J Integr Plant Biol. ›› 2023, Vol. 65 ›› Issue (5): 1204-1225.DOI: 10.1111/jipb.13462

• Molecular Ecology and Evolution • Previous Articles     Next Articles

Comprehensive phylogenetic analyses of Orchidaceae using nuclear genes and evolutionary insights into epiphytism

Guojin Zhang1, Yi Hu1, Ming‐Zhong Huang2, Wei‐Chang Huang3, Ding‐Kun Liu2, Diyang Zhang2, Haihua Hu4, Jason L. Downing5, Zhong‐Jian Liu2† and Hong Ma1*   

  1. 1. Department of Biology, 510 Mueller Laboratory, Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, Pennsylvania 16802, USA;
    2. Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization at College of Landscape Architecture, Fujian Agriculture and Forestry University, Fuzhou 350002, China;
    3. Shanghai Chenshan Botanical Garden, Songjiang, Shanghai 201602, China;
    4. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China;
    5. Fairchild Tropical Botanic Garden, Coral Gables, Florida 33156, USA
    This author is co‐senior author.
    *Correspondence: Hong Ma (hxm16@psu.edu)
  • Received:2022-12-18 Accepted:2023-02-03 Online:2023-03-15 Published:2023-05-01

Abstract: 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.

Key words: convergence, epiphytes, evolution, orchids, parallel rainforest, phylogenomics, transcriptome

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