Comprehensive phylogenetic analyses of Orchidaceae using nuclear genes and evolutionary insights into epiphytism.
convergence
epiphytes
evolution
orchids
parallel rainforest
phylogenomics
transcriptome
Journal
Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502
Informations de publication
Date de publication:
May 2023
May 2023
Historique:
received:
18
12
2022
accepted:
03
02
2023
medline:
15
5
2023
pubmed:
5
2
2023
entrez:
4
2
2023
Statut:
ppublish
Résumé
Orchidaceae (with >28,000 orchid species) are one of the two largest plant families, with economically and ecologically important species, and occupy global and diverse niches with primary distribution in rainforests. Among orchids, 70% grow on other plants as epiphytes; epiphytes contribute up to ~50% of the plant diversity in rainforests and provide food and shelter for diverse animals and microbes, thereby contributing to the health of these ecosystems. Orchids account for over two-thirds of vascular epiphytes and provide an excellent model for studying evolution of epiphytism. Extensive phylogenetic studies of Orchidaceae and subgroups have ;been crucial for understanding relationships among many orchid lineages, although some uncertainties remain. For example, in the largest subfamily Epidendroideae with nearly all epiphytic orchids, relationships among some tribes and many subtribes are still controversial, hampering evolutionary analyses of epiphytism. Here we obtained 1,450 low-copy nuclear genes from 610 orchid species, including 431 with newly generated transcriptomes, and used them for the reconstruction of robust Orchidaceae phylogenetic trees with highly supported placements of tribes and subtribes. We also provide generally well-supported phylogenetic placements of 131 genera and 437 species that were not sampled by previous plastid and nuclear phylogenomic studies. Molecular clock analyses estimated the Orchidaceae origin at ~132 million years ago (Ma) and divergences of most subtribes from 52 to 29 Ma. Character reconstruction supports at least 14 parallel origins of epiphytism; one such origin was placed at the most recent common ancestor of ~95% of epiphytic orchids and linked to modern rainforests. Ten occurrences of rapid increase in the diversification rate were detected within Epidendroideae near and after the K-Pg boundary, contributing to ~80% of the Orchidaceae diversity. This study provides a robust and the largest family-wide Orchidaceae nuclear phylogenetic tree thus far and new insights into the evolution of epiphytism in vascular plants.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1204-1225Informations de copyright
© 2023 The Authors. Journal of Integrative Plant Biology published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.
Références
Alghamdi, S.A. (2019). Influence of mycorrhizal fungi on seed germination and growth in terrestrial and epiphytic orchids. Saudi J. Biol. Sci. 26: 495-502.
Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Barrett, C.F., Sinn, B.T., Kennedy, A.H., and Pupko, T. (2019). Unprecedented parallel photosynthetic losses in a heterotrophic orchid genus. Mol. Biol. Evol. 36: 1884-1901.
Barthlott, W., Große-Veldmann, B., and Korotkova, N. (2014). Orchid seed diversity: A scanning electron microscopy survey. Englera 32: 1-239.
Benton, M.J., Wilf, P., and Sauquet, H. (2022). The Angiosperm Terrestrial Revolution and the origins of modern biodiversity. New Phytol. 233: 2017-2035.
van den Berg, C., Goldman, D.H., Freudenstein, J.V., Pridgeon, A.M., Cameron, K.M., and Chase, M.W. (2005). An overview of the phylogenetic relationships within Epidendroideae inferred from multiple DNA regions and recircumscription of Epidendreae and Arethuseae (Orchidaceae). Am. J. Bot. 92: 613-624.
van den Berg, C., Higgins, W.E., Dressler, R.L., Whitten, W.M., Soto-Arenas, M.A., and Chase, M.W. (2009). A phylogenetic study of Laeliinae (Orchidaceae) based on combined nuclear and plastid DNA sequences. Ann. Bot. 104: 417-430.
Berry, K. (2020). Evidence for fungal proliferation following the Cretaceous/Paleogene mass-extinction event, based on chemostratigraphy in the Raton and Powder River basins, western North America. Acta Palaeobot. 60: 134-142.
Bulpitt, C.J. (2005). The uses and misuses of orchids in medicine. QJM 98: 625-631.
Bulpitt, C.J., Li, Y., Bulpitt, P.F., and Wang, J. (2007). The use of orchids in Chinese medicine. J. R. Soc. Med. 100: 558-563.
Bushnell, B. (2015). BBMap short-read aligner, and other bioinformatics tools. https://sourceforge.net/projects/bbmap/
Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., and Madden, T.L. (2009). BLAST+: Architecture and applications. BMC Bioinformatics 10: 421.
Cameron, K.M., Chase, M.W., Whitten, W.M., Kores, P.J., Jarrell, D.C., Albert, V.A., Yukawa, T., Hills, H.G., and Goldman, D.H. (1999). A phylogenetic analysis of the Orchidaceae: Evidence from rbcL nucleotide sequences. Am. J. Bot. 86: 208-224.
Capella-Gutiérrez, S., Silla-Martínez, J.M., and Gabaldón, T. (2009). trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973.
Cardelús, C.L., Mack, M.C., Woods, C., DeMarco, J., and Treseder, K.K. (2009). The influence of tree species on canopy soil nutrient status in a tropical lowland wet forest in Costa Rica. Plant and Soil. 318: 47-61.
Carlsward, B.S., Whitten, W.M., Williams, N.H., and Bytebier, B. (2006). Molecular phylogenetics of Vandeae (Orchidaceae) and the evolution of leaflessness. Am. J. Bot. 93: 770-786.
Carvalho, M.R., Jaramillo, C., de la Parra, F., Caballero-Rodríguez, D., Herrera, F., Wing, S., Turner, B.L., D'Apolito, C., Romero-Báez, M., Narváez, P., Martínez, C., Gutierrez, M., Labandeira, C., Bayona, G., Rueda, M., Paez-Reyes, M., Cárdenas, D., Duque, Á., Crowley, J.L., Santos, C., and Silvestro, D. (2021). Extinction at the end-Cretaceous and the origin of modern Neotropical rainforests. Science 372: 63-68.
Chase, M.W., Cameron, K.M., Freudenstein, J.V., Pridgeon, A.M., Salazar, G., van den Berg, C., and Schuiteman, A. (2015). An updated classification of Orchidaceae. Bot. J. Linn. Soc. 177: 151-174.
Chomicki, G., Bidel, L.P.R., Ming, F., Coiro, M., Zhang, X., Wang, Y., Baissac, Y., Jay-Allemand, C., and Renner, S.S. (2015). The velamen protects photosynthetic orchid roots against UV-B damage, and a large dated phylogeny implies multiple gains and losses of this function during the Cenozoic. New Phytol. 205: 1330-1341.
Christenhusz, M.J.M. and Byng, J.W. (2016). The number of known plants species in the world and its annual increase. Phytotaxa 261: 201-217.
Cramer, M.J. and Willig, M.R. (2002). Habitat heterogeneity, habitat associations, and rodent species diversity in a sand-shinnery-oak landscape. J. Mammal. 83: 743-753.
Crayn, D.M., Winter, K., and Smith, J.A.C. (2004). Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proc. Natl. Acad. Sci. U.S.A. 101: 3703-3708.
Cvetkovic, T., Areces-Berazain, F., Hinsinger, D.D., Thomas, D.C., Wieringa, J.J., Ganesan, S.K., and Strijk, J.S. (2021). Phylogenomics resolves deep subfamilial relationships in Malvaceae s.l. G3 Genes Genomes Genetics 11: kab136.
Darwin, C. (1877). The Various Contrivances by Which Orchids Are Fertilised by Insects (London: John Murray).
Dearnaley, J.D.W., Martos, F., and Selosse, M.A. (2012). Orchid mycorrhizas: Molecular ecology, physiology, evolution and conservation aspects. In: B. Hock ed. Fungal Associations, 2nd Ed., Heidelberg: Springer, Berlin. pp. 207-230.
Deng, H., Zhang, G., Lin, M., Wang, Y., and Liu, Z. (2015). Mining from transcriptomes: 315 single-copy orthologous genes concatenated for the phylogenetic analyses of Orchidaceae. Ecol. Evol. 5: 3800-3807.
Dewi, E.R.S., Nurgroho, A.S., and Ulfah, M. (2020). Types of epiphytic orchids and host plants on ungaran mountain limbangan kendal central java and its potential as orchid conservation area. Int. J. Conserv. Sci 11: 117-124.
Du, X.Y., Lu, J.M., Zhang, L.B., Wen, J., Kuo, L.Y., Mynssen, C.M., Schneider, H., and Li, D.Z. (2021). Simultaneous diversification of Polypodiales and angiosperms in the Mesozoic. Cladistics 37: 518-539.
Ebersberger, I., Strauss, S., and Von Haeseler, A. (2009). HaMStR: Profile hidden markov model based search for orthologs in ESTs. BMC Evol. Biol. 9: 157.
Eguchi, S. and Tamura, M.N. (2016). Evolutionary timescale of monocots determined by the fossilized birth-death model using a large number of fossil records. Evolution 70: 1136-1144.
Emms, D.M. and Kelly, S. (2019). OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biol. 20: 1-14.
Engwald, S., Schmit-Neuerburg, V., and Barthlott, W. (2000). Epiphytes in rain forests of Venezuela - Diversity and dynamics of a biocenosis. In: Breckle, S. W., Schweizer B., eds. Results of Worldwide Ecological Studies. Proceedings of the 1st Symposium by the A.F.W Schimper-Foundation - from H. and E. Walter - Hoheneim, Oktober 1998, Hohenheim: Verlag GünterHeimbach, Stuttgart. pp. 425-433.
Eserman, L.A., Thomas, S.K., Coffey, E.E.D., and Leebens-Mack, J.H. (2021). Target sequence capture in orchids: Developing a kit to sequence hundreds of single-copy loci. Appl. Plant Sci. 9: e11416.
Fernández, M., Kaur, J., and Sharma, J. (2023). Co-occurring epiphytic orchids have specialized mycorrhizal fungal niches that are also linked to phenology. Mycorrhiza.
Freudenstein, J.V. and Chase, M.W. (2015). Phylogenetic relationships in Epidendroideae (Orchidaceae), one of the great flowering plant radiations: Progressive specialization and diversification. Ann. Bot. 115: 665-681.
Gallage, N.J. and Møller, B.L. (2015). Vanillin-bioconversion and bioengineering of the most popular plant flavor and its de novo biosynthesis in the vanilla orchid. Mol. Plant 8: 40-57.
Gebauer, G., Preiss, K., and Gebauer, A.C. (2016). Partial mycoheterotrophy is more widespread among orchids than previously assumed. New Phytol. 211: 11-15.
Givnish, T.J., Spalink, D., Ames, M., Lyon, S.P., Hunter, S.J., Zuluaga, A., Doucette, A., Caro, G.G., McDaniel, J., Clements, M.A., Arroyo, M.T.K., Endara, L., Kriebel, R., Williams, N.H., and Cameron, K.M. (2016). Orchid historical biogeography, diversification, Antarctica and the paradox of orchid dispersal. J. Biogeogr. 43: 1905-1916.
Givnish, T.J., Spalink, D., Ames, M., Lyon, S.P., Hunter, S.J., Zuluaga, A., Iles, W.J.D., Clements, M.A., Arroyo, M.T.K., Leebens-Mack, J., Endara, L., Kriebel, R., Neubig, K.M., Whitten, W.M., Williams, N.H., and Cameron, K.M. (2015). Orchid phylogenomics and multiple drivers of their extraordinary diversification. Proc. R. Soc. B Biol. Sci. 282.
Górniak, M., Paun, O., and Chase, M.W. (2010). Phylogenetic relationships within Orchidaceae based on a low-copy nuclear coding gene, Xdh: Congruence with organellar and nuclear ribosomal DNA results. Mol. Phylogenet. Evol. 56: 784-795.
Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., Di Palma, F., Birren, B.W., Nusbaum, C., Lindblad-Toh, K., Friedman, N., and Regev, A. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29: 644-652.
Gustafsson, A.L.S., Verola, C.F., and Antonelli, A. (2010). Reassessing the temporal evolution of orchids with new fossils and a Bayesian relaxed clock, with implications for the diversification of the rare South American genus Hoffmannseggella (Orchidaceae: Epidendroideae). BMC Evol. Biol. 10: 1-13.
Hasing, T., Tang, H., Brym, M., Khazi, F., Huang, T., and Chambers, A.H. (2020). A phased Vanilla planifolia genome enables genetic improvement of flavour and production. Nat. Food 1: 811-819.
Hernández-Pérez, E., Solano, E., Ríos-Gómez, R., Hernández-Pérez, E., Solano, E., and Ríos-Gómez, R. (2018). Host affinity and vertical distribution of epiphytic orchids in a montane cloud forest in southern Mexico. Bot. Sci. 96: 200-217.
Hew, C.S. (2001). Ancient Chinese orchid cultivation. A fresh look at an age-old practice. Sci. Hortic. (Amsterdam) 87: 1-10.
Holbrook, N.M. and Putz, F.E. (1996). Physiology of tropical vines and Hemiepiphytes: Plants that climb up and plants that climb down. In Tropical Forest Plant Ecophysiology, S. S. Mulkey, R. L. Chazdon and A. P. Smith, eds. (Boston, MA: Springer). pp. 363-394.
Huang, B.Q., Yang, X.Q., Yu, F.H., Luo, Y.B., and Tai, Y.D. (2008). Surprisingly high orchid diversity in travertine and forest areas in the Huanglong valley, China, and implications for conservation. Biodivers. Conserv. 17: 2773-2786.
Huang, W., Zhang, L., Columbus, J.T., Hu, Y., Zhao, Y., Tang, L., Guo, Z., Chen, W., McKain, M., Bartlett, M., Huang, C.H., Li, D.Z., Ge, S., and Ma, H. (2022). A well-supported nuclear phylogeny of Poaceae and implications for the evolution of C4 photosynthesis. Mol. Plant 15: 755-777.
Huurdeman, E.P., Frieling, J., Reichgelt, T., Bijl, P.K., Bohaty, S.M., Holdgate, G.R., Gallagher, S.J., Peterse, F., Greenwood, D.R., and Pross, J. (2021). Rapid expansion of meso-megathermal rain forests into the southern high latitudes at the onset of the Paleocene-Eocene Thermal Maximum. Geology 49: 40-44.
Iles, W.J.D., Smith, S.Y., Gandolfo, M.A., and Graham, S.W. (2015). Monocot fossils suitable for molecular dating analyses. Bot. J. Linn. Soc. 178: 346-374.
Jaramillo, C., Ochoa, D., Contreras, L., Pagani, M., Carvajal-Ortiz, H., Pratt, L.M., Krishnan, S., Cardona, A., Romero, M., Quiroz, L., Rodriguez, G., Rueda, M.J., De La Parra, F., Morón, S., Green, W., Bayona, G., Montes, C., Quintero, O., Ramirez, R., Mora, G., Schouten, S., Bermudez, H., Navarrete, R., Parra, F., Alvarán, M., Osorno, J., Crowley, J.L., Valencia, V., and Vervoort, J. (2010). Effects of rapid global warming at the paleocene-eocene boundary on neotropical vegetation. Science 330: 957-961.
Joca, T.A.C., Oliveira, D.C., de Zotz, G., Winkler, U., and Moreira, A.S.F.P. (2017). The velamen of epiphytic orchids: Variation in structure and correlations with nutrient absorption. Flora 230: 66-74.
Kaiho, K., Oshima, N., Adachi, K., Adachi, Y., Mizukami, T., Fujibayashi, M., and Saito, R. (2016). Global climate change driven by soot at the K-Pg boundary as the cause of the mass extinction. Sci. Rep. 6: 1-13.
Kassambara, A. (2020). ggpubr: “ggplot2” based publication ready plots. https://CRAN.R-project.org/package=ggpubr
Katoh, K. and Standley, D.M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30: 772-780.
Kelly, D.L., Tanner, E.V.J., Lughadha, E.M.N., and Kapos, V. (1994). Floristics and biogeography of a rain forest in the Venezuelan Andes. J. Biogeogr. 21: 421.
Kim, Y.K., Jo, S., Cheon, S.H., Joo, M.J., Hong, J.R., Kwak, M., and Kim, K.J. (2020). Plastome evolution and phylogeny of orchidaceae, with 24 new sequences. Front. Plant Sci. 11: 22.
Krause, G.H., Koroleva, O.Y., Dalling, J.W., and Winter, K. (2001). Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant Cell Environ. 24: 1345-1352.
Küper, W., Kreft, H., Nieder, J., Köster, N., and Barthlott, W. (2004). Large-scale diversity patterns of vascular epiphytes in Neotropical montane rain forests. J. Biogeogr 31: 1477-1487.
Li, H.T., Yi, T.S., Gao, L.M., Ma, P.F., Zhang, T., Yang, J.B., Gitzendanner, M.A., Fritsch, P.W., Cai, J., Luo, Y., Wang, H., van der Bank, M., Zhang, S.D., Wang, Q.F., Wang, J., Zhang, Z.R., Fu, C.N., Yang, J., Hollingsworth, P.M., Chase, M.W., Soltis, D.E., Soltis, P.S., and Li, D.Z. (2019). Origin of angiosperms and the puzzle of the Jurassic gap. Nat. Plants 5: 461-470.
Li M.H., Liu K.W., Li Z., Lu H.C., Ye Q.L., Zhang D., Wang J.Y., Li Y.F., Zhong Z.M., Liu X., Yu X., Liu D.K., Tu X.D, Liu B., Hao Y., Liao X.Y., Jiang Y.T., Sun W.H., Chen J., Chen Y.Q., Ai Y., Zhai J.W., Wu S.S., Zhou Z., Hsiao Y.Y., Wu W.L., Chen Y.Y., Lin Y.F., Hsu J.L., Li C.Y., Wang Z.W., Zhao X., Zhong W.Y., Ma X.K., Ma L., Huang J., Chen G.Z., Huang M.Z., Huang L., Peng D.H., Luo Y.B., Zou S.Q., Chen S.P., Lan S., Tsai W.C., Van de Peer Y., Liu Z.J. (2022) Genomes of leafy and leafless Platanthera orchids illuminate the evolution of mycoheterotrophy. Nat. Plants 8: 373-388.
Li M.H., Zhang G.Q., Lan S.R., Liu Z.J., Chen Z.D., Lu A.M., Kong H.Z., Wang X.Q., Wang Y.Z., Zhou S.L., Zhang S.Z., Wang X.M., Liu Z.J., Wang Q.F., Li J.H., Li D.Z., Yi T.S., Hong M.A., Soltis D.E., Soltis P.S., Li J.H., Fu C.X., Liu Q.X. (2016) A molecular phylogeny of Chinese orchids. J. Syst. Evol. 54: 349-362.
Li, W. and Godzik, A. (2006). Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
Li, Y.X., Li, Z.H., Schuitman, A., Chase, M.W., Li, J.W., Huang, W.C., Hidayat, A., Wu, S.S., and Jin, X.H. (2019). Phylogenomics of Orchidaceae based on plastid and mitochondrial genomes. Mol. Phylogenet. Evol. 139: 106540.
Li, Z.H., Jiang, Y., Ma, X., Li, J.W., Yang, J.B., Wu, J.Y., and Jin, X.H. (2020). Plastid genome evolution in the Subtribe Calypsoinae (Epidendroideae, Orchidaceae). Genome Biol. Evol. 12: 867-870.
de Lima, J.F. and Moreira, A.S.F.P. (2022). Structural plasticity in roots of the Hemiepiphyte Vanilla phaeantha Rchb.f. (Orchidaceae): A relationship between environment and function. Naturwissenschaften 109: 46.
Maddison, W.P. and Maddison, D.R. (2021). Mesquite: A modular system for evolutionary analysis. http://www.mesquiteproject.org
Madison, M., Dodson, C.H., Dressler, R.L., Howard, R.A., Luteyn, J., Plowman, T., Smith, L.B., Stevens, P.F., Steyermark, J., Stone, B.C., Van Royen, P., Wiehler, H., and Wurdack, J. (1977). Vascular epiphytes: Their systematic occurrence and salnent features. Selbyana 2: 1-13.
Martos, F., Munoz, F., Pailler, T., Kottke, I., Gonneau, C., and Selosse, M.A. (2012). The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids. Mol. Ecol. 21: 5098-5109.
McCormick, M.K., Whigham, D.F., and Canchani-Viruet, A. (2018). Mycorrhizal fungi affect orchid distribution and population dynamics. New Phytol. 219: 1207-1215.
Morales-Linares, J., Flores-Palacios, A., Corona-López, A.M., and Toledo-Hernández, V.H. (2021). Diversity and interactions of the epiphyte community associated with ant-gardens are not influenced by elevational and environmental gradients. J. Veg. Sci. 32: e13076.
Nadkarni, N.M., Schaefer, D., Matelson, T.J., and Solano, R. (2002). Comparison of arboreal and terrestrial soil characteristics in a lower montane forest, Monteverde, Costa Rica. Pedobiologia (Jena) 46: 24-33.
Nakamura, A., Kitching, R.L., Cao, M., Creedy, T.J., Fayle, T.M., Freiberg, M., Hewitt, C.N., Itioka, T., Koh, L.P., Ma, K., Malhi, Y., Mitchell, A., Novotny, V., Ozanne, C.M.P., Song, L., Wang, H., and Ashton, L.A. (2017). Forests and their canopies: Achievements and horizons in canopy science. Trends. Ecol. Evol. 32: 438-451.
Ng, C.K.Y., and Hew, C.S. (2000). Orchid pseudobulbs - ‘false’ bulbs with a genuine importance in orchid growth and survival!. Scientia Horticulturae. 83: 165-172.
Pérez-Escobar, O.A., Chomicki, G., Condamine, F.L., Karremans, A.P., Bogarín, D., Matzke, N.J., Silvestro, D., and Antonelli, A. (2017). Recent origin and rapid speciation of Neotropical orchids in the world's richest plant biodiversity hotspot. New Phytol. 215: 891-905.
Pérez-Escobar, O.A., Dodsworth, S., Bogarín, D., Bellot, S., Balbuena, J.A., Schley, R.J., Kikuchi, I.A., Morris, S.K., Epitawalage, N., Cowan, R., Maurin, O., Zuntini, A., Arias, T., Serna-Sánchez, A., Gravendeel, B., Torres Jimenez, M.F., Nargar, K., Chomicki, G., Chase, M.W., Leitch, I.J., Forest, F., and Baker, W.J. (2021). Hundreds of nuclear and plastid loci yield novel insights into orchid relationships. Am. J. Bot. 108: 1166-1180.
Petter, G., Zotz, G., Kreft, H., and Cabral, J.S. (2021). Agent-based modeling of the effects of forest dynamics, selective logging, and fragment size on epiphyte communities. Ecol. Evol. 11: 2937-2951.
Philippe, H., Brinkmann, H., Lavrov, D.V., Littlewood, D.T.J., Manuel, M., Wörheide, G., and Baurain, D. (2011). Resolving difficult phylogenetic questions: Why more sequences are not enough. PLoS Biol. 9: e1000602.
Qin, J., Zhang, W., Zhang, S.B., and Wang, J.H. (2020). Similar mycorrhizal fungal communities associated with epiphytic and lithophytic orchids of Coelogyne corymbosa. Plant Divers. 42: 362-369.
Rabosky, D.L. (2014). Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9: e89543.
Rabosky, D.L., Grundler, M., Anderson, C., Title, P., Shi, J.J., Brown, J.W., Huang, H., and Larson, J.G. (2014). BAMMtools: An R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods Ecol. Evol. 5: 701-707.
Ramírez, S.R., Gravendeel, B., Singer, R.B., Marshall, C.R., and Pierce, N.E. (2007). Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Nature 448: 1042-1045.
Rico-Gray, V. and Thien, L.B. (1989). Effect of different ant species on reproductive fitness of Schomburgkia tibicinis (Orchidaceae). Oecologia 1989 814 81: 487-489.
Romero, G.Q., Nomura, F., Gonçalves, A.Z., Dias, N.Y.N., Mercier, H., Conforto, E.deC., and Rossa-Feres, D.deC. (2010). Nitrogen fluxes from treefrogs to tank epiphytic bromeliads: An isotopic and physiological approach. Oecologia 162: 941-949.
Schneider, H., Schuetipelz, E., Pryer, K.M., Cranfill, R., Magallón, S., and Lupia, R. (2004). Ferns diversified in the shadow of angiosperms. Nature 428(6982): 553-557.
Schuettpelz, E. and Pryer, K.M. (2009). Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proc. Natl. Acad. Sci. U.S.A. 106: 11200-11205.
Serna-Sánchez, M.A., Pérez-Escobar, O.A., Bogarín, D., Torres-Jimenez, M.F., Alvarez-Yela, A.C., Arcila-Galvis, J.E., Hall, C.F., de Barros, F., Pinheiro, F., Dodsworth, S., Chase, M.W., Antonelli, A., and Arias, T. (2021). Plastid phylogenomics resolves ambiguous relationships within the orchid family and provides a solid timeframe for biogeography and macroevolution. Sci. Rep. 11: 1-11.
Shaw, D.C. (2004). Vertical organization of canopy biota. In: Forest Canopies: Second Edition, M. D. Lowman and H. B. Rinker, eds. (Amsterdam: Elsevier). pp. 73-101.
Shen, W., Le, S., Li, Y., and Hu, F. (2016). SeqKit: A cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS One 11: e0163962.
Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V., and Zdobnov, E.M. (2015). BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31: 3210-3212.
Smith, S.A. and O'Meara, B.C. (2012). treePL: Divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics 28: 2689-2690.
Spicer, M.E. and Woods, C.L. (2022). A case for studying biotic interactions in epiphyte ecology and evolution. Perspect. Plant Ecol. Evol. Syst. 54: 125658.
Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313.
Stanton, D.E., Huallpa Chávez, J., Villegas, L., Villasante, F., Armesto, J., Hedin, L.O., and Horn, H. (2014). Epiphytes improve host plant water use by microenvironment modification. Funct. Ecol. 28: 1274-1283.
Sukumaran, J. and Holder, M.T. (2010). DendroPy: A Python library for phylogenetic computing. Bioinformatics 26: 1569-1571.
Takahashi, C.A., Coutinho Neto, A.A., Mercier, H. (2022). An overview of water and nutrient uptake by Epiphytic Bromeliads: New insights into the absorptive capability of leaf trichomes and roots. In: Lüttge, U., Cánovas, F. M., eds. Progress in Botany. Springer, Berlin, Heidelberg. pp. 1-18.
Teoh, E.S. (2019). Australian orchids as food and medicine. In: Teoh, E.S., Orchids as Aphrodisiac, Medicine or Food, Springer International Publishing, pp. 291-303.
Trevail, A.M., Green, J.A., Bolton, M., Daunt, F., Harris, S.M., Miller, P.I., Newton, S., Owen, E., Polton, J.A., Robertson, G., Sharples, J., and Patrick, S.C. (2021). Environmental heterogeneity promotes individual specialisation in habitat selection in a widely distributed seabird. J. Anim. Ecol. 90: 2875-2887.
Vajda, V. and Bercovici, A. (2014). The global vegetation pattern across the Cretaceous-Paleogene mass extinction interval: A template for other extinction events. Glob. Planet. Change 122: 29-49.
Vance, E.D., and Nadkarni, N.M. (1990). Microbial biomass and activity in canopy organic matter and the forest floor of a tropical cloud forest. Soil Biology and Biochemistry. 22: 677-684.
Veizer, J., Godderis, Y., and François, L.M. (2000). Evidence for decoupling of atmospheric CO2 and global climate during the Phanerozoic Eon. Nature 408: 698-701.
Wang, X., Long, W., Schamp, B.S., Yang, X., Kang, Y., Xie, Z., and Xiong, M. (2016). Vascular epiphyte diversity differs with host crown zone and diameter, but not orientation in a tropical cloud forest. PLoS One 11: e0158548.
Watkins, J.E. and Cardelús, C.L. (2012). Ferns in an angiosperm world: Cretaceous radiation into the epiphytic niche and diversification on the forest floor. Int. J. Plant Sci. 173: 695-710.
Westerhold, T., Marwan, N., Drury, A.J., Liebrand, D., Agnini, C., Anagnostou, E., Barnet, J.S.K., Bohaty, S.M., De Vleeschouwer, D., Florindo, F., Frederichs, T., Hodell, D.A., Holbourn, A.E., Kroon, D., Lauretano, V., Littler, K., Lourens, L.J., Lyle, M., Pälike, H., Röhl, U., Tian, J., Wilkens, R.H., Wilson, P.A., and Zachos, J.C. (2020). An astronomically dated record of Earth's climate and its predictability over the last 66 million years. Science 369: 1383-1388.
Wong, D.C.J. and Peakall, R. (2022). Orchid Phylotranscriptomics: The prospects of repurposing multi-tissue transcriptomes for phylogenetic analysis and beyond. Front. Plant Sci. 13: 1493.
Xing, X., Gai, X., Liu, Q., Hart, M.M., and Guo, S. (2015). Mycorrhizal fungal diversity and community composition in a lithophytic and epiphytic orchid. Mycorrhiza 25: 289-296.
Yang, S.-J., Sun, M., Yang, Q.-Y., Ma, R.-Y., Zhang, J.-L., and Zhang, S.-B. (2016). Two strategies by epiphytic orchids for maintaining water balance: thick cuticles in leaves and water storage in pseudobulbs. AoB PLANTS. 8: plw046.
Ye, H., Wang, Z., Hou, H., Wu, J., Gao, Y., Han, W., Ru, W., Sun, G., and Wang, Y. (2021). Localized environmental heterogeneity drives the population differentiation of two endangered and endemic Opisthopappus Shih species. BMC Ecol. Evol. 21: 1-20.
Yuan, Y., Jin, X., Liu, J., Zhao, X., Zhou, J., Wang, X., Wang, D., Lai, C., Xu, W., Huang, J., Zha, L., Liu, D., Ma, X., Wang, L., Zhou, M., Jiang, Z., Meng, H., Peng, H., Liang, Y., Li, R., Jiang, C., Zhao, Y., Nan, T., Jin, Y., Zhan, Z., Yang, J., Jiang, W., and Huang, L. (2018). The Gastrodia elata genome provides insights into plant adaptation to heterotrophy. Nat. Commun. 9: 1-11.
Zeng, R.Z., Zhu, J., Xu, S.Y., Du, G.H., Guo, H.R., Chen, J., Zhang, Z.S., and Xie, L. (2020). Unreduced male gamete formation in cymbidium and its use for developing sexual polyploid cultivars. Front. Plant Sci. 11: 558.
Zhang, C., Rabiee, M., Sayyari, E., and Mirarab, S. (2018). ASTRAL-III: Polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19: 153.
Zhang, Z., Yan, Y., Tian, Y., Li, J., He, J.S., and Tang, Z. (2015). Distribution and conservation of orchid species richness in China. Biol. Conserv. 181: 64-72.
Zhao, D.K., Selosse, M.A., Wu, L., Luo, Y., Shao, S.C., and Ruan, Y.L. (2021). Orchid reintroduction based on seed germination-promoting mycorrhizal fungi derived from protocorms or seedlings. Front. Plant Sci. 12: 1298.
Zhao, Y., Zhang, R., Jiang, K.W., Qi, J., Hu, Y., Guo, J., Zhu, R., Zhang, T., Egan, A.N., Yi, T.S., Huang, C.H., and Ma, H. (2021). Nuclear phylotranscriptomics and phylogenomics support numerous polyploidization events and hypotheses for the evolution of rhizobial nitrogen-fixing symbiosis in Fabaceae. Mol. Plant 14: 748-773.
Zotz, G. (2016). Biogeography: Latitudinal and elevational trends. In: Zotz, G. ed. Plants on Plants - The Biology of Vascular Epiphytes. Springer, Cham. pp. 51-66.
Zotz, G. (2013). The systematic distribution of vascular epiphytes - A critical update. Bot. J. Linn. Soc. 171: 453-481.
Zotz, G., Leja, M., Aguilar-Cruz, Y., and Einzmann, H.J.R. (2020). How much water is in the tank? An allometric analysis with 205 bromeliad species. Flora 264: 151557.
Zotz, G., Weigelt, P., Kessler, M., Kreft, H., and Taylor, A. (2021). EpiList 1.0: A global checklist of vascular epiphytes. Ecology 102: e03326.
Zotz, G. and Winkler, U. (2013). Aerial roots of epiphytic orchids: The Velamen radicum and its role in water and nutrient uptake. Oecologia 171: 733-741.
Zou, L.H., Huang, J.X., Zhang, G.Q., Liu, Z.J., and Zhuang, X.Y. (2015). A molecular phylogeny of Aeridinae (Orchidaceae: Epidendroideae) inferred from multiple nuclear and chloroplast regions. Mol. Phylogenet. Evol. 85: 247-254.