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Genetic, Morphological, and Spectral Characterization of Relictual Niobrara River Hybrid Aspens ( Populus ×Smithii ) 1

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Genetic, Morphological, and Spectral Characterization of Relictual Niobrara River Hybrid Aspens ( Populus ×Smithii ) 1 AJB Advance Article published on December 15, 2017, as 10.3732/ajb.1700268. The latest version is at http://www.amjbot.org/cgi/doi/10.3732/ajb.1700268 RESEARCH ARTICLE AMERICAN JOURNAL OF BOTANY Genetic, morphological, and spectral characterization of relictual Niobrara River hybrid aspens ( Populus × smithii ) 1 Nicholas John Deacon 2,3,5 , Jake Joseph Grossman 2,5, Anna Katharina Schweiger 2 , Isabella Armour4 , and Jeannine Cavender-Bares2 PREMISE OF THE STUDY: Aspen groves along the Niobrara River in Nebraska have long been a biogeographic curiosity due to morphological diff erences from nearby remnant Populus tremuloides populations. Pleistocene hybridization between P. tremuloides and P. grandidentata has been proposed, but the nearest P. grandidentata populations are currently several hundred kilometers east. We tested the hybrid-origin hypothesis using genetic data and char- acterized putative hybrids phenotypically. METHODS: We compared nuclear microsatellite loci and chloroplast sequences of Niobrara River aspens to their putative parental species. Parental species and putative hybrids were also grown in a common garden for phenotypic comparison. On the common garden plants, we measured leaf morphological traits and leaf-level spectral refl ectance profi les, from which chemical traits were derived. KEY RESULTS: The genetic composition of the three unique Niobrara aspen genotypes is consistent with the hybridization hypothesis and with maternal chloroplast inheritance from P. grandidentata . Leaf margin dentition and abaxial pubescence diff erentiated taxa, with the hybrids showing intermediate values. Spectral profi les allowed statistical separation of taxa in short-wave infrared wavelengths, with hybrids showing intermediate values, indicating that traits associated with internal structure of leaves and water absorption may vary among taxa. However, refl ectance values in the visible region did not diff erentiate taxa, indicating that traits related to pigments are not diff erentiated. CONCLUSIONS: Both genetic and phenotypic results support the hypothesis of a hybrid origin for these genetically unique aspens. However, low genetic diversity and ongoing ecological and climatic threats to the hybrid taxon present a challenge for conservation of these relictual boreal communities. KEY WORDS clonal growth; common garden; hybridization; Populus ; Nebraska; Niobrara River; relictual communities; Salicaceae; Smith’s aspen; spectra Interspecific hybridization is widespread across the flowering in other cases in which intraspecifi c sexual reproduction may be plants ( Mallet, 2005 ), oft en leading to the formation of genetically limited, hybridization can present critical opportunities for adap- diverse hybrid zones where interfertile parental populations meet tive evolution and conservation of threatened stands ( Allendorf ( Barton and Hewitt, 1985 ). It is increasingly recognized that inter- et al., 2001 ; Seehausen, 2004 ; Bridle and Vines, 2007 ). Lotsy (1925) specifi c hybridization can play an important role in adaptation to originally hypothesized the nature and importance of this phenom- changing environments, particularly in long-lived plants ( Holliday, enon using the term syngameon, referring to lineages capable of 2006 ). Especially at the range boundaries of one or more species, or adaptive introgression. Th e phenotypic outcomes and genetic architecture of hybridiza- 1 Manuscript received 6 July 2017; revision accepted 6 November 2017. tion can vary widely, even in separate cases involving the same 2 Ecology, Evolution and Behavior, University of Minnesota, 140 Gortner Laboratory, 1479 parental species ( Rieseberg, 1991 ; Steen et al., 2000 ). Among phe- Gortner Avenue, St. Paul, MN 55108 USA; and notypic traits, leaf morphology is readily accessible for identifying 3 Plant Biology, University of Minnesota, 140 Gortner Laboratory, 1479 Gortner Avenue, and classifying species and has long been used for this purpose, but St. Paul, MN 55108 USA 4 Author for correspondence (e-mail: [email protected]) it can be infl uenced by environmental variation ( Klingenberg, 2002 ; 5 Equal contributors Cristofolini and Crema, 2005 ; González-Rodríguez and Oyama, https://doi.org/10.3732/ajb.1700268 2005 ; Ives et al., 2007 ; Viscosi et al., 2009 ; Hulshof and Swenson, AMERICAN JOURNAL OF BOTANY 104 (12): 1 – 13 , 2017; http://www.amjbot.org/ © 2017 Botanical Society of America • 1 Copyright 2017 by the Botanical Society of America 2 • AMERICAN JOURNAL OF BOTANY 2010 ). Common garden comparisons eliminate uncertainty related is the case, these hybrids are isolated from the nearest stand of to the eff ect of the environment and allow for comparisons between quaking aspen by 60 km and from the western range edge of big- species based on genetically controlled variation ( Rowland, 2001 ; tooth aspen by 650 km. Yet before the eastward range contraction Givnish and Montgomery, 2014 ; Zohner and Renner, 2014 ). Ad- of bigtooth aspen at the end of the Pleistocene, both species were vances in molecular techniques have also made it possible to deter- abundant in the Midwestern United States ( Wright et al., 1985 ). As mine the genetic architecture of hybridization. Characterization of such, the NRV aspens would be not only an unusual Pleistocene biparentally inherited nuclear genomes and uniparentally inherited relict, but also of special conservation interest since hybrids occur- chloroplast and mitochondrial genomes can indicate the pattern of ring at the “rear edge” of a retracting parental range ( Petit et al., hybridization where morphological evidence is unclear or cryptic 2005 ) and/or in proximity to or associated with relatively isolated, ( Isoda et al., 2000 ). Depending on the directionality of hybridiza- peripheral stands of either parent ( Leppig and White, 2006 ) can tion, hybrid genomes—and especially cytoplasmically inherited harbor unique adaptive genetic diversity ( Kramer et al., 2008 ). De- components of the genome like the chloroplast—can be predomi- spite considerable treatment of aspen phylogenetics ( Hamzeh and nantly derived from one parental species ( Hamzeh et al., 2007 ; Dayanandan, 2004 ; Cervera et al., 2005 ; Wang et al., 2015 ) and hy- Hamilton and Aitken, 2013 ) or relatively equally from both ( Hersch- bridization ( Hamzeh et al., 2007 ; Hersch-Green et al., 2014 ; Floate Green et al., 2014 ; Floate et al., 2016 ), with commensurate impacts et al., 2016 ) as well as eff orts to produce Smith’s aspen artifi cially on morphology ( Wu et al., 1997 ; Floate, 2004 ; Tovar-Sánchez and as a potential timber cultivar in areas where the parental ranges Oyama, 2004 ). currently overlap ( Reighard and Hanover, 1984 ; Reighard and Th erefore, while phenotypic information can be informative in Hanover, 1990 ), to our knowledge, systematic molecular and mor- identifying hybrids, individual traits are rarely suffi cient, and the phological analyses have yet to demonstrate that NRV aspens are eff ort to measure dozens of traits individually is intractable for fi eld hybrids formed during historical range overlap between P. grandi- observations. Spectral characteristics of plants measured across a dentata and P. tremuloides in this region. wide range of wavelengths could potentially provide an integrated Currently, NRV aspen stands appear to suff er from various means to describe their phenotype, given that anatomical proper- threats, including decline related to herbivore browsing, disease, ties of plant cells and tissues have wavelength-specifi c absorbance, and cedar encroachment ( Robertson, 2015 ). Th eir decline mirrors refl ectance, and transmittance features ( Li et al., 2014 ). Leaf spectra that of NRV paper birch (Betula papyrifera ) populations, which are also strongly associated with genetic and phylogenetic informa- have similar physiological tolerances to aspens, and their decline tion, even able to diff erentiate diff erent populations of the same has been attributed to climate change ( Stroh and Miller, 2009 ; species ( Madritch et al., 2014 ; Cavender-Bares et al., 2016 ). Leaf Stroh, 2011 ). Numerous western quaking aspen stands have already spectra are determined by leaf tissue composition: plant pigments collapsed due to a complex combination of physiological stress and absorb most of the incident light in the visible part of the elec- infestation by pathogens and insect pests in a phenomenon termed tromagnetic spectrum (VIS, ca. 400–700 nm), while changes in vi- sudden aspen decline (SAD, Rehfeldt et al., 2009 ; Anderegg et al., brational and rotational frequencies of larger molecules, such as 2012 ; Anderegg et al., 2013 ; Worrall et al., 2013 , 2015 ), and both carbohydrates, proteins, and water cause characteristic absorption quaking and bigtooth aspen are predicted to experience range re- features in the near-infrared (NIR, ca. 700–1400 nm) and short- traction with further climate change ( Iverson and Prasad, 2002 ; wave infrared (SWIR, ca. 1400–2400 nm) regions of the spectrum. Iverson et al., 2008 ). Th e entire range of the NRV aspen population In addition, internal and external structural components of leaves, is within the boundaries of the National Park Service’s Niobrara such as air–cell interfaces, trichomes, and the cuticle, cause absorp- National Scenic River unit, and land managers require a more tion and light scattering at these longer wavelengths ( Ollinger, complete understanding of the identity and diversity of the stands 2011 ). Classifi cation methods based on leaf
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