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Genetic diversity in North American Cercis Canadensis reveals an ancient population bottleneck that originated after the last glacial maximum

  • 1.

    Hewitt, G. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913. https://doi.org/10.1038/35016000 (2000).

    ADS 
    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 2.

    Hewitt, G. Genetic consequences of climatic oscillations in the Quaternary. Philos. Trans. R. Soc. Lond. 359, 183–195. https://doi.org/10.1098/rstb.2003.1388 (2004).

    Article 
    CAS 

    Google Scholar 

  • 3.

    Ehlers, J. & Gibbard, P. Quaternary Glaciations-Extent and Chronology: Part I: Europe Vol. 2 (Elsevier, New York, 2004).

    Google Scholar 

  • 4.

    Call, A. et al. Genetic structure and post-glacial expansion of Cornus florida L. (Cornaceae): Integrative evidence from phylogeography, population demographic history, and species distribution modeling. J. Syst. Evol. 54, 136–151. https://doi.org/10.1111/jse.12171 (2016).

    Article 

    Google Scholar 

  • 5.

    Jackson, S. et al. Vegetation and environment in eastern North America during the Last Glacial Maximum. Quatern. Sci. Rev. 19, 489–508. https://doi.org/10.1016/S0277-3791(99)00093-1 (2000).

    ADS 
    Article 

    Google Scholar 

  • 6.

    Nadeau, S. et al. 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. Am. J. Bot. 102, 1342–1355. https://doi.org/10.3732/ajb.1500160 (2015).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 7.

    Beaulieu, J. & Simon, J. Genetic structure and variability in Pinus strobus in Quebec. Can. J. For. Res. 24, 1726–1733. https://doi.org/10.1139/x94-223 (1994).

    Article 

    Google Scholar 

  • 8.

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

    Article 
    PubMed 

    Google Scholar 

  • 9.

    Soltis, D., Morris, A., McLachlan, J., Manos, P. & Soltis, P. Comparative phylogeography of unglaciated eastern North America. Mol. Ecol. 15, 4261–4293. https://doi.org/10.1111/j.1365-294X.2006.03061.x (2006).

    Article 
    PubMed 

    Google Scholar 

  • 10.

    Mee, J. & Moore, J. The ecological and evolutionary implications of microrefugia. J. Biogeogr. 41, 837–841. https://doi.org/10.1111/jbi.12254 (2014).

    Article 

    Google Scholar 

  • 11.

    Hoban, S. et al. 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. Mol. Ecol. 19, 4876–4891. https://doi.org/10.1111/j.1365-294X.2010.04834.x (2010).

    Article 
    PubMed 

    Google Scholar 

  • 12.

    Hampe, A. & Petit, R. Conserving biodiversity under climate change: The rear edge matters. Ecol. Lett. 8, 461–467. https://doi.org/10.1111/j.1461-0248.2005.00739.x (2005).

    Article 
    PubMed 

    Google Scholar 

  • 13.

    Excoffier, L., Foll, M. & Petit, R. Genetic consequences of range expansions. Annu. Rev. Ecol. Evol. Syst. 40, 481–501. https://doi.org/10.1146/annurev.ecolsys.39.110707.173414 (2009).

    Article 

    Google Scholar 

  • 14.

    McLachlan, J., Clark, J. & Manos, P. Molecular indicators of tree migration capacity under rapid climate change. Ecology 86, 2088–2098. https://doi.org/10.1890/04-1036 (2005).

    Article 

    Google Scholar 

  • 15.

    Bemmels, J. & Dick, C. Genomic evidence of a widespread southern distribution during the Last Glacial Maximum for two eastern North American hickory species. J. Biogeogr. 45, 1739–1750. https://doi.org/10.1111/jbi.13358 (2018).

    Article 

    Google Scholar 

  • 16.

    Jaramillo-Correa, J., Beaulieu, J., Khasa, D. & Bousquet, J. Inferring the past from the present phylogeographic structure of North American forest trees: Seeing the forest for the genes. Can. J. For. Res. 39, 286–307. https://doi.org/10.1139/X08-181 (2009).

    Article 

    Google Scholar 

  • 17.

    Eckert, C., Samis, K. & Lougheed, S. Genetic variation across species’ geographical ranges: The central–marginal hypothesis and beyond. Mol. Ecol. 17, 1170–1188. https://doi.org/10.1111/j.1365-294X.2007.03659.x (2008).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 18.

    Foll, M. & Gaggiotti, O. Identifying the environmental factors that determine the genetic structure of populations. Genetics 174, 875–891. https://doi.org/10.1534/genetics.106.059451 (2006).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar 

  • 19.

    Loveless, M. & Hamrick, J. Ecological determinants of genetic structure in plant populations. Ann. Rev. Ecol. Syst. 15, 65–95. https://doi.org/10.1146/annurev.es.15.110184.000433 (1984).

    Article 

    Google Scholar 

  • 20.

    Roberts, D., Werner, D., Wadl, P. & Trigiano, R. Inheritance and allelism of morphological traits in eastern redbud (Cercis canadensis L.). Hortic. Res. 2, 1–11 (2015).

    Article 

    Google Scholar 

  • 21.

    Couvillon, G. Cercis canadensis L. seed size influences germination rate, seedling dry matter, and seedling leaf area. HortScience 37, 206–207 (2002).

    Article 

    Google Scholar 

  • 22.

    Li, S. et al. Methods for breaking the dormancy of eastern redbud (Cercis canadensis) seeds. Seed Sci. Technol. 41, 27–35 (2013).

    Article 

    Google Scholar 

  • 23.

    Cheong, E. & Pooler, M. Micropropagation of Chinese redbud (Cercis yunnanensis) through axillary bud breaking and induction of adventitious shoots from leaf pieces. In Vitro Cell. Dev. Biol. Plant 39, 455–458 (2003).

    Article 

    Google Scholar 

  • 24.

    Pooler, M., Jacobs, K. & Kramer, M. Differential resistance to Botryosphaeria ribis among Cercis taxa. Plant Dis. 86, 880–882. https://doi.org/10.1094/PDIS.2002.86.8.880 (2002).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 25.

    Trigiano, R., Beaty, R. & Graham, E. Somatic embryogenesis from immature embryos of redbud (Cercis canadensis). Plant Cell Rep. 7, 148–150. https://doi.org/10.1007/BF00270127 (1988).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 26.

    Wadl, P., Trigiano, R., Werner, D., Pooler, M. & Rinehart, T. Simple sequence repeat markers from Cercis canadensis show wide cross-species transfer and use in genetic studies. J. Am. Soc. Hortic. Sci. 137, 189–201. https://doi.org/10.21273/JASHS.137.3.189 (2012).

    Article 

    Google Scholar 

  • 27.

    Ony, M. et al. Habitat fragmentation influences genetic diversity and differentiation: Fine-scale population structure of Cercis canadensis (eastern redbud). Ecol. Evol. 10, 3655–3670. https://doi.org/10.1002/ece3.6141 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 28.

    Amos, W. et al. Automated binning of microsatellite alleles: Problems and solutions. Mol. Ecol. Resour. 7, 10–14. https://doi.org/10.1111/j.1471-8286.2006.01560.x (2007).

    Article 
    CAS 

    Google Scholar 

  • 29.

    R: A language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria, 2019).

  • 30.

    Kamvar, Z., Tabima, J. & Grünwald, N. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281. https://doi.org/10.7717/peerj.281 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 31.

    Kamvar, Z., Brooks, J. & Grünwald, N. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front. Genet. 6, 208. https://doi.org/10.3389/fgene.2015.00208 (2015).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar 

  • 32.

    Tsui, C. et al. Population structure and migration pattern of a conifer pathogen, Grosmannia clavigera, as influenced by its symbiont, the mountain pine beetle. Mol. Ecol. 21, 71–86. https://doi.org/10.1111/j.1365-294X.2011.05366.x (2012).

    Article 
    PubMed 

    Google Scholar 

  • 33.

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

    Article 
    CAS 

    Google Scholar 

  • 34.

    Shannon, C. E. A mathematical theory of communication. Bell System Tech. J. 27, 379–423 (1948).

    MathSciNet 
    Article 

    Google Scholar 

  • 35.

    Goudet, J. Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol. Ecol. Notes 5, 184–186. https://doi.org/10.1111/j.1471-8286.2004.00828.x (2005).

    Article 

    Google Scholar 

  • 36.

    Hurlbert, S. The nonconcept of species diversity: A critique and alternative parameters. Ecology 52, 577–586. https://doi.org/10.2307/1934145 (1971).

    Article 

    Google Scholar 

  • 37.

    El Mousadik, A. & Petit, R. High level of genetic differentiation for allelic richness among populations of the Argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor. Appl. Genet. 92, 832–839. https://doi.org/10.1007/BF00221895 (1996).

    Article 
    PubMed 

    Google Scholar 

  • 38.

    Bird, C., Karl, S., Smouse, P. & Toonen, R. In Phylogeography and Population Genetics in Crustacea Vol. 19 (eds Held Christoph, Koenemann Stefan, & Schubart Christoph) pp. 31–55 (Boca Raton, FL: CRC Press, 2011).

  • 39.

    Meirmans, P. & Hedrick, P. Assessing population structure: FST and related measures. Mol. Ecol. Resour. 11, 5–18. https://doi.org/10.1111/j.1755-0998.2010.02927.x (2011).

    Article 
    PubMed 

    Google Scholar 

  • 40.

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

    Article 
    CAS 

    Google Scholar 

  • 41.

    Earl, D. & Bridgett, V. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7 (2012).

    Article 

    Google Scholar 

  • 42.

    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x (2005).

    Article 
    CAS 

    Google Scholar 

  • 43.

    Francis, R. Pophelper: An R package and web app to analyse and visualize population structure. Mol. Ecol. Resour. 17, 27–32. https://doi.org/10.1111/1755-0998.12509 (2017).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 44.

    Becker, R. & Wilks, A. MAPS: An R Package to Drae Geographical Maps (Version package 3.3.0, 2018).

  • 45.

    Lemon, J. Plotrix: An R Package for Various Plotting Functions (Version R package 3.8–1, 2006).

  • 46.

    Bruvo, R., Michiels, N., D’souza, T. & Schulenburg, H. A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol. Ecol. 13, 2101–2106. https://doi.org/10.1111/j.1365-294X.2004.02209.x (2004).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 47.

    Grünwald, N., Everhart, S., Knaus, B. & Kamvar, Z. Best practices for population genetic analyses. Phytopathology 107, 1000–1010. https://doi.org/10.1094/PHYTO-12-16-0425-RVW (2017).

    Article 
    PubMed 

    Google Scholar 

  • 48.

    Jombart, T. & Ahmed, I. adegenet 1.3–1: New tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3072. https://doi.org/10.1093/bioinformatics/btr521 (2011).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar 

  • 49.

    Jombart, T., Devillard, S. & Balloux, F. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11, 9. https://doi.org/10.1186/1471-2156-11-94 (2010).

    Article 

    Google Scholar 

  • 50.

    Cullingham, C., Cooke, J. & Coltman, D. Effects of introgression on the genetic population structure of two ecologically and economically important conifer species: Lodgepole pine (Pinus contorta var. latifolia) and jack pine (Pinus banksiana). Genome 56, 577–585. https://doi.org/10.1139/gen-2013-0071 (2013).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 51.

    Diniz-Filho, J. et al. Mantel test in population genetics. Genet. Mol. Biol. 36, 475–485. https://doi.org/10.1590/S1415-47572013000400002 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 52.

    Mantel, N. The detection of disease clustering and a generalized regression approach. Can. Res. 27, 209–220 (1967).

    CAS 

    Google Scholar 

  • 53.

    Vegan: Community ecology package v. R package version 2.5–3 (R package version 2.5–3). (2018).

  • 54.

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

    Article 
    CAS 

    Google Scholar 

  • 55.

    Cornuet, J., Ravigné, V. & Estoup, A. Inference on population history and model checking using DNA sequence and microsatellite data with the software DIYABC (v1.0). BMC Bioinform. 11, 401–411. https://doi.org/10.1186/1471-2105-11-401 (2010).

    Article 
    CAS 

    Google Scholar 

  • 56.

    Cornuet, J. et al. DIYABC v2.0: A software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30, 1187–1189. https://doi.org/10.1093/bioinformatics/btt763 (2014).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 57.

    Dickson, J. In Silvics of North America Vol. 2 (eds Burns, R. & Honkala, B.) 266–269 (United States Department of Agriculture-Forest Service, 1990).

  • 58.

    Thomson, A., Dick, C. & Dayanandan, S. A similar phylogeographical structure among sympatric North American birches (Betula) is better explained by introgression than by shared biogeographical history. J. Biogeogr. 42, 339–350. https://doi.org/10.1111/jbi.12394 (2015).

    Article 

    Google Scholar 

  • 59.

    Petit, R. et al. Glacial refugia: Hotspots but not melting pots of genetic diversity. Science 300, 1563–1565 (2003).

    ADS 
    Article 
    CAS 

    Google Scholar 

  • 60.

    David, R. & Hamann, A. Glacial refugia and modern genetic diversity of 22 western North American tree species. Proc. R. Soc. B Biol. Sci. 282, 20142903. https://doi.org/10.1098/rspb.2014.2903 (2015).

    Article 

    Google Scholar 

  • 61.

    Lumibao, C., Hoban, S. & McLachlan, J. Ice ages leave genetic diversity ‘hotspots’ in Europe but not in Eastern North America. Ecol. Lett. 20, 1459–1468. https://doi.org/10.1111/ele.12853 (2017).

    Article 
    PubMed 

    Google Scholar 

  • 62.

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

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 63.

    Petit, R. Early insights into the genetic consequences of range expansions. Heredity 106, 203–204. https://doi.org/10.1038/hdy.2010.60 (2011).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 64.

    Dubreuil, M. et al. Genetic effects of chronic habitat fragmentation revisited: Strong genetic structure in a temperate tree, Taxus baccata (Taxaceae), with great dispersal capability. Am. J. Bot. 97, 303–310. https://doi.org/10.3732/ajb.0900148 (2010).

    Article 
    PubMed 

    Google Scholar 

  • 65.

    Hamrick, J., Godt, M. & Sherman-Broyles, S. In Population Genetics of Forest Trees Vol. 42 (eds Adams, W., Strauss, S., Copes, D. & Griffin, A) 95–124 (Springer, Dordrecht, 1992).

  • 66.

    Hamrick, J. & Godt, M. Effects of life history traits on genetic diversity in plant species. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 351, 1291–1298 (1996).

    ADS 
    Article 

    Google Scholar 

  • 67.

    Spaulding, H. & Rieske, L. The aftermath of an invasion: Structure and composition of central appalachian hemlock forests following establishment of the hemlock woolly adelgid, Aelges tsugae. Biol. Invasions 12, 3135–3143. https://doi.org/10.1007/s10530-010-9704-0 (2010).

    Article 

    Google Scholar 

  • 68.

    Hadziabdic, D. et al. Analysis of genetic diversity in flowering dogwood natural stands using microsatellites: The effects of dogwood anthracnose. Genetica 138, 1047–1057. https://doi.org/10.1007/s10709-010-9490-8 (2010).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 69.

    Marquardt, P., Echt, C., Epperson, B. & Pubanz, D. Genetic structure, diversity, and inbreeding of eastern white pine under different management conditions. Can. J. For. Res. 37, 2652–2662 (2007).

    Article 
    CAS 

    Google Scholar 

  • 70.

    Potter, K. et al. Widespread inbreeding and unexpected geographic patterns of genetic variation in eastern hemlock (Tsuga canadensis), an imperiled North American conifer. Conserv. Genet. 13, 475–498. https://doi.org/10.1007/s10592-011-0301-2 (2012).

    Article 

    Google Scholar 

  • 71.

    Thammina, C., Kidwell-Slak, D., Lura, S. & Pooler, M. SSR markers reveal the genetic diversity of asian Cercis taxa at the US National Arboretum. HortScience 52, 498–502. https://doi.org/10.21273/hortsci11441-16 (2017).

    Article 

    Google Scholar 

  • 72.

    Chang, C., Bongarten, B. & Hamrick, J. Genetic structure of natural populations of black locust (Robinia pseudoacacia L.) at Coweeta, North Carolina. J. Plant Res. 111, 17–24. https://doi.org/10.1007/BF02507146.pdf (1998).

    Article 

    Google Scholar 

  • 73.

    Marquardt, P. & Epperson, B. Spatial and population genetic structure of microsatellites in white pine. Mol. Ecol. 13, 3305–3315. https://doi.org/10.1111/j.1365-294X.2004.02341.x (2004).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 74.

    Victory, E., Glaubitz, J., Rhodes-Jr, O. & Woeste, K. Genetic homogeneity in Juglans nigra (Juglandaceae) at nuclear microsatellites. Am. J. Bot. 93, 118–126. https://doi.org/10.3732/ajb.93.1.118 (2006).

    Article 
    CAS 

    Google Scholar 

  • 75.

    Hadziabdic, D. et al. Genetic diversity of flowering dogwood in the Great Smoky Mountains National Park. Tree Genet. Genomes 8, 855–871. https://doi.org/10.1007/s11295-012-0471-1 (2012).

    Article 

    Google Scholar 

  • 76.

    Nybom, H. Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol. Ecol. 13, 1143–1155. https://doi.org/10.1111/j.1365-294X.2004.02141.x (2004).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 77.

    Donselman, H. Variation in native populations of eastern redbud (Cercis canadensis L.) as influenced by geographic location [USA]. In Proceedings, of the Florida State Horticulture Society Vol. 89. 370–373 (1976).

  • 78.

    Dirr, M. Manual of Woody Landscape Plants: Their Identification, Ornamental Characteristics, Culture, Propagation and Uses (Stipes Publishing Co, Champaign, 1990).

    Google Scholar 

  • 79.

    Fritsch, P., Schiller, A. & Larson, K. Taxonomic implications of morphological variation in Cercis canadensis (Fabaceae) from Mexico and adjacent parts of Texas. Syst. Bot. 34, 510–520. https://doi.org/10.1600/036364409789271254 (2009).

    Article 

    Google Scholar 

  • 80.

    Nevo, E. et al. Drought and light anatomical adaptive leaf strategies in three woody species caused by microclimatic selection at evolution canyon, Israel. Israel J. Plant Sci. 48, 33–46 (2000).

    Google Scholar 

  • 81.

    Fritsch, P. et al. Leaf adaptations and species boundaries in North American Cercis: Implications for the evolution of dry floras. Am. J. Bot. 105, 1577–1594. https://doi.org/10.1002/ajb2.1155 (2018).

    Article 
    PubMed 

    Google Scholar 

  • 82.

    Raulston, J. Redbud. Am. Nurseryman 171, 39–51 (1990).

    Google Scholar 

  • 83.

    Robertson, K. Cercis: The redbuds. Arnoldia 36, 37–49 (1976).

    Google Scholar 

  • 84.

    Davis, C., Fritsch, P., Li, J. & Donoghue, M. Phylogeny and biogeography of Cercis (Fabaceae): Evidence from nuclear ribosomal ITS and chloroplast ndhF sequence data. Syst. Bot. 27, 289–302. https://doi.org/10.1043/0363-6445-27.2.289 (2002).

    Article 

    Google Scholar 

  • 85.

    Hopkins, M. In Rhodora Vol. 44 (eds M Fernald, C Eatherby, L Griscom, & S Marris) 193–211 (New England Botanical Club, Inc., 1942).

  • 86.

    Griffin, J., Ranney, T. & Pharr, D. Heat and drought influence photosynthesis, water relations, and soluble carbohydrates of two ecotypes of redbud (Cercis canadensis). J. Am. Soc. Hortic. Sci. 129, 497–502. https://doi.org/10.21273/JASHS.129.4.0497 (2004).

    Article 
    CAS 

    Google Scholar 

  • 87.

    Fritsch, P. & Cruz, B. Phylogeny of Cercis based on DNA sequences of nuclear ITS and four plastid regions: Implications for transatlantic historical biogeography. Mol. Phylogenet. Evol. 62, 816–825. https://doi.org/10.1016/j.ympev.2011.11.016 (2012).

    Article 
    PubMed 

    Google Scholar 

  • 88.

    Chung, M., Chung, M., Oh, G. & Epperson, B. Spatial genetic structure in a Neolitsea sericea population (Lauraceae). Heredity 85, 490–497. https://doi.org/10.1046/j.1365-2540.2000.00781.x (2000).

    Article 
    PubMed 

    Google Scholar 

  • 89.

    Dean, D. et al. Analysis of genetic diversity and population structure for the native tree Viburnum rufidulum occurring in Kentucky and Tennessee. J. Am. Soc. Hortic. Sci. 140, 523–531. https://doi.org/10.21273/JASHS.140.6.523 (2015).

    Article 
    CAS 

    Google Scholar 

  • 90.

    Hagler, J., Mueller, S., Teuber, L., Machtley, S. & Van-Deynze, A. Foraging range of honey bees, Apis mellifera, in alfalfa seed production fields. J. Insect Sci. 11, 144. https://doi.org/10.1673/031.011.14401 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 91.

    Pasquet, R. et al. Long-distance pollesn flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proc. Natl. Acad. Sci. 105, 13456–13461 (2008).

    ADS 
    Article 

    Google Scholar 

  • 92.

    Hayden, W. Redbud seedpods hold surprises. Bull. Virginia Native Plant Soc. 32, 1–6 (2013).

    Google Scholar 

  • 93.

    Schnabel, A., Laushman, R. & Hamrick, J. Comparative genetic structure of two co-occurring tree species, Maclura pomifera (Moraceae) and Gleditsia triacanthos (Leguminosae). Heredity 67, 357–364. https://doi.org/10.1038/hdy.1991.99 (1991).

    Article 

    Google Scholar 

  • 94.

    Nakanishi, A., Tomaru, N., Yoshimaru, H., Manabe, T. & Yamamoto, S. Effects of seed- and pollen-mediated gene dispersal on genetic structure among Quercus salicina saplings. Heredity 102, 182–189. https://doi.org/10.1038/hdy.2008.101 (2008).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 95.

    Vekemans, X. & Hardy, O. New insights from fine-scale spatial genetic structure analyses in plant populations. Mol. Ecol. 13, 921–935. https://doi.org/10.1046/j.1365-294X.2004.02076.x (2004).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 96.

    Gonzales, E., Hamrick, J., Smouse, P., Trapnell, D. & Peakall, R. The impact of landscape disturbance on spatial genetic structure in the Guanacaste tree, Enterolobium cyclocarpum (Fabaceae). J. Hered. 101, 133–143. https://doi.org/10.1093/jhered/esp101 (2009).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 97.

    Post, D. Change in nutrient content of foods stored by eastern woodrats (Neotoma floridana). J. Mammal. 73, 835–839 (1992).

    Article 

    Google Scholar 

  • 98.

    Surrency, D. & Owsley, C. (ed. Natural Resources Conservation Service United States Department of Agriculture) 146 (United States Department of Agriculture, Natural Resources Conservation Service, 2001).

  • 99.

    Wakeland, B. & Swihart, R. Ratings of white-tailed deer preferences for woody browse in Indiana. Proceedings of the Indiana Academy of Science 118, 96–101 (2009).

    Google Scholar 

  • 100.

    Wright, V., Fleming, E. & Post, D. Survival of Rhyzopertha dominica (Coleoptera, Bostrichidae) on fruits and seeds collected from woodrat nests in Kansas. J. Kansas Entomol. Soc. 63, 344–347 (1990).

    Google Scholar 

  • 101.

    Sullivan, J. (ed. Forest Service U.S. Department of Agriculture, Rocky Mountain Research Station) (U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station. Fire Sciences Laboratory, 1994).

  • 102.

    Weir, B. & Ott, J. Genetic data analysis II. Trends Genet. 13, 379 (1997).

    Article 

    Google Scholar 

  • 103.

    Magni, C., Ducousso, A., Caron, H., Petit, R. & Kremer, A. Chloroplast DNA variation of Quercus rubra L. in North America and comparison with other Fagaceae. Mol. Ecol. 14, 513–524. https://doi.org/10.1111/j.1365-294X.2005.02400.x (2005).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 104.

    Peterson, B. & Graves, W. Chloroplast phylogeography of Dirca palustris L. indicates populations near the glacial boundary at the Last Glacial Maximum in eastern North America. Journal of Biogeography 43, 314–327, doi:https://doi.org/10.1111/jbi.12621 (2016).

  • 105.

    Shaw, J. & Small, R. Chloroplast DNA phylogeny and phylogeography of the North American plums (Prunus subgenus Prunus section Prunocerasus, Rosaceae). Am. J. Bot. 92, 2011–2030. https://doi.org/10.3732/ajb.92.12.2011 (2005).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 106.

    Rowe, K., Heske, E., Brown, P. & Paige, K. Surviving the ice: Northern refugia and postglacial colonization. Proc. Natl. Acad. Sci. 101, 10355–10359 (2004).

    ADS 
    Article 
    CAS 

    Google Scholar 

  • 107.

    Graignic, N., Tremblay, F. & Bergeron, Y. Influence of northern limit range on genetic diversity and structure in a widespread North American tree, sugar maple (Acer saccharum Marshall). Ecol. Evol. 8, 2766–2780. https://doi.org/10.1002/ece3.3906 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 108.

    Bemmels, J., Knowles, L. & Dick, C. Genomic evidence of survival near ice sheet margins for some, but not all, North American trees. Proc. Natl. Acad. Sci. 116, 8431–8436. https://doi.org/10.7302/Z2JS9NNG (2019).

    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar 

  • 109.

    Jia, H. & Steven, R. Fossil leaves and fruits of Cercis L. (Leguminosae) from the Eocene of western North America. International Journal of Plant Sciences 175, 601–612, doi:https://doi.org/10.1086/675693 (2014).

  • 110.

    Kraemer, M. & Favi, F. Emergence phenology of Osmia lignaria subsp lignaria (Hymenoptera: Megachilidae), its parasitoid Chrysura kyrae (Hymenoptera: Chrysididae), and bloom of Cercis canadensis. Environ. Entomol. 39, 351–358. https://doi.org/10.1603/en09242 (2010).

    Article 
    PubMed 
    CAS 

    Google Scholar 

  • 111.

    USDA. Census of horticultural specialties. Volume 3 AC-12-SS-3, Washington, DC (2014).


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