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Geometric Morphometric Analyses of Leaf Shapes in Two Sympatric Geometric morphometric analyses of leaf shapes in two sympatric Chinese oaks: Quercus dentata Thunberg and Quercus aliena Blume (Fagaceae) Yuan Liu, Yuejuan Li, Jialin Song, Ruipu Zhang, Yu Yan, Yuyao Wang, Fang K. Du To cite this version: Yuan Liu, Yuejuan Li, Jialin Song, Ruipu Zhang, Yu Yan, et al.. Geometric morphometric analyses of leaf shapes in two sympatric Chinese oaks: Quercus dentata Thunberg and Quercus aliena Blume (Fagaceae). Annals of Forest Science, Springer Nature (since 2011)/EDP Science (until 2010), 2018, 75 (4), pp.90. 10.1007/s13595-018-0770-2. hal-02306695 HAL Id: hal-02306695 https://hal.archives-ouvertes.fr/hal-02306695 Submitted on 7 Oct 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Annals of Forest Science (2018) 75: 90 https://doi.org/10.1007/s13595-018-0770-2 RESEARCH PAPER Geometric morphometric analyses of leaf shapes in two sympatric Chinese oaks: Quercus dentata Thunberg and Quercus aliena Blume (Fagaceae) Yuan Liu1 & Yuejuan Li1 & Jialin Song2 & Ruipu Zhang3 & Yu Yan1 & Yuyao Wang1 & Fang K. Du1 Received: 6 June 2018 /Accepted: 14 September 2018 /Published online: 4 October 2018 # INRA and Springer-Verlag France SAS, part of Springer Nature 2018 Abstract & Key message Geometric morphometric analyses (GMMs) of the leaf shape can distinguish two congeneric oak species Quercus dentata Thunberg and Quercus aliena Blume in sympatric areas. & Contexts High genetic and morphological variation in different Quercus species hinder efforts to distinguish them. In China, Q. dentata and Q. aliena are generally sympatrically distributed in warm temperate forests, and share some leaf morphological characteristics. & Aims The aim of this study was to use the morphometric methods to discriminate these sympatric Chinese oaks preliminarily identified from molecular markers. & Methods Three hundred sixty-seven trees of seven sympatric Q. dentata and Q. aliena populations were genetically assigned to one of the two species or hybrids using Bayesian clustering analysis based on nSSR. This grouping served as a priori classification of the trees. Shapes of 1835 leaves from the 367 trees were analyzed in terms of 13 characters (landmarks) by GMMs. Correlations between environmental and leaf morphology parameters were studied using linear regression analyses. & Results The two species were efficiently discriminated by the leaf morphology analyses (96.9 and 95.9% of sampled Q. aliena trees and Q. dentata trees were correctly identified), while putative hybrids between the two species were found to be morpho- logically intermediate. Moreover, we demonstrated that the leaf morphological variations of Q. aliena, Q. dentata, and their putative hybrids are correlated with environmental factors, possibly because the variation of leaf morphology is part of the response to different habitats and environmental disturbances. & Conclusion GMMs were able to correctly classify individuals from the two species preliminary identified as Q. dentata or Q. aliena by nSSR. The high degree of classification accuracy provided by this approach may be exploited to discriminate other problematic species and highlight its utility in plant ecology and evolution studies. Keywords Geometric morphometrics . Genetic assignment . Leaf morphology . Quercus . Sympatric distribution Handling Editor: Erwin Dreyer Contribution of the co-authors F.K.D. designed the research; Y.L. performed the experiment and analysis; Y.J.L. performed the environmental correlation analysis; R.P. Z, Y.Y.,and Y.Y.W did sampling and assigned leaf landmarks; Y.L., J.L.S., and F.K.D. wrote the manuscript; All authors revised the manuscript. Electronic supplementary material The online version of this article (https://doi.org/10.1007/s13595-018-0770-2) contains supplementary material, which is available to authorized users. * Fang K. Du 2 School of Biological Science and Technology, University of Jinan, [email protected] 250022 Jinan, People’s Republic of China 3 Kunyushan National Forest Park, 264000 Yantai, People’s Republic 1 College of Forestry, Beijing Forestry University, of China 100083 Beijing, People’sRepublicofChina 90 Page 2 of 12 Annals of Forest Science (2018) 75: 90 1 Introduction Viscosi and Fortini 2011 ; Souza et al. 2012; Viscosi et al. 2009; Tucić et al. 2018). Moreover, recent advances have There are many phenotypic traits which can be used for the shown that combinations of leaf morphological characters differentiation of taxa, such as leaf morphology, anatomical and molecular markers can significantly improve taxonomic descriptors, and other structural characters. Among them, leaf delimitations (Viscosi et al. 2012;Rellstabetal.2016). morphology is important for differentiating plant taxa (Costa In recent years, molecular markers were widely used in et al. 2009), especially congeneric woody species, which tend species discrimination due to the rapid development of DNA to have little variation in floral features and short flowering technology (e.g., Jaramillo-Correa et al. 2008;Duetal.2011 seasons (Elias 1980). This is particularly true for oaks for gymnosperm-conifers; Arnold et al. 2012; Eaton et al. (Quercus L., Fagaceae), in which leaf features are Bthe most 2015 for angiosperms). Various molecular markers have been important^ characters for discrimination (Stace 1982). used for species classification. Among them, nuclear micro- Quercus is a genus of evergreen or deciduous shrubs and trees, satellite markers or simple sequence repeats (nSSRs) are bi- and the largest genus in the Fagaceae family. About 450 spe- parentally inherited and experience extensive gene flow cies are widely distributed in temperate and subtropical re- through both pollen and seeds (e.g., Petit et al. 2005;Du gions of the northern hemisphere (Nixon 1993, 1997;Huang et al. 2013). Due to their co-dominant inheritance, high degree et al. 1999a, b; Manos et al. 1999), and 35 species are widely of polymorphism and relative ease of transfer between closely distributed in China (Huang et al. 1999a, b). Quercus taxono- related species, nSSRs have become one of the most popular my is extremely complex due to wide geographical distribu- sources of molecular markers (Guichoux et al. 2011). Leaf tion and species overlap, high levels of variability and pheno- shape is mainly genetically fixed but also affected by environ- typic plasticity, and widespread hybridization where species mental factors (Graham et al. 2010). The environmental het- ranges overlap (Rushton 1993; Bacilieri et al. 1996;Manos erogeneity such as elevation, temperature, water, etc. can also et al. 1999; Petit et al. 2005;Gerberetal.2014). affect the shape and size of leaves, e.g., leaves must be as wide Thus, discriminating oak species in mixed stands is not as possible to absorb sufficient light and as flat and thin as straightforward. However, progress has been made in the de- possible to facilitate gas exchange, but will be dried out if too velopment of leaf morphological methods capable of resolv- wide and thin (Tsukaia 2005). Thus, it is important to take ing these problems in recent years. Traditional morphological environment factors into account when trying to explain the measurements typically apply statistical techniques to a wide morphological differences. range of measurements, such as distances and distance ratios, Quercus dentata Thunberg and Quercus aliena Blume are angles, areas, and volumes (Mitteroecker and Gunz 2009). It generally sympatrically distributed in warm temperate forests, can be efficient for discriminating the species. For example, and they are important components of both deciduous broad- Kremer et al. (2002) distinguished two oak species in nine leaved and mixed broad-leaved forests (Ren and Wang 1985; mixed oak stands using 14 shape-related traits. However, tra- Peng et al. 2007). The two species are found, and play major ditional morphological methods are not effective for shape ecological roles, on southern slopes of mountains in northern analysis, and do not allow interpretable graphic representa- China, and the neighboring countries Japan and Korea (Kazue tion. Modern geometric morphometric methods (GMMs) and Atsuko 2015). In addition, like other oaks, the two species using landmark and outline data are suitable for differentiating have great economic values, e.g., their leaves are used for complex taxa because they can partition total coordinate var- sericulture, fruits for starch extraction, and bark for tannin ex- iation into shape and non-shape (translation, rotation, and traction (Peng et al. 2007). Genetically, the two species are size) components, regardless of location, orientation, and members of the Quercus (white oak) section, closely related, scale factors (Slice 1996;MacLeodandForey2002;Adams and regarded as sister species (Hubert et al. 2014). There are et al. 2004; Mitteroecker and Gunz 2009; Viscosi et al. 2009). several major morphological differences between leaves of GMMs are also helpful for studying bilateral asymmetry and Q. dentata and Q. aliena: the former
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