Evolution of fruit functional traits provides insights into the drivers of cycle-cup oaks (Quercus section Cyclobalanopsis) diversification in evergreen broadleaf forests

doi:10.1016/j.pld.2025.07.004

Plant Diversity ›› 2026, Vol. 48 ›› Issue (04): 655-669.DOI: 10.1016/j.pld.2025.07.004

• Articles • Previous Articles Next Articles

Evolution of fruit functional traits provides insights into the drivers of cycle-cup oaks (Quercus section Cyclobalanopsis) diversification in evergreen broadleaf forests

Liang-Hai Yang^a, Ganesh K. Jaganathan^b, Si-Di Liang^a, Si-Si Zheng^a, Hong-Hu Meng^c, Xi-Qing Sun^a, Xin Ning^a, Ru-Ning Hou^a, Xin Zhong^a, Tian-Rui Wang^a, Bin-Jie Ge^a, Gregor Kozlowski^a,d,e, Yi-Gang Song^a,f

a. Eastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai, China;
b. Germplasm Conservation Laboratory, University of Shanghai for Science and Technology, Shanghai, China;
c. Plant Phylogenetics and Conservation Group, Centre for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming 650223, China;
d. Department of Biology and Botanic Garden, University of Fribourg, Fribourg, Switzerland;
e. Natural History Museum Fribourg, Fribourg, Switzerland;
f. College of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, China

Received:2024-12-27 Revised:2025-07-21 Accepted:2025-07-24 Online:2025-08-05 Published:2026-07-25
Contact: Yi-Gang Song,E-mail:ygsong@cemps.ac.cn
Supported by:
This project was supported by the National Natural Science Foundation of China, China (No. 31901217) and the Special Fund for Scientific Research of Shanghai Landscaping and City Appearance Administrative Bureau, China (grant number G242414, G242415, and G242416). This study was also supported by National Wild Plant Germplasm Resource Center for Chenshan, China. We thank Prof. Si-Chong Chen for giving suggestions for this paper.

Evolution of fruit functional traits provides insights into the drivers of cycle-cup oaks (Quercus section Cyclobalanopsis) diversification in evergreen broadleaf forests

a. Eastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai, China;
b. Germplasm Conservation Laboratory, University of Shanghai for Science and Technology, Shanghai, China;
c. Plant Phylogenetics and Conservation Group, Centre for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming 650223, China;
d. Department of Biology and Botanic Garden, University of Fribourg, Fribourg, Switzerland;
e. Natural History Museum Fribourg, Fribourg, Switzerland;
f. College of Forestry and Biotechnology, Zhejiang A&F University, Hangzhou 311300, China

通讯作者: Yi-Gang Song,E-mail:ygsong@cemps.ac.cn
基金资助:
This project was supported by the National Natural Science Foundation of China, China (No. 31901217) and the Special Fund for Scientific Research of Shanghai Landscaping and City Appearance Administrative Bureau, China (grant number G242414, G242415, and G242416). This study was also supported by National Wild Plant Germplasm Resource Center for Chenshan, China. We thank Prof. Si-Chong Chen for giving suggestions for this paper.

Abstract

Abstract: The impact of key traits on lineage diversity remains a central focus in macroevolutionary research. Seeds, encapsulated within fruits, carry the complete genetic blueprint of their species, and the capacity of their adaptive evolution to diverse environmental conditions shapes species origination and extinction dynamics. However, the role of specific traits in driving species diversification under changing environmental conditions remains poorly understood, particularly among taxa that produce desiccation-sensitive seeds. In this study, we reconstructed the phylogenetic relationships of Quercus section Cyclobalanopsis based on whole-genome resequencing data from 52 species, covering approximately 50% of the section. We investigated six fruit traits—fruit volume, shape, maturation period, cotyledonary petiole, embryonic axis position and dormancy type—through experimental observations and data collection. The influence of these traits, climatic variables, and phylogenetic signal on diversification rates, along with the effects of climatic variables on these traits were analysed. Our findings reveal substantial diversity in fruit trait states within the section Cyclobalanopsis. Climates characterized by hot summers and wet-cold winters provide favorable habitat conditions that promote speciation. Furthermore, ancestral fruit traits, such as small acorns, oblong ellipsoid shapes, normal cotyledonary petioles, and embryonic axes near the apex, along with the derived trait of annual fruit maturation, were associated with increased net diversification rates. These ancestral fruit traits, adapted to the subtropical evergreen broad-leaved forests of East Asia, facilitated rapid evolutionary radiation during the Miocene through climatic niche innovation. In contrast, species inhabiting tropical landscapes appear to adapt to local environmental changes through fruit trait innovations, such as larger fruits and rapid germination.

Key words: Climatic niche, Quercus section Cyclobalanopsis, Diversification rate, Fruit functional traits

摘要： The impact of key traits on lineage diversity remains a central focus in macroevolutionary research. Seeds, encapsulated within fruits, carry the complete genetic blueprint of their species, and the capacity of their adaptive evolution to diverse environmental conditions shapes species origination and extinction dynamics. However, the role of specific traits in driving species diversification under changing environmental conditions remains poorly understood, particularly among taxa that produce desiccation-sensitive seeds. In this study, we reconstructed the phylogenetic relationships of Quercus section Cyclobalanopsis based on whole-genome resequencing data from 52 species, covering approximately 50% of the section. We investigated six fruit traits—fruit volume, shape, maturation period, cotyledonary petiole, embryonic axis position and dormancy type—through experimental observations and data collection. The influence of these traits, climatic variables, and phylogenetic signal on diversification rates, along with the effects of climatic variables on these traits were analysed. Our findings reveal substantial diversity in fruit trait states within the section Cyclobalanopsis. Climates characterized by hot summers and wet-cold winters provide favorable habitat conditions that promote speciation. Furthermore, ancestral fruit traits, such as small acorns, oblong ellipsoid shapes, normal cotyledonary petioles, and embryonic axes near the apex, along with the derived trait of annual fruit maturation, were associated with increased net diversification rates. These ancestral fruit traits, adapted to the subtropical evergreen broad-leaved forests of East Asia, facilitated rapid evolutionary radiation during the Miocene through climatic niche innovation. In contrast, species inhabiting tropical landscapes appear to adapt to local environmental changes through fruit trait innovations, such as larger fruits and rapid germination.

关键词: Climatic niche, Quercus section Cyclobalanopsis, Diversification rate, Fruit functional traits

Liang-Hai Yang, Ganesh K. Jaganathan, Si-Di Liang, Si-Si Zheng, Hong-Hu Meng, Xi-Qing Sun, Xin Ning, Ru-Ning Hou, Xin Zhong, Tian-Rui Wang, Bin-Jie Ge, Gregor Kozlowski, Yi-Gang Song. Evolution of fruit functional traits provides insights into the drivers of cycle-cup oaks (Quercus section Cyclobalanopsis) diversification in evergreen broadleaf forests[J]. Plant Diversity, 2026, 48(04): 655-669.

References

[1] Abels, H.A., Lauretano, V., van Yperen, A.E., et al., 2016. Environmental impact and magnitude of paleosol carbonate carbon isotope excursions marking five Early Eocene hyperthermals in the Bighorn basin, Wyoming. Clim. Past 12, 1151-1163. https://doi.org/10.5194/cp-12-1151-2016.
[2] Ackerly, D., 2009. Conservatism and diversification of plant functional traits: Evolutionary rates versus phylogenetic signal. Proc. Natl. Acad. Sci. U.S.A. 106, 19699-19706. https://doi.org/10.1073/pnas.0901635106.
[3] Alcantara, S., Ree, R.H., Mello-Silva, R., 2018. Accelerated diversification and functional trait evolution in Velloziaceae reveal new insights into the origins of the campos rupestres’ exceptional floristic richness. Ann. Bot. 122, 165-180. https://doi.org/10.1093/aob/mcy063.
[4] Baskin, C.C., Baskin, J.M. 2014. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination, 2nd ed.; Elsevier/Academic Press: San Diego, CA, USA, pp. 41-863.
[5] Baskin, J.M., Baskin, C.C., 2021. The great diversity in kinds of seed dormancy: A revision of the Nikolaeva-Baskin classification system for primary seed dormancy. Seed Sci. Res. 31, 249-277. https://doi.org/10.1017/S096025852100026X.
[6] Beaulieu, J.M., O’Meara, B.C., 2016. Detecting hidden diversification shifts in models of trait-dependent speciation and extinction. Syst. Biol. 65, 583-601. https://doi.org/10.1093/sysbio/syw022.
[7] Berjak, P., Pammenter, N.W., 2008. From Avicennia to Zizania: Seed recalcitrance in perspective. Ann. Bot. 101, 213-228. https://doi.org/10.1093/aob/mcm168.
[8] Blomberg, S.P., Garland, T., Ives, A.R., 2003. Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57, 717-745. https://doi.org/10.1111/j.0014-3820.2003.tb00285.x.
[9] Bollback, J.P., 2006. SIMMAP: Stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7, 88. https://doi.org/10.1186/1471-2105-7-88.
[10] Cadotte, M., Albert, C.H., Walker, S.C., 2013. The ecology of differences: Assessing community assembly with trait and evolutionary distances. Ecol. Lett. 16, 1234-1244. https://doi.org/10.1111/ele.12161.
[11] Carrero, C., Jerome, D., Beckman, E., et al., 2020. The Red List of Oaks. The Morton Arboretum: Lisle, IL, USA.
[12] CFH, 2024. Chinese Field Herbarium. URL http://www.cfh.ac.cn/ (Accessed 20 March 2024)
[13] Chen, S., 2023. Ultrafast one-pass FASTQ data preprocessing, quality control, and deduplication using fastp. iMeta 2, e107. https://doi.org/10.1002/imt2.107.
[14] Choi, E.J., Yong, S.H., Park, D.J., et al., 2022. Germination and growth characteristics of Quercus myrsinifolia Blume seedlings according to seed coat removal, type of potting soil and irrigation cycle. Forests 13, 938. https://doi.org/10.3390/f13060938.
[15] Coelho, M.T.P., Barreto, E., Rangel, T.F., et al., 2023. The geography of climate and the global patterns of species diversity. Nature 622, 537-544. https://doi.org/10.1038/s41586-023-06577-5.
[16] Cortes-Flores, C.J., Cornejo-Tenorio G., Urrea-Galean, L.A., et al., 2019. Phylogeny, fruit traits, and ecological correlates of fruiting phenology in a Neotropical dry forest. Oecologia 189, 159-169. https://doi.org/10.1007/s00442-018-4295-z.
[17] Crisp, M.D., Arroyo, M.T.K., Cook, L.G., et al., 2009. Phylogenetic biome conservatism on a global scale. Nature 458, 754-756. https://doi.org/10.1038/nature07764.
[18] CVH, 2024. Chinese Virtual Herbarium. URL http://www.cvh.ac.cn/ (Accessed 20 March 2024)
[19] Dalling, J.W., Davis, A.S., Schutte, B.J., et al., 2011. Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. J. Ecol. 99, 89-95. https://doi.org/10.1111/j.1365-2745.2010.01739.x.
[20] Danecek, P., Auton, A., Abecasis, G., et al., 2011. The variant call format and VCFtools. Bioinformatics 27, 2156-2158. https://doi.org/10.1093/bioinformatics/btr330.
[21] Danecek, P., Bonfield, J.K., Liddle, J., et al., 2021. Twelve years of SAMtools and BCFtools. GigaScience 10, giab008. https://doi.org/10.1093/gigascience/giab008.
[22] Deng, M., Jiang, X.L., Hipp, A.L., et al., 2018. Phylogeny and biogeography of East Asian evergreen oaks (Quercus section Cyclobalanopsis; Fagaceae): Insights into the Cenozoic history of evergreen broad-leaved forests in subtropical Asia. Mol. Phylogenet. Evol. 119, 170-181. https://doi.org/10.1016/j.ympev.2017.11.003.
[23] Denk, T., Grimm, G.W., Manos, P.S., et al., 2017. An updated infrageneric classification of the oaks: review of previous taxonomic schemes and synthesis of evolutionary patterns. In: Gil-Pelegrin, E., Peguero-Pina, J.J., Sancho- Knapik, D. (Eds.), Oaks Physiological Ecology. Exploring the Functional Diversity of Genus Quercus L., Tree Physiology. Springer, Cham, Switzerland, pp. 13-38.
[24] Diaz, S., Kattge, J., Cornelissen, J.H.C., et al., 2016. The global spectrum of plant form and function. Nature 529, 167-171. https://doi.org/10.1038/nature16489.
[25] Dickie, J.B., Pritchard, H.W., 2002. Systematic and evolutionary aspects of desiccation tolerance in seeds. In desiccation and survival in plants: Drying without dying. Wallingford UK: CABI, pp. 239-259.
[26] Donoghue, M.J., 2008. A phylogenetic perspective on the distribution of plant diversity. Proc. Natl. Acad. Sci. U.S.A. 105, 11549-11555. https://doi.org/10.1073/pnas.0801962105.
[27] Donohue, K., Dorn, L., Griffith, C., et al., 2005. Niche construction through germination cueing: Life-history responses to timing of germination in Arabidopsis thaliana. Evolution 59, 771-785. https://doi.org/10.1111/j.0014-3820.2005.tb01752.x.
[28] Donohue, K., Rubio De Casas, R., Burghardt, L., et al., 2010. Germination, post germination adaptation, and species ecological ranges. Annu. Rev. Ecol. Evol. Syst. 41, 293-319. https://doi.org/10.1146/annurev-ecolsys-102209-144715.
[29] Doyle, J.J., Doyle, J.L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11-15.
[30] Eriksson, O., Friis, E.M., Lofgren, P., 2000. Seed size, fruit size, and dispersal systems in angiosperms from the early cretaceous to the late tertiary. Am. Nat. 156, 47-58. https://doi.org/10.1086/303367.
[31] Fazan, L., Song, Y.G., Kozlowski, G., 2020. The woody planet: From past triumph to manmade decline. Plants 9, 1593. https://doi.org/10.3390/plants9111593.
[32] Farnsworth, E., 2000. The ecology and physiology of viviparous and recalcitrant seeds. Annu. Rev. Ecol. Syst. 31, 107-138. https://doi.org/10.1146/annurev.ecolsys.31.1.107.
[33] Fenner, M., and K. Thompson. 2005. The ecology of seeds. Cambridge Univ Press, Cambridge, UK.
[34] Fick, S.E., Hijmans, R.J., 2017. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302-4315. https://doi.org/10.1002/joc.5086.
[35] Finch-Savage, W.E., Leubner-Metzger, G., 2006. Seed dormancy and the control of germination. New Phytol. 171, 501-523. https://doi.org/10.1111/j.1469-8137.2006.01787.x.
[36] FitzJohn, R.G., 2012. Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3, 1084-1092. https://doi.org/10.1111/j.2041-210X.2012.00234.x.
[37] Flaishman, M.A., Peles, Y., Dahan, Y., et al., 2015. Differential response of cell-cycle and cell-expansion regulators to heat stress in apple (Malus domestica) fruitlets. Plant Sci. 233, 82-94. https://doi.org/10.1016/j.plantsci.2015.01.005.
[38] Galetti, M., Guevara, R., Cortes, M.C., et al., 2013. Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340, 1086-1090. https://doi.org/10.1126/science.1233774.
[39] Gamisch, A., 2016. Notes on the statistical power of the binary state speciation and extinction (BiSSE) model. Evol. Bioinform. 12, 165-174. https://doi.org/10.4137/EBO.S39732.
[40] GBIF, 2024. GBIF Home Page. URL https://www.gbif.org (Accessed 20 March 2024)
[41] Geritz, S.A.H., 1998. Co-evolution of seed size and seed predation. Evol. Ecol. 12, 891-911.
[42] Gugger, P.F., Cavender-Bares, J., 2013. Molecular and morphological support for a Florida origin of the Cuban oak. J. Biogeogr. 40, 632-645. https://doi.org/10.1111/j.1365-2699.2011.02610.x.
[43] Han, T., Zheng, Q., Onstein, R.E., et al., 2020. Polyploidy promotes species diversification of Allium through ecological shifts. New Phytol. 225, 571-583. https://doi.org/10.1111/nph.16098.
[44] Hipp, A.L., Manos, P.S., Hahn, M., et al., 2020. Genomic landscape of the global oak phylogeny. New Phytol. 226, 1198-1212. https://doi.org/10.1111/nph.16162.
[45] Hirayama, D., Okada, M., Nanami, S., et al., 2019. Correlation between the shoot-cutting behavior of the acorn weevil and the reproductive traits of host fagaceous trees. Plant. Spec. Biol. 34, 184-191. https://doi.org/10.1111/1442-1984.12246.
[46] Hohna, S., Landis, M.J., Heath, T.A., et al., 2016. RevBayes: Bayesian phylogenetic inference using graphical models and an interactive model-specification language. Syst. Biol. 65, 726-736. https://doi.org/10.1093/sysbio/syw021.
[47] Huang, C., Zhang, Y., Bartholomew, B., 1999. Fagaceae. In: Wu, Z.Y., Raven, P.H., Hong, D.Y. (Eds.), Flora of China, vol. 4. Missouri Botanical Garden Press & Science Press, St. Louis & Beijing, pp. 380–400.
[48] Jaganathan, G.K., Phartyal, S.S., 2024. A classification system for germination in desiccation-sensitive Fagaceae acorns: with particular focus on physiological and epicotyl dormancy. Bot. J. Linn. Soc. 207, 197-207. https://doi.org/10.1093/botlinnean/boae049.
[49] Jaganathan, G.K., Canelo, T., Phartyal, S.S., et al., 2024. The reproductive biology of Fagaceae acorns in the current and future climate. Flora 315, 152504. https://doi.org/10.1016/j.flora.2024.152504.
[50] Jaganathan, G.K., 2021. Ecological insights into the coexistence of dormancy and desiccation-sensitivity in Arecaceae species. Ann. For. Sci. 78, 10. https://doi.org/10.1007/s13595-021-01032-9.
[51] Jansen, P.A., Bongers, F., Prins, H.H.T., 2006. Tropical rodents change rapidly germinating seeds into long-term food supplies. Oikos 113, 449-458. https://doi.org/10.1111/j.2006.0030-1299.14461.x.
[52] Jin, D., Yuan, Q., Dai, X., et al., 2024. Enhanced precipitation has driven the evolution of subtropical evergreen broad-leaved forests in eastern China since the early Miocene: Evidence from ring-cupped oaks. J. Syst. Evol. 62, 677-686. https://doi.org/10.1111/jse.13022.
[53] Kang, H., Jaganathan, G.K., Han, Y., et al., 2023. Revisiting the pericarp as a barrier restricting water entry/loss from cotyledons and embryonic axis of temperate desiccation-sensitive Quercus acorns. Planta 257, 33. https://doi.org/10.1007/s00425-022-04061-4.
[54] Kassambara, A., Mundt, F., 2016. factoextra: Extract and visualize the results of multivariate data analyses. URL https://CRAN.R-project.org/package=factoextra (accessed March.20.2024).
[55] Kempel, A., Chrobock, T., Fischer, M., et al., 2013. Determinants of plant establishment success in a multispecies introduction experiment with native and alien species. Proc. Natl. Acad. Sci. U.S.A. 110, 12727-12732. https://doi.org/10.1073/pnas.1300481110.
[56] Kim, M.H., Park, D.H., Bae, M.S., et al., 2018. Analysis of the active constituents and evaluation of the biological effects of Quercus acuta Thunb. (Fagaceae) extracts. Molecules 23, 1772. https://doi.org/10.3390/molecules23071772.
[57] Kolde, R., 2010. pheatmap: Pretty heatmaps. URL https://CRAN.R-project.org/package=pheatmap (accessed March.20.2024).
[58] Kraft, T.S., Wright, S.J., Turner, I., et al., 2015. Seed size and the evolution of leaf defences. J. Ecol. 103, 1057-1068. https://doi.org/10.1111/1365-2745.12407.
[59] Lei, J., Shen, Z., Yi, X., 2012. Pericarp thickness and seed size determine acorn dispersal of five rodent-dispersed oak species. Acta Theriologica Sinica 32, 83-89.
[60] Le, S., Josse, J., Husson, F., 2008. FactoMineR: An R package for multivariate analysis. J. Stat. Soft. 25. https://doi.org/10.18637/jss.v025.i01.
[61] Li, H., Durbin, R., 2009. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25, 1754-1760. https://doi.org/10.1093/bioinformatics/btp324.
[62] Li, Y., Zheng, S., Wang, T., et al., 2024. New insights on the phylogeny, evolutionary history, and ecological adaptation mechanism in cycle-cup oaks based on chloroplast genomes. Ecol. Evol. 14, e70318. https://doi.org/10.1002/ece3.70318.
[63] Li, J., Jaganathan, G.K., Kang, H., et al., 2023. The co-occurrence of physiological and epicotyl physiological dormancy in three desiccation-sensitive Castanopsis (Fagaceae) acorns from China with specific reference to the embryonic axis position. Forests 14, 2330. https://doi.org/10.3390/f14122330.
[64] Li, M., Wu, J.J., Su, R.P., et al., 2025. Genome analyses provide insights into Engelhardia’s adaptation to East Asia Summer Monsoon. Plant Divers. https://doi.org/10.1016/j.pld.2025.07.003.
[65] Li, Q., Zhang, J., Coombes, A., 2016. Quercus lineata (Fagaceae): new distribution records from China and Vietnam and its leaf anatomical features. Phytotaxa 266, 226. https://doi.org/10.11646/phytotaxa.266.3.7.
[66] Linkies, A., Graeber, K., Knight, C., et al., 2010. The evolution of seeds. New Phytol. 186, 817-831. https://doi.org/10.1111/j.1469-8137.2010.03249.x.
[67] Liu, H., Yin, D., He, P., et al., 2024a. Linking plant functional traits to biodiversity under environmental change. Biol. Divers. 1, 22-28. https://doi.org/10.1002/bod2.12004.
[68] Liu, K., Li, E., Cui, X., et al., 2024b. Key innovations and niche variation promoted rapid diversification of the widespread Juniperus (Cupressaceae). Commun. Biol. 7, 1002. https://doi.org/10.1038/s42003-024-06687-4.
[69] Lord, J.M., 2004. Frugivore gape size and the evolution of fruit size and shape in southern hemisphere floras. Austral Ecol 29, 430–436. doi:10.1111/j.1442-9993.2004.01382.x.
[70] Ma, R., Xu, Q., Gao, Y., et al., 2024. Patterns and drivers of plant sexual systems in the dry-hot valley region of southwestern China. Plant Divers. 46, 158-168. https://doi.org/10.1016/j.pld.2023.07.010.
[71] Maddison, W.P., FitzJohn, R.G., 2015. The unsolved challenge to phylogenetic correlation tests for categorical characters. Syst. Biol. 64, 127-136. https://doi.org/10.1093/sysbio/syu070.
[72] Maddison, W.P., Midford, P.E., Otto, S.P., 2007. Estimating a binary character’s effect on speciation and extinction. Syst. Biol. 56, 701-710. https://doi.org/10.1080/10635150701607033.
[73] Meijer, N., Licht, A., Woutersen, A., et al., 2024. Proto-monsoon rainfall and greening in central Asia due to extreme Early Eocene warmth. Nat. Geosci. 17, 158-164. https://doi.org/10.1038/s41561-023-01371-4.
[74] Mendoza, I., Perez, C.A., Morellato, L.P.C., 2017. Continental-scale patterns and climatic drivers of fruiting phenology: a quantitative neotropical review. Global Planet. Change 148, 227-241. https://doi.org/10.1016/j.gloplacha.2016.12.001.
[75] Meng, H., Song, G., Hu, X., et al., 2025. Evolution of East Asian subtropical evergreen broad-leaved forests: When and how? J. Syst. Evol. https://doi.org/10.1111/jse.70001.
[76] Mitchell, N., Moore, T.E., Mollmann, H.K., et al., 2015. Functional traits in parallel evolutionary radiations and trait-environment associations in the cape floristic region of South Africa. Am. Nat. 185, 525-537. https://doi.org/10.1086/680051.
[77] Onstein, R.E., Jordan, G.J., Sauquet, H., et al., 2016. Evolutionary radiations of Proteaceae are triggered by the interaction between traits and climates in open habitats. Glob. Ecol. Biogeogr. 25, 1239-1251. https://doi.org/10.1111/geb.12481.
[78] Orme, D., Rob, F., Gavin, T., et al., 2018. The caper package: comparative analysis of phylogenetics and evolution in R. Caper Package Comp. Anal. Phylogenetics Evol. R. URL https://CRAN.R-project.org/package=caper.
[79] Pagel, M., 1999. Inferring the historical patterns of biological evolution. Nature 401, 877-884. https://doi.org/10.1038/44766.
[80] Parolin, P., 2000. Seed mass in Amazonian floodplain forests with contrasting nutrient supplies. J. Trop. Ecol. 16, 417-428. https://doi.org/10.1017/S0266467400001486.
[81] Peres-Neto, P.R., Leibold, M.A., Dray, S., 2012. Assessing the effects of spatial contingency and environmental filtering on metacommunity phylogenetics. Ecology 93, S14-S30. https://doi.org/10.1890/11-0494.1.
[82] Pritchard, H.W., Sershen, Tsan, F.Y., Wen, B., et al., 2022. Regeneration in recalcitrant-seeded species and risks from climate change, In: Carol, C. Baskin., Jerry, M. Baskin. (Eds.), Plant regeneration from seeds. Elsevier, pp. 259-273. https://doi.org/10.1016/B978-0-12-823731-1.00014-7.
[83] Poschlod, P., Abedi, M., Bartelheimer, M., et al., 2013. Seed ecology and assembly rules in plant communities. In: Van Der Maarel, E., Franklin, J. (Eds.), Vegetation Ecology. Wiley, pp. 164-202. https://doi.org/10.1002/9781118452592.ch6.
[84] Rabosky, D.L., Goldberg, E.E., 2015. Model inadequacy and mistaken inferences of trait-dependent speciation. Syst. Biol. 64, 340-355. https://doi.org/10.1093/sysbio/syu131.
[85] Rambaut, A., Drummond, A.J., Xie, D., et al., 2018. Posterior summarization in bayesian phylogenetics using tracer 1.7. Syst. Biol. 67, 901-904. https://doi.org/10.1093/sysbio/syy032.
[86] Read, Q.D., Moorhead, L.C., Swenson, N.G., et al., 2014. Convergent effects of elevation on functional leaf traits within and among species. Funct. Ecol. 28, 37-45. https://doi.org/10.1111/1365-2435.12162.
[87] Revell, L.J., 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223. https://doi.org/10.1111/j.2041-210X.2011.00169.x.
[88] Roberts, E., 1973. Predicting the storage life of seeds. Seed Sci. Technol. 13, 499-514.
[89] Rodriguez, A., Sanchez, E., De La Casa, A., 2011. Contributions of early season temperatures to Pyrus Communis “Bartlett” fruit growth. Acta Hortic. 909, 657-664. https://doi.org/10.17660/ActaHortic.2011.909.80.
[90] Saatkamp, A., Cochrane, A., Commander, L., et al., 2019. A research agenda for seed-trait functional ecology. New Phytol. 221, 1764-1775. https://doi.org/10.1111/nph.15502.
[91] Seidler, T.G., Plotkin, J.B., 2006. Seed dispersal and spatial pattern in tropical trees. PLoS Biology 4, e344. https://doi.org/10.1371/journal.pbio.0040344.
[92] Serit, M., Okubo, T., Su, R.H., et al., 1991. Antibacterial compounds from oak, Quercus acuta Thunb. Agric. Biol. Chem. 55, 19-23. https://doi.org/10.1271/bbb1961.55.19.
[93] Sobrino-Vesperinas, E., Viviani, A.B., 2000. Pericarp micromorphology and dehydration characteristics of Quercus suber L. acorns. Seed Sci. Res. 10, 401-407. https://doi.org/10.1017/S0960258500000441.
[94] Song, Y.G., Petitpierre, B., Deng, M., et al., 2019. Predicting climate change impacts on the threatened Quercus arbutifolia in montane cloud forests in southern China and Vietnam: Conservation implications. For. Ecol. Manag. 444, 269-279. https://doi.org/10.1016/j.foreco.2019.04.028.
[95] Soumoy, L., Thiebaut, B., Serey, I.,1996. The growth of Japanese Fagaceae-Germination, architectural model and systematic status. Can. J. Bot. 74, 1248-1259.
[96] Spicer, R.A., 2017. Tibet, the Himalaya, Asian monsoons and biodiversity-In what ways are they related? Plant Divers. 39, 233-244. https://doi.org/10.1016/j.pld.2017.09.001.
[97] Sternberg, D., Kennard, M.J., 2014. Phylogenetic effects on functional traits and life history strategies of Australian freshwater fish. Ecography 37, 54-64. https://doi.org/10.1111/j.1600-0587.2013.00362.x.
[98] Sun, X.Q., Song, Y.G., Ge, B.J., et al., 2021. Intermediate epicotyl physiological dormancy in the recalcitrant seed of Quercus chungii F.P. Metcalf with the elongated cotyledonary petiole. Forests 12, 263. https://doi.org/10.3390/f12030263.
[99] Tribble, C.M., Freyman, W.A., Landis, M.J., et al., 2022. RevGadgets: An R package for visualizing bayesian phylogenetic analyses from RevBayes. Methods Ecol. Evol. 13, 314-323. https://doi.org/10.1111/2041-210X.13750.
[100] Tucker, C.M., Davies, T.J., Cadotte, M.W., et al., 2018. On the relationship between phylogenetic diversity and trait diversity. Ecology 99, 1473-1479. https://doi.org/10.1002/ecy.2349.
[101] Wang, T.R., Ning, X., Zheng, S.S., et al., 2024. Genomic insights into ecological adaptation of oaks revealed by phylogenomic analysis of multiple species. Plant Divers. 47, 53-67. https://doi.org/10.1016/j.pld.2024.07.008.
[102] Wang, L., Schneider, H., Zhang, X.C., et al., 2012. The rise of the Himalaya enforced the diversification of SE Asian ferns by altering the monsoon regimes. BMC Plant Biol. 12, 210. https://doi.org/10.1186/1471-2229-12-210.
[103] Wang, S., Liao, Z., Cao, P., et al., 2025. General-purpose genotypes and evolution of higher plasticity in clonality underlie knotweed invasion. New Phytol. 246, 758-768. https://doi.org/10.1111/nph.20452.
[104] Wang, Y., Wang, J., Lai, L., et al., 2014. Geographic variation in seed traits within and among forty-two species of Rhododendron (Ericaceae) on the Tibetan plateau: relationships with altitude, habitat, plant height, and phylogeny. Ecol. Evol. 4, 1913-1923. https://doi.org/10.1002/ece3.1067.
[105] Welch, R.M., 2024. Importance of seed mineral nutrient reserves in crop growth and development. In: Rengel Z. (editor), Mineral nutrition of crops. CRC Press, pp. 205-226.
[106] Westerhold, T., Marwan, N., Drury, A.J., et al., 2020. An astronomically dated record of earth’s climate and its predictability over the last 66 million years. Science 369, 1383-1387. https://doi.org/10.1126/science.aba6853.
[107] Wiens, J.J., Donoghue, M.J., 2004. Historical biogeography, ecology and species richness. Trends Ecol. Evol. 19, 639-644. https://doi.org/10.1016/j.tree.2004.09.011.
[108] Willis, C.G., Baskin, C.C., Baskin, J.M., et al., 2014. The evolution of seed dormancy: environmental cues, evolutionary hubs, and diversification of the seed plants. New Phytol. 203, 300-309. https://doi.org/10.1111/nph.12782.
[109] Wyse, S.V., Dickie, J.B., 2017. Predicting the global incidence of seed desiccation sensitivity. J. Ecol. 105, 1082-1093. https://doi.org/10.1111/1365-2745.12725.
[110] Xia, K., Daws, M.I., Zhu, Z.Q., 2025. Climate drives patterns of response of recalcitrant embryonic axes of Quercus species to cryopreservation. Plant Divers. https://doi.org/10.1016/j.pld.2025.04.004.
[111] Xia, K., Daws, M.I., Peng, L., 2022. Climate drives patterns of seed traits in Quercus species across China. New Phytol. 234, 1629-1638. https://doi.org/10.1111/nph.18103.
[112] Xia, K., Fan, L., Sun, W., et al., 2016. Conservation and fruit biology of Sichou oak (Quercus sichourensis, Fagaceae) - A critically endangered species in China. Plant Divers. 38, 233-237. https://doi.org/10.1016/j.pld.2016.07.001.
[113] Xia, K., Daws, M.I., Zhou, Z.K., et al., 2015. Habitat-linked temperature requirements for fruit germination in Quercus species: A comparative study of Quercus subgenus Cyclobalanopsis (Asian evergreen oaks) and Quercus subgenus Quercus. S. Afr. J. Bot. 100, 108-113. https://doi.org/10.1016/j.sajb.2015.04.015.
[114] Xia, K., Daws, M.I., Stuppy, W., et al., 2012. Rates of water loss and uptake in recalcitrant fruits of Quercus species are determined by pericarp anatomy. PLoS ONE 7, e47368. https://doi.org/10.1371/journal.pone.0047368.
[115] Xu, J., Song, Y.G., Deng, M., et al., 2020. Seed germination schedule and environmental context shaped the population genetic structure of subtropical evergreen oaks on the Yun-Gui Plateau, Southwest China. Heredity 124, 499-513. https://doi.org/10.1038/s41437-019-0283-2.
[116] Xue, B., Guo, X., Landis, J.B., et al., 2020. Accelerated diversification correlated with functional traits shapes extant diversity of the early divergent angiosperm family Annonaceae. Mol. Phylogenet. Evol. 142, 106659. https://doi.org/10.1016/j.ympev.2019.106659.
[117] Yadav, Shubham., Korat, J.R., Yadav, Sanjeev., et al., 2023. Impacts of climate change on fruit crops: A comprehensive review of physiological, phenological, and pest-related responses. IJECC 13, 363-371. https://doi.org/10.9734/ijecc/2023/v13i113179.
[118] Yang, Z., 2007. PAML 4: Phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591. https://doi.org/10.1093/molbev/msm088.
[119] Yi, X., Curtis, R., Bartlow, A.W., et al., 2013. Ability of chestnut oak to tolerate acorn pruning by rodents: The role of the cotyledonary petiole. Naturwissenschaften 100, 81-90. https://doi.org/10.1007/s00114-012-0996-z.
[120] You, Y., Yu, J., Nie, Z., et al., 2024. Transition of survival strategies under global climate shifts in the grape family. Nat. Plants 10, 1100-1111. https://doi.org/10.1038/s41477-024-01726-8.
[121] Yu, X., Du, C., Wang, X., et al., 2024. Multivariate analysis between environmental factors and fruit quality of citrus at the core navel orange-producing area in China. Front. Plant Sci. 15, 1510827. https://doi.org/10.3389/fpls.2024.1510827.
[122] Zhang, C., Rabiee, M., Sayyari, E., Mirarab, S., 2018. ASTRAL-III: Polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19, 153. https://doi.org/10.1186/s12859-018-2129-y.
[123] Zhang, C., Gu, R., Lin, L., et al., 2024a. Functional traits and ecological niches as correlates of the interspecific growth-mortality trade-off among seedlings of 14 tropical tree species. Funct. Ecol. 38, 1888-1901. https://doi.org/10.1111/1365-2435.14624.
[124] Zhang, Q., Yang, Y.C., Liu, B., et al., 2024b. Meta-analysis provides insights into the origin and evolution of East Asian evergreen broad-leaved forests. New Phytol. 242, 2369-2379.
[125] Zhang, X., Landis, J.B., Sun, Y., et al., 2021. Macroevolutionary pattern of Saussurea (Asteraceae) provides insights into the drivers of radiating diversification. Proc. R. Soc. B-Biol. Sci. 288, 20211575. https://doi.org/10.1098/rspb.2021.1575.
[126] Zhao, J., Li, S., Huang, J., et al., 2025. Heterogeneous occurrence of evergreen broad-leaved forests in East Asia: Evidence from plant fossils. Plant Divers. 47, 1-12. https://doi.org/10.1016/j.pld.2024.07.004.
[127] Zhao, L., Yang, Y.Y., Qu, X.J., et al., 2023. Phylotranscriptomic analyses reveal multiple whole-genome duplication events, the history of diversification and adaptations in the Araceae. Ann. Bot. 131, 199-214. https://doi.org/10.1093/aob/mcac062.
[128] Zhong, J., Jin, X., Orr, M.C., et al., 2025. The ethics of theft: Reevaluating the impacts of floral larceny on plant reproductive success. Plant Divers. 47, 148-158. https://doi.org/10.1016/j.pld.2024.12.004.

Evolution of fruit functional traits provides insights into the drivers of cycle-cup oaks (Quercus section Cyclobalanopsis) diversification in evergreen broadleaf forests

Evolution of fruit functional traits provides insights into the drivers of cycle-cup oaks (Quercus section Cyclobalanopsis) diversification in evergreen broadleaf forests

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 3

Recommended Articles

Metrics

Comments

[1]	Tao Zhou, Xiaodan Chen, Jordi López-Pujol, Guoqing Bai, Sonia Herrando-Moraira, Neus Nualart, Xiao Zhang, Yuemei Zhao, Guifang Zhao. Genetically-and environmentally-dependent processes drive interspecific and intraspecific divergence in the Chinese relict endemic genus Dipteronia [J]. Plant Diversity, 2024, 46(05): 585-599.
[2]	Xiao-Yan Liu, Han-Zhang Song, Xin-Kai Wu, Jia-Rong Hu, Wei-Ye Huang, Cheng Quan, Jian-Hua Jin. Late Oligocene fossil acorns and nuts of Quercus section Cyclobalanopsis from the Nanning Basin, Guangxi, South China [J]. Plant Diversity, 2023, 45(04): 434-445.
[3]	Han-Yang Lin, Miao Sun, Ya-Jun Hao, Daijiang Li, Matthew A. Gitzendanner, Cheng-Xin Fu, Douglas E. Soltis, Pamela S. Soltis, Yun-Peng Zhao. Phylogenetic diversity of eastern Asia-eastern North America disjunct plants is mainly associated with divergence time [J]. Plant Diversity, 2023, 45(01): 27-35.