Species evolution determines epiphyte evolution in Orchids

doi:10.1016/j.pld.2026.01.005

Plant Diversity ›› 2026, Vol. 48 ›› Issue (02): 422-428.DOI: 10.1016/j.pld.2026.01.005

Previous Articles Next Articles

Species evolution determines epiphyte evolution in Orchids

Tianwen Zhang^a,b, Jun-Wen Zhai^a, Gang Wang^b,c

a. Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization at College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350000, Fujian, China;
b. Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China;
c. State Key Laboratory of Plant Diversity and Specialty Crops, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China

Received:2025-09-01 Revised:2026-01-18 Online:2026-05-19 Published:2026-03-25
Contact: Jun-Wen Zhai,E-mail:zhai-jw@163.com;Gang Wang,E-mail:wanggang@xtbg.org.cn
Supported by:
We would like to thank Yanbao Ma and Ying Feng for their contributions to improving the clarity and quality of the manuscript. This work was supported by the Yunnan Revitalization Talent Support Program (XDYC-QNRC-20230573), the National Natural Science Foundation of China grant (32371701), the 14th Five-Year Plan of the Xishuangbanna Tropical Botanical Garden, CAS (E3ZKFF3B), Xizang Yarlung Zangbu Grand Canyon National Nature Reserve expenditure project of forestry and grassland ecological protection and restoration funding (GZFCG2023-14256), and construction and management of the research center for the protection and utilization of orchids in Motuo, Xizang Autonomous Region, China (KH230350A).

Species evolution determines epiphyte evolution in Orchids

Tianwen Zhang^a,b, Jun-Wen Zhai^a, Gang Wang^b,c

a. Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization at College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350000, Fujian, China;
b. Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China;
c. State Key Laboratory of Plant Diversity and Specialty Crops, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, Yunnan, China

通讯作者: Jun-Wen Zhai,E-mail:zhai-jw@163.com;Gang Wang,E-mail:wanggang@xtbg.org.cn
基金资助:
We would like to thank Yanbao Ma and Ying Feng for their contributions to improving the clarity and quality of the manuscript. This work was supported by the Yunnan Revitalization Talent Support Program (XDYC-QNRC-20230573), the National Natural Science Foundation of China grant (32371701), the 14th Five-Year Plan of the Xishuangbanna Tropical Botanical Garden, CAS (E3ZKFF3B), Xizang Yarlung Zangbu Grand Canyon National Nature Reserve expenditure project of forestry and grassland ecological protection and restoration funding (GZFCG2023-14256), and construction and management of the research center for the protection and utilization of orchids in Motuo, Xizang Autonomous Region, China (KH230350A).

Abstract

Abstract: Orchid diversity and conservation are tightly linked to the evolution of orchid lifeforms (e.g., epiphytic or terrestrial) as epiphytic species are highly sensitive to environmental changes and includes super-high species diversity. However, the factors that drive the evolution of orchid lifeform remain unclear. Here, we used a global orchid phylogeny (2272 species, all five subfamilies and 302 genera) to evaluate the relative contributions of potential factors (i.e., phylogeny, climate region, pollination traits) that may drive orchid lifeform evolution using partial framework. Conventional correlation results indicated that orchid lifeforms are strongly associated with climate regions and weakly related to pollination traits. In contrast, partial analyses revealed that orchid phylogeny alone accounted for 62% of lifeform variation; pollinator attraction strategies independently explained an additional 23.9% variation, while climate region only further explained 3.4%. The discrepancies arise from variation in phylogenetic conservatism of different orchid traits: both orchid lifeform and climate region are more phylogenetically conserved than pollination traits. Specifically, our findings that species evolution plays a key role in lifeform evolution together with variation in phylogenetic conservatism among key traits provide insights into trait evolution and species conservation in orchids.

Key words: trait evolution, partial R², epiphytic orchids, phylogenetic conservatism, orchid conservation

摘要： Orchid diversity and conservation are tightly linked to the evolution of orchid lifeforms (e.g., epiphytic or terrestrial) as epiphytic species are highly sensitive to environmental changes and includes super-high species diversity. However, the factors that drive the evolution of orchid lifeform remain unclear. Here, we used a global orchid phylogeny (2272 species, all five subfamilies and 302 genera) to evaluate the relative contributions of potential factors (i.e., phylogeny, climate region, pollination traits) that may drive orchid lifeform evolution using partial framework. Conventional correlation results indicated that orchid lifeforms are strongly associated with climate regions and weakly related to pollination traits. In contrast, partial analyses revealed that orchid phylogeny alone accounted for 62% of lifeform variation; pollinator attraction strategies independently explained an additional 23.9% variation, while climate region only further explained 3.4%. The discrepancies arise from variation in phylogenetic conservatism of different orchid traits: both orchid lifeform and climate region are more phylogenetically conserved than pollination traits. Specifically, our findings that species evolution plays a key role in lifeform evolution together with variation in phylogenetic conservatism among key traits provide insights into trait evolution and species conservation in orchids.

关键词: trait evolution, partial R², epiphytic orchids, phylogenetic conservatism, orchid conservation

Tianwen Zhang, Jun-Wen Zhai, Gang Wang. Species evolution determines epiphyte evolution in Orchids[J]. Plant Diversity, 2026, 48(02): 422-428.

References

[1] Ackerly, D.D., 2009. Conservatism and diversification of plant functional traits: evolutionary rates versus phylogenetic signal. Proc. Natl. Acad. Sci. U.S.A. 106, 19699-19706.
[2] Ackerly, D.D., Dudley, S.A., Sultan, S.E., et al., 2000. The evolution of plant ecophysiological traits: recent advances and future directions. BioScience 50, 979-995.
[3] Ackerman, J.D., Phillips, R.D., Tremblay, R.L., et al., 2023. Beyond the various contrivances by which orchids are pollinated: global patterns in orchid pollination biology. Bot. J. Linn. Soc. 202, 295-324.
[4] Adams, D.C., Collyer, M.L., 2018. Phylogenetic ANOVA: group-clade aggregation, biological challenges, and a refined permutation procedure. Evolution 72, 1204-1215.
[5] Aguiar, J.M.R.B.V., Pansarin, L.M., Ackerman, J.D., et al., 2012. Biotic versus abiotic pollination in Oeceoclades maculata (Lindl.) Lindl. (Orchidaceae). Plant Species Biol. 27, 86-95.
[6] Boyko, J.D., Beaulieu, J.M., 2021. Generalized hidden Markov models for phylogenetic comparative datasets. Methods Ecol. Evol. 12, 468-478.
[7] Broennimann, O., Treier, U.A., Muller-Scharer, H., et al., 2007. Evidence of climatic niche shift during biological invasion. Ecol. Lett. 10, 701-709.
[8] Bruijnzeel, L.A., Scatena, F.N., Hamilton, L.S., et al., 2011. Tropical montane cloud forests: science for conservation and management. Cambridge University Press, Cambridge.
[9] Carmona-Higuita, M.J., Mendieta-Leiva, G., Gomez-Diaz, J.A., et al., 2024. Conservation status of vascular epiphytes in the Neotropics. Biodivers. Conserv. 33, 51-71.
[10] Chase, M.W., Cameron, K.M., Freudenstein, J.V., et al., 2015. An updated classification of Orchidaceae. Bot. J. Linn. Soc. 177, 151-174.
[11] Chen, X., Wei, L., 2003. A comparison of recent methods for the analysis of small-sample cross-over studies. Stat. Med. 22, 2821-2833.
[12] Collobert, G., Perez-Lamarque, B., Dubuisson, J.-Y., et al., 2023. Gains and losses of the epiphytic lifestyle in epidendroid orchids: review and new analyses of succulence traits. Ann. Bot. 132, 787-800.
[13] Cooper, N., Jetz, W., Freckleton, R.P., 2010. Phylogenetic comparative approaches for studying niche conservatism. J. Evol. Biol. 23, 2529-2539.
[14] Crisp, M.D., Cook, L.G., 2012. Phylogenetic niche conservatism: what are the underlying evolutionary and ecological causes? New Phytol. 196, 681-694.
[15] Davis, E.B., 2005. Comparison of climate space and phylogeny of Marmota (Mammalia: Rodentia) indicates a connection between evolutionary history and climate preference. Proc. R. Soc. B-Biol. Sci. 272, 519-526.
[16] Darwin, C., 1859. On the Origin of Species by Means of Natural Selection, or, the Preservation of Favoured Races in the Struggle for Life. John Murray, London.
[17] Darwin, C., 1890. The Various Contrivances by which Orchids are Fertilised by Insects, Second ed. John Murray, London.
[18] Dorey, T., Schiestl, F.P., 2024. Bee-pollination promotes rapid divergent evolution in plants growing in different soils. Nat. Commun. 15, 2703.
[19] Fay, M.F., 2018. Orchid conservation: how can we meet the challenges in the twenty-first century? Bot. Stud. 59, 16.
[20] Givnish, T.J., 2010. Ecology of plant speciation. Taxon 59, 1326-1366.
[21] Gotsch, S.G., Davidson, K., Murray, J.G., et al., 2017. Vapor pressure deficit predicts epiphyte abundance across an elevational gradient in a tropical montane region. Am. J. Bot. 104, 1790-1801.
[22] Govaerts, R., Nic Lughadha, E., Black, N., et al., 2021. The world checklist of vascular plants, a continuously updated resource for exploring global plant diversity. Sci. Data 8, 215.
[23] Gravendeel, B., Smithson, A., Slik, F.J.W., et al., 2004. Epiphytism and pollinator specialization: drivers for orchid diversity? Philos. Trans. R. Soc. Lond. B-Biol. Sci. 359, 1523-1535.
[24] Hansen, T.F., 1997. Stabilizing selection and the comparative analysis of adaptation. Evolution 51, 1341-1351.
[25] Ho, L.S.T., Ane, C., 2014. A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Syst. Biol. 63, 397-408.
[26] Housworth, E.A., Martins, E.P., Lynch, M., 2004. The phylogenetic mixed model. Am. Nat. 163, 84-96.
[27] Huda, M.K., Wilcock, C.C., 2008. Impact of floral traits on the reproductive success of epiphytic and terrestrial tropical orchids. Oecologia 154, 731-741.
[28] Ives, A.R., 2019. R2s for correlated data: phylogenetic models, LMMs, and GLMMs. Syst. Biol. 68, 234-251.
[29] Ives, A.R., Garland, T., Jr., 2010. Phylogenetic logistic regression for binary dependent variables. Syst. Biol. 59, 9-26.
[30] Ives, A.R., Li, D., 2018. rr2: an R package to calculate R2s for regression models. J. Open Source Softw. 3, 1028.
[31] Jacquemyn, H., Brys, R., Merckx, V.S.F.T., et al., 2014. Coexisting orchid species have distinct mycorrhizal communities and display strong spatial segregation. New Phytol. 202, 616-627.
[32] Jia, L.B., Huang, S.Q., 2022. An examination of nectar production in 34 species of Dendrobium indicates that deceptive pollination in the orchids is not popular. J. Syst. Evol. 60, 1371-1377.
[33] Jin, Y., Qian, H., 2023. U.PhyloMaker: an R package that can generate large phylogenetic trees for plants and animals. Plant Divers. 45, 347-352.
[34] Johnson, L.J.A.N., Gonzalez-Chavez, M.C.A., Carrillo-Gonzalez, R., et al., 2021. Vanilla aerial and terrestrial roots host rich communities of orchid mycorrhizal and ectomycorrhizal fungi. Plants People Planet 3, 541-552.
[35] Johnson, S.D., 2010. The pollination niche and its role in the diversification and maintenance of the southern African flora. Philos. Trans. R. Soc. Lond. B-Biol. Sci. 365, 499-516.
[36] Kreft, H., Jetz, W., 2007. Global patterns and determinants of vascular plant diversity. Proc. Natl. Acad. Sci. U.S.A. 104, 5925-5930.
[37] Kuper, W., Kreft, H., Nieder, J., et al., 2004. Large-scale diversity patterns of vascular epiphytes in Neotropical montane rain forests. J. Biogeogr. 31, 1477-1487.
[38] Labra, A., Pienaar, J., Hansen, T.F., 2009. Evolution of thermal physiology in Liolaemus lizards: adaptation, phylogenetic inertia, and niche tracking. Am. Nat. 174, 204-220.
[39] Lima, J.F., Boanares, D., Costa, V.E., et al., 2023. Do photosynthetic metabolism and habitat influence foliar water uptake in orchids? Plant Biol. 25, 257-267.
[40] Losos, J.B., 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol. Lett. 11, 995-1003.
[41] Martos, F., Munoz, F., Pailler, T., et al., 2012. The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids. Mol. Ecol. 21, 5098-5109.
[42] McCormick, M.K., Whigham, D.F., Canchani-Viruet, A., 2018. Mycorrhizal fungi affect orchid distribution and population dynamics. New Phytol. 219, 1207-1215.
[43] Miller, B.D., Carter, K.R., Reed, S.C., et al., 2021. Only sun-lit leaves of the uppermost canopy exceed both air temperature and photosynthetic thermal optima in a wet tropical forest. Agric. For. Meteorol. 301-302, 108347.
[44] Moraes, A.P., Engel, T.B.J., Forni-Martins, E.R., et al., 2022. Are chromosome number and genome size associated with habit and environmental niche variables? Insights from the Neotropical orchids. Ann. Bot. 130, 11-25.
[45] Neiland, M.R.M., Wilcock, C.C., 1998. Fruit set, nectar reward, and rarity in the Orchidaceae. Am. J. Bot. 85, 1657-1671.
[46] Pagel, M., 1997. Inferring evolutionary processes from phylogenies. Zool. Scr. 26, 331-348.
[47] Papadopulos, A.S.T., Powell, M.P., Pupulin, F., et al., 2013. Convergent evolution of floral signals underlies the success of Neotropical orchids. Proc. R. Soc. B-Biol. Sci. 280, 20130960.
[48] Paradis, E., Schliep, K., 2019. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526-528.
[49] Pennell, M., Eastman, J., Slater, G., et al., 2014. Geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30, 2216-2218.
[50] Perez-Escobar, O.A., Bogarin, D., Przelomska, N.A.S., et al., 2024. The origin and speciation of orchids. New Phytol. 242, 700-716.
[51] Phillips, R.D., Reiter, N., Peakall, R., 2020. Orchid conservation: from theory to practice. Ann. Bot. 126, 345-362.
[52] R Core Team, 2023. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
[53] Ramos, S.E., Schiestl, F.P., 2019. Rapid plant evolution driven by the interaction of pollination and herbivory. Science 364, 193-196.
[54] Rasmussen, H.N., Rasmussen, F.N., 2018. The epiphytic habitat on a living host: reflections on the orchid-tree relationship. Bot. J. Linn. Soc. 186, 456-472.
[55] Rohlfs, R.V., Nielsen, R., 2015. Phylogenetic ANOVA: the expression variance and evolution model for quantitative trait evolution. Syst. Biol. 64, 695-708.
[56] Sanchez-Martinez, P., Ackerly, D.D., Martinez-Vilalta, J., et al., 2024. A framework to study and predict functional trait syndromes using phylogenetic and environmental data. Methods Ecol. Evol. 15, 666-681.
[57] Scopece, G., Cozzolino, S., Johnson, S.D., et al., 2010. Pollination efficiency and the evolution of specialized deceptive pollination systems. Am. Nat. 175, 98-105.
[58] Shrestha, N., Shen, X., Wang, Z., 2019. Biodiversity hotspots are insufficient in capturing range-restricted species. Conserv. Sci. Pract. 1, e103.
[59] Silvera, K., Santiago, L.S., Cushman, J.C., et al., 2009. Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae. Plant Physiol. 149, 1838-1847.
[60] Smith, S.A., Brown, J.W., 2018. Constructing a broadly inclusive seed plant phylogeny. Am. J. Bot. 105, 302-314.
[61] Spicer, M.E., Woods, C.L., 2022. A case for studying biotic interactions in epiphyte ecology and evolution. Perspect. Plant Ecol. Evol. Syst. 54, 125658.
[62] Steffelova, M., Traxmandlova, I., Stipkova, Z., et al., 2023. Pollination strategies of deceptive orchids - a review. Eur. J. Environ. Sci. 13, 110-116.
[63] Swarts, N.D., Dixon, K.W., 2009. Terrestrial orchid conservation in the age of extinction. Ann. Bot. 104, 543-556.
[64] Taylor, A., Keppel, G., Weigelt, P., et al., 2021. Functional traits are key to understanding orchid diversity on islands. Ecography 44, 703-714.
[65] Tremblay, R.L., Ackerman, J.D., Zimmerman, J.K., et al., 2005. Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biol. J. Linn. Soc. 84, 1-54.
[66] Van der Niet, T., Peakall, R., Johnson, S.D., 2014. Pollinator-driven ecological speciation in plants: new evidence and future perspectives. Ann. Bot. 113, 199-212.
[67] Veach, V., Di Minin, E., Pouzols, F.M., et al., 2017. Species richness as criterion for global conservation area placement leads to large losses in coverage of biodiversity. Divers. Distrib. 23, 715-726.
[68] Wang, G., Ives, A.R., Zhu, H., et al., 2022. Phylogenetic conservatism explains why plants are more likely to produce fleshy fruits in the tropics. Ecology 103, e03555.
[69] Whittaker, R.J., Nogues-Bravo, D., Araujo, M.B., 2007. Geographical gradients of species richness: a test of the water-energy conjecture of Hawkins et al. (2003) using European data for five taxa. Glob. Ecol. Biogeogr. 16, 76-89.
[70] Wiens, J.J., 2004. Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution 58, 193-197.
[71] Wiens, J.J., Ackerly, D.D., Allen, A.P., et al., 2010. Niche conservatism as an emerging principle in ecology and conservation biology. Ecol. Lett. 13, 1310-1324.
[72] Wraith, J., Pickering, C., 2018. Quantifying anthropogenic threats to orchids using the IUCN Red List. Ambio 47, 307-317.
[73] Yukawa, T., Ogura-Tsujita, Y., Shefferson, R.P., et al., 2009. Mycorrhizal diversity in Apostasia (Orchidaceae) indicates the origin and evolution of orchid mycorrhiza. Am. J. Bot. 96, 1997-2009.
[74] Zanne, A.E., Tank, D.C., Cornwell, W.K., et al., 2014. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89-92.
[75] Zhang, G., Hu, Y., Huang, M., et al., 2023. Comprehensive phylogenetic analyses of Orchidaceae using nuclear genes and evolutionary insights into epiphytism. J. Integr. Plant Biol. 65, 1204-1225.
[76] Zhang, S., Dai, Y., Hao, G., et al., 2015. Differentiation of water-related traits in terrestrial and epiphytic Cymbidium species. Front. Plant Sci. 6, 260.
[77] Zotz, G., 2005. Vascular epiphytes in the temperate zones-a review. Plant Ecol. 176, 173-183.
[78] Zotz, G., Hietz, P., 2001. The physiological ecology of vascular epiphytes: current knowledge, open questions. J. Exp. Bot. 52, 2067-2078.
[79] Zotz, G., Weigelt, P., Kessler, M., et al., 2021. EpiList 1.0: a global checklist of vascular epiphytes. Ecology 102, e03326.

Species evolution determines epiphyte evolution in Orchids

Species evolution determines epiphyte evolution in Orchids

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 1

Recommended Articles

Metrics

Comments