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Genetic, geographic, and climatic factors jointly shape leaf morphology of an alpine oak, Quercus aquifolioides Rehder & E.H. Wilson

Abstract

Key message

Leaf symmetry and leaf size are explained by genetic variation between and within lineages and to a lesser extent by climatic factors, while leaf asymmetry can only be partly explained by geographic factors in Quercus aquifolioides Rehder & E.H. Wilson.

Context

Leaves are the primary photosynthetic organs of plants, and their morphology affects various crucial physiological processes potentially linked to fitness.

Aims

We explored the variation in leaf morphology of an alpine oak, Quercus aquifolioides, in order to examine its relationship to genetic, geographic, and climatic factors.

Methods

We conducted a genetic survey using 25 nuclear microsatellites. Based on Bayesian clustering analysis, 273 sampled trees from 29 populations of Q. aquifolioides were assigned to two lineages that correspond to the Western Sichuan Plateau-Hengduan Mountains (WSP-HDM) and Tibet geographic areas, with some individuals showing mixed ancestry. To undertake morphological analyses, we collected 1435 leaves from these trees and characterized them in terms of 13 landmarks. The metric dimensions of these leaves were digitally captured in the two-dimensional coordinates of these landmarks, then divided into leaf size and symmetric and asymmetric components of leaf shape. To analyze how different components of leaf morphology vary across lineages, we employed Procrustes Analysis of Variance (ANOVA), two-block partial least-square analysis (2B-PLS), and several other multivariate analysis approaches. We also applied distance-based redundancy analysis (dbRDAs) to explore relations between leaf morphology and genetic, geographic, and climatic factors.

Results

Multivariate analysis indicated significant differentiation in leaf symmetric shape components and leaf size between the WSP-HDM and Tibet lineages, while the mixed individuals were morphologically intermediate. The dbRDA analysis showed that most of the variation in symmetric components and leaf size was explained by genotypic effects, with the symmetric components of leaf shape being also significantly explained by geography and climate; however, variation in asymmetric components is only very weakly explained by geography.

Conclusion

Our results demonstrated that leaf morphological variation in shape and size across Q. aquifolioides geographic range is related to both its genetic differentiation and to a lesser extent to climatic factors. We discuss how these patterns could be interpreted in terms of both geographical isolations among and within lineages, and possible adaptive responses for particular traits, in contrast to asymmetric variation.

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Data availability

Data for this study are available at figshare: https://doi.org/10.6084/m9.figshare.14579349

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Acknowledgements

We indebted to two anonymous reviewers for helpful comments on a previous version of this manuscript. We thank Dr. Pauline Garnier- Géré from INRAE, France, for thorough and constructive review of this manuscript, and especially for her contribution to the Bayesian analysis and reorganizing the discussion part. We thank Dr. Rong Wang working in East China Normal University for comments on the manuscript. We thank Yi Zhang and Yang Xu from BFU, China, for suggestions on the revised version of manuscript and sampling.

Funding

This research was supported by the National Science Foundation of China (grant no. 42071060) to FKD. Stays of FKD and YJL in Japan were supported by the JST SAKURA SCIENCE Exchange Program (Sakura Science Plan), Japan.

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Correspondence to Fang K. Du.

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Contribution of co-authors F.K.D. designed the research; Y.J.L. performed the analysis and wrote the manuscript under the help of F.K.D.; Y.Y.Z. wrote the manuscript partly; P.C.L. performed the redundancy analysis; T.R.W. did sampling; X.Y.W. assigned leaf landmarks; S.U. reviewed and revised the paper. All authors revised the manuscript.

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Appendix

Appendix

Table 4 Geographical location of each population and numbers of individuals within it assigned to indicated lineages based on genotype assignment (Q = 0.8)
Table 5 Information regarding the 25 nuclear simple sequence repeats (nSSR) loci primers used for genotyping
Table 6 Climate variables for sampling localities for Quercus aquifolioides. Bio17 precipitation of driest quarter, Bio03 isothermality, Prec12 December precipitation, Wind03 March wind speed
Table 7 Results of tests of the association of symmetric component, asymmetric component and leaf size on the total sample with several individual predictor variables, using the dbRDA multivariate F-statistic. %VAR, percentage of variance explained by each variable; F, F values; ***P < 0.001; **P < 0.01; *P < 0.05
Table 8 Results of Mantel and partial Mantel tests of pairwise relations between genetic distance (FST/(1 − FST)), symmetric component, asymmetric component, and leaf size with geographic and environmental distances, using all samples. ***P < 0.001; **P < 0.01; *P < 0.05
Fig. 5
figure5

Results of generalized Procrustes analysis of the leaf shape of Quercus aquifolioides based on Cartesian x and y coordinates of 13 landmarks (LMs): a using the full raw coordinate matrix; b and c using the separated symmetric and asymmetric components, respectively

Fig. 6
figure6

Results of Principal Component Analysis (PCA) of the symmetric component (a) and asymmetric component (b) of leaves of two Quercus aquifolioides lineages (WSP-HDM and Tibet) and mixed individuals. Scatter plots of PC1 and PC2 scores, with 95% confidence ellipses in a. Transformation grids for the left and right graphs represent shapes corresponding to extreme negative ( −) and positive ( +) PC scores. Symmetric component (a) of PCA formed Tibet and WSP-HDM as distinct groups with some overlap, while the mix group was scattered between the two lineages. Along PC1, the change of leaf shape from subelliptical to suborbicular form was primarily related to the shape of the apical and basal regions and the length of petiole. The variation along PC2 mainly associated with the position of the maximum width of the leaf. For asymmetric component (b), all the specimens overlapped almost completely and the three lineages could not be discriminated, as has already been reported in several previous studies (Viscosi and Cardini 2011; Viscosi 2015; Liu et al. 2018). In detail, the variation along PC1 was mainly the changes in the relative position of the left/right sides at the maximum width of the leaf blade and the differences in the relative sizes of the leaf blade, whereas the variation along PC2 principally focused on the bending direction of the leaf blade toward left or right in asymmetric component

Fig. 7
figure7

Results of discriminant analysis (DA) of the shapes of leaves of the WSP-HDM vs. Tibet lineages (a), mixed individuals vs. Tibet lineage (b), and mixed individuals vs. WSP-HDM lineage (c). Black bars, Tibet lineage; red bars, WSP-HDM lineage; blue bars, mixed individuals

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Li, Y., Zhang, Y., Liao, PC. et al. Genetic, geographic, and climatic factors jointly shape leaf morphology of an alpine oak, Quercus aquifolioides Rehder & E.H. Wilson. Annals of Forest Science 78, 64 (2021). https://doi.org/10.1007/s13595-021-01077-w

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Keywords

  • Allometry
  • Geometric morphometrics
  • Leaf morphological variation
  • Multilocus genotypes
  • Quercus