CA (2009) A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Mol Ecol 18:1207–1224

    PubMed  Google Scholar 

  • Gompert Z, Buerkle CA (2010) Introgress: a software package for mapping components of isolation in hybrids. Mol Ecol Resour 10:278–384

    Google Scholar 

  • Gompert Z, Buerkle CA (2011) Bayesian estimates of genomic clines. Mol Ecol 20:2111–2127

    PubMed  Google Scholar 

  • Gompert Z, Parchman TL, Buerkle CA (2012) Genomics of isolation in hybrids. Philos Trans R Soc B 367:439–450

    Google Scholar 

  • Grant V (1981) Plant speciation, 2nd edn. Columbia University Press, New York

    Google Scholar 

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

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    CAS  PubMed  Google Scholar 

  • Hamzeh M, Sawchyn C, Périnet P, Dayanandan S (2007) Asymmetrical natural hybridization between Populus deltoides and P. balsamifera (Salicaceae). Can J Bot 85:1127–1132

    Google Scholar 

  • Hardy OJ, Vekemans X (1999) Isolation by distance in a continuous population: reconciliation between spatial autocorrelation analysis and population genetics models. Heredity 83:145–154

    PubMed  Google Scholar 

  • Harrison RG, Bogdanowicz SM (1997) Patterns of variation and linkage disequilibrium in a field cricket hybrid zone. Evolution 51:493–505

    CAS  Google Scholar 

  • Haselhorst MSH, Buerkle CA (2013) Population genetic structure of Picea engelmannii, P. glauca and their previously unrecognized hybrids in the Central Rocky Mountains. Tree Genet Genomes 9:669–681

    Google Scholar 

  • Hendrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    Google Scholar 

  • Hoban S, McCleary T, Schlarbaum S, Romero-Severson J (2009) Geographically extensive hybridization between the forest trees American butternut and Japanese walnut. Biol Lett 5:324–327

    PubMed Central  PubMed  Google Scholar 

  • Horning ME, Cronn R (2006) Length polymorphism scanning is an efficient approach for revealing chloroplast DNA variation. Genome 49:134–142

    CAS  PubMed  Google Scholar 

  • Jakobssen M, Rosenberg N (2006) CLUMPP: cluster matching and permutation program, version 1.0. University of Michigan, Ann Arbor

    Google Scholar 

  • Jiggins CD, Mallet J (2000) Bimodal hybrid zones and speciation. Trends Ecol Evol 15:250–255

    PubMed  Google Scholar 

  • Keim P, Paige K, Whitham T, Lark K (1989) Genetic analysis of an interspecific hybrid swarm of Populus: occurrence of unidirectional introgression. Genetics 123:557–566

    CAS  PubMed Central  PubMed  Google Scholar 

  • Keller SR, Levesen N, Olson MS, Tiffin P (2012) Local adaptation in the flowering-time gene network of balsam poplar, Populus balsamifera L. Mol Biol Evol 10:3143–3152

    Google Scholar 

  • Key KHL (1968) The concept of stasipatric speciation. Syst Zool 14:14–22

    Google Scholar 

  • Lexer C, Buerkle A, Joseph J, Heinze B, Fay MF (2007) Admixture in European Populus hybrid zones makes feasible the mapping of loci that contribute to reproductive isolation and trait differences. Heredity 98:74–84

    CAS  PubMed  Google Scholar 

  • Lexer C, Joseph JA, van Loo M, Barbara 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 186:699–712

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lindtke D, Buerkle CA, Barbara 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 21:5042–5058

    CAS  PubMed  Google Scholar 

  • Mallet J (2007) Hybrid speciation. Nature 446:279–283

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Milne RI, Terzioglu S, Abbott RJ (2003) A hybrid zone dominated by fertile F1s: maintenance of species barriers in Rhododendron. Mol Ecol 12:2719–2729

    CAS  PubMed  Google Scholar 

  • Mir C, Toumi L, Jarne P, Sarda V, Giusto FD, 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

    CAS  PubMed  Google Scholar 

  • Mir C, Sarda JV, Bonin A, Lumaret R (2009) Contrasting nuclear and cytoplasmic exchanges between phylogenetically distant oak species (Quercus suber L. and Q. ilex L.) in southern France: inferring crosses and dynamics. Plant Biol 11:213–226

    CAS  PubMed  Google Scholar 

  • Moore WS (1977) Evaluation of narrow hybrid zones in vertebrates. Q Rev Biol 52:263–277

    Google Scholar 

  • Moore WS, Price JT (1993) Nature of selection in the northern flicker hybrid zone and its implications for speciation theory. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, Oxford, pp 196–225

    Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Newcombe G, Stirling B, McDonald S, Bradshaw HD (2000) Melampsora columbiana, a natural hybrid of M. medusae and M. occidentalis. Mycol Res 104:261–274

    Google Scholar 

  • Nolte AW, Gompert Z, Buerkle CA (2009) Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations. Mol Ecol 18:2615–2627

    CAS  PubMed  Google Scholar 

  • Paige KN, Capman WC, Jennetten P (1991) Mitochondrial inheritance patterns across a cottonwood hybrid zone: cytonuclear disequilibria and hybrid zone dynamics. Evolution 45:1360–1369

    Google Scholar 

  • Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Google Scholar 

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

    Google Scholar 

  • Potts BM, Dungey HS (2004) Interspecific hybridization of Eucalyptus: key issues for breeders and geneticists. New For 27:115–138

    Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Google Scholar 

  • Rajora OP, Dancik BP (1992) Chloroplast DNA inheritance in Populus. Theor Appl Genet 84:280–285

    CAS  PubMed  Google Scholar 

  • Raufaste N, Orth A, Belkhir K, Senet D, Smadja C, Baird SJE, Bonhomme F, Dod B, Boursot P (2005) Inferences of selection and migration in the Danish house mouse hybrid zone. Biol J Linn Soc 84:593–616

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Google Scholar 

  • Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389

    Google Scholar 

  • Rieseberg LH, Carney SE (1998) Plant hybridization. New Phytol 140:599–624

    Google Scholar 

  • Rieseberg LH, Whitton J, Gardner K (1999) Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152:713–727

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rushton BS (1993) Natural hybridization within the genus Quercus L. Ann Sci For 50:73–90

    Google Scholar 

  • Schierenbeck KA, Ellstrand NC (2009) Hybridization and the evolution of invasiveness in plants and other organisms. Biol Invasions 11:1093–1105

    Google Scholar 

  • Schweitzer JA, Bailey JK, Rehill BJ, Martinsen GD, Hart SC, Lindroth RL, Keim P, Whitham TG (2004) Genetically based trait in a dominant tree affects ecosystem processes. Ecol Lett 7:127–134

    Google Scholar 

  • Schweitzer JA, Madritch MD, Felker-Quinn E, Bailey JK (2012) From genes to ecosystems: how plant genetics links above- and below-ground processes In: Wall D (ed) Soil ecology and ecosystem services. Oxford University Press, Oxford, pp 82–98

  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166

    CAS  PubMed  Google Scholar 

  • Shriver MD, Smith MW, Jin L, Marcini A, Akey JM, Deka R, Ferrell RE (1997) Ethnic-affiliation estimation by use of population-specific DNA markers. Am J Hum Genet 60:957–964

    CAS  PubMed Central  PubMed  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smith RL, Systma KJ (1990) Evolution of Populus nigra (sect. Aigeiros): introgressive hybridization and the chloroplast contribution of Populus alba (sect. Populus). Am J Bot 77:1176–1187

    Google Scholar 

  • Smulders MJM, Van Der Schoot J, Arens P, Vosman B (2001) Trinucleotide repeat microsatellite markers for black poplar (Populus nigra L.). Mol Ecol Notes 1:188–190

    CAS  Google Scholar 

  • Strauss SY (1994) Levels of herbivory and parasitism in host hybrid zones. Trends Ecol Evol 9:209–214

    CAS  PubMed  Google Scholar 

  • Strauss SH (2003) Genetic technologies—genomics, genetic engineering, and domestication of crops. Science 300:61–62

    Google Scholar 

  • Stuckas H, Stoof K, Quesada H, Tiedemann R (2009) Evolutionary implications of discordant clines across the Baltic Mytilus hybrid zone (Mytilus edulis and Mytilus trossulus). Heredity 103:146–156

    CAS  PubMed  Google Scholar 

  • Szymura JM, Barton NH (1991) The genetic structure of the hybrid zone between the fire-bellied toads Bombina bombina and B. variegata: comparisons between transects and between loci. Evolution 45:237–261

    Google Scholar 

  • Teeter KC, Thibodeau LM, Gompert Z, Buerkle CA, Nachman MW, Tucker PK (2010) The variable genomic architecture of isolation between hybridizing species of house mice. Evolution 64:472–485

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Tuskan GA, Gunter LE, Yang ZK, Yin TM, Sewell MM, DiFazio SP (2004) Characterization of microsatellites revealed by genomic sequencing of Populus trichocarpa. Can J For Res 34:85–93

    CAS  Google Scholar 

  • Vähä J-P, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72

    PubMed  Google Scholar 

  • van der Schoot J, Pospiskova M, Vosman B, Smulders MJM (2000) Development and characterization of microsatellite markers in black poplar (Populus nigra L.). Theor Appl Genet 101:317–322

    Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Google Scholar 

  • Walls S (2009) The role of climate in the dynamics of a hybrid zone in Appalachian salamanders. Glob Change Biol 15:1903–1910

    Google Scholar 

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

    Google Scholar 

  • Whitham TG, Martinsen GD, Floate KD, Dungey HS, Potts BM, Keim P (1999) Plant hybrid zones affect biodiversity: tools for a genetic-based understanding of community structure. Ecology (Wash DC) 80:416–428

    Google Scholar 

  • Whitham TG, Bailey JK, Schweitzer JA MSS, Bangert RK, LeRoy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523

    CAS  PubMed  Google Scholar 

  • Whitham TG, DiFazio SP, Schweitzer JA, Shuster SM, Allan GJ, Bailey JK, Woolbright SA (2008) Extending genomics to natural communities and ecosystems. Science 320:492–495

    CAS  PubMed  Google Scholar 

  • Whitney KD, Randell RA, Rieseberg LH (2006) Adaptive introgression of herbivore resistance traits in the weedy sunflower, Helianthus annuus. Am Nat 167:794–807

    PubMed  Google Scholar 

  • Whitney KD, Randell RA, Rieseberg LH (2010) Adaptive introgression of abiotic tolerance traits in the sunflower, Helianthus annuus. New Phytol 187:230–239

    PubMed  Google Scholar 

  • Zhu X, Luke A, Cooper RS, Quetermous T, Hanis C, Mosley T, Gu CC, Tang H, Rao DC, Risch N, Weder A (2005) Admixture mapping for hypertension loci with genome-scan markers. Nat Genet 37:177–181

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank M. Zinkgraf for help in the field; R. Cronn, K. Mayer, T. Max, and E. Olson for help in the lab; and H. Bothwell for providing unpublished data. Our research was supported by NSF–FIBR DEB-0425908.

Data archiving statement

All nuclear and cpDNA microsatellite data will be submitted to Dryad.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erika I. Hersch-Green.

Additional information

Communicated by P. Ingvarsson

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 71 kb)

ESM 2

(PDF 63 kb)

ESM 3

(PDF 120 kb)

ESM 4

(PDF 233 kb)

ESM 5

(PDF 51 kb)

ESM 6

(PDF 135 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hersch-Green, E.I., Allan, G.J. & Whitham, T.G. Genetic analysis of admixture and patterns of introgression in foundation cottonwood trees (Salicaceae) in southwestern Colorado, USA. Tree Genetics & Genomes 10, 527–539 (2014). https://doi.org/10.1007/s11295-014-0701-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-014-0701-9

Keywords

Navigation