Diversification Slowdown in the Cirrhopetalum Alliance (Bulbophyllum, Orchidaceae): Insights From the Evolutionary Dynamics of Crassulacean Acid Metabolism
Evolutionary slowdowns in diversification have been inferred in various plant and animal lineages. Investigation based on diversification models integrated with environmental factors and key characters could provide critical insights into this diversification trend. We evaluate diversification rates...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-02-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.794171/full |
| _version_ | 1818510198690545664 |
|---|---|
| author | Ai-Qun Hu Ai-Qun Hu Ai-Qun Hu Stephan W. Gale Zhong-Jian Liu Gunter A. Fischer Richard M. K. Saunders |
| author_facet | Ai-Qun Hu Ai-Qun Hu Ai-Qun Hu Stephan W. Gale Zhong-Jian Liu Gunter A. Fischer Richard M. K. Saunders |
| author_sort | Ai-Qun Hu |
| collection | DOAJ |
| description | Evolutionary slowdowns in diversification have been inferred in various plant and animal lineages. Investigation based on diversification models integrated with environmental factors and key characters could provide critical insights into this diversification trend. We evaluate diversification rates in the Cirrhopetalum alliance (Bulbophyllum, Orchidaceae subfam. Epidendroideae) using a time-calibrated phylogeny and assess the role of Crassulacean acid metabolism (CAM) as a hypothesised key innovation promoting the spectacular diversity of orchids, especially those with an epiphytic habit. An explosive early speciation in the Cirrhopetalum alliance is evident, with the origin of CAM providing a short-term advantage under the low atmospheric CO2 concentrations (pCO2) associated with cooling and aridification in the late Miocene. A subsequent slowdown of diversification in the Cirrhopetalum alliance is possibly explained by a failure to keep pace with pCO2 dynamics. We further demonstrate that extinction rates in strong CAM lineages are ten times higher than those of C3 lineages, with CAM not as evolutionarily labile as previously assumed. These results challenge the role of CAM as a “key innovation” in the diversification of epiphytic orchids. |
| first_indexed | 2024-12-10T22:56:02Z |
| format | Article |
| id | doaj.art-e2c92f129e464245b13c710502984d4d |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-10T22:56:02Z |
| publishDate | 2022-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-e2c92f129e464245b13c710502984d4d2022-12-22T01:30:16ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-02-011310.3389/fpls.2022.794171794171Diversification Slowdown in the Cirrhopetalum Alliance (Bulbophyllum, Orchidaceae): Insights From the Evolutionary Dynamics of Crassulacean Acid MetabolismAi-Qun Hu0Ai-Qun Hu1Ai-Qun Hu2Stephan W. Gale3Zhong-Jian Liu4Gunter A. Fischer5Richard M. K. Saunders6Royal Botanic Gardens, Kew, Richmond, United KingdomDivision of Ecology and Biodiversity, School of Biological Sciences, The University of Hong Kong, Pokfulam, Hong Kong SAR, ChinaKadoorie Farm and Botanic Garden, Tai Po, Hong Kong SAR, ChinaKadoorie Farm and Botanic Garden, Tai Po, Hong Kong SAR, ChinaKey Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization at College of Landscape Architecture, Fujian Agriculture and Forestry University, Fuzhou, ChinaKadoorie Farm and Botanic Garden, Tai Po, Hong Kong SAR, ChinaDivision of Ecology and Biodiversity, School of Biological Sciences, The University of Hong Kong, Pokfulam, Hong Kong SAR, ChinaEvolutionary slowdowns in diversification have been inferred in various plant and animal lineages. Investigation based on diversification models integrated with environmental factors and key characters could provide critical insights into this diversification trend. We evaluate diversification rates in the Cirrhopetalum alliance (Bulbophyllum, Orchidaceae subfam. Epidendroideae) using a time-calibrated phylogeny and assess the role of Crassulacean acid metabolism (CAM) as a hypothesised key innovation promoting the spectacular diversity of orchids, especially those with an epiphytic habit. An explosive early speciation in the Cirrhopetalum alliance is evident, with the origin of CAM providing a short-term advantage under the low atmospheric CO2 concentrations (pCO2) associated with cooling and aridification in the late Miocene. A subsequent slowdown of diversification in the Cirrhopetalum alliance is possibly explained by a failure to keep pace with pCO2 dynamics. We further demonstrate that extinction rates in strong CAM lineages are ten times higher than those of C3 lineages, with CAM not as evolutionarily labile as previously assumed. These results challenge the role of CAM as a “key innovation” in the diversification of epiphytic orchids.https://www.frontiersin.org/articles/10.3389/fpls.2022.794171/fullCAMdiversification slowdownevolutionary dead-endkey innovationpCO2 |
| spellingShingle | Ai-Qun Hu Ai-Qun Hu Ai-Qun Hu Stephan W. Gale Zhong-Jian Liu Gunter A. Fischer Richard M. K. Saunders Diversification Slowdown in the Cirrhopetalum Alliance (Bulbophyllum, Orchidaceae): Insights From the Evolutionary Dynamics of Crassulacean Acid Metabolism Frontiers in Plant Science CAM diversification slowdown evolutionary dead-end key innovation pCO2 |
| title | Diversification Slowdown in the Cirrhopetalum Alliance (Bulbophyllum, Orchidaceae): Insights From the Evolutionary Dynamics of Crassulacean Acid Metabolism |
| title_full | Diversification Slowdown in the Cirrhopetalum Alliance (Bulbophyllum, Orchidaceae): Insights From the Evolutionary Dynamics of Crassulacean Acid Metabolism |
| title_fullStr | Diversification Slowdown in the Cirrhopetalum Alliance (Bulbophyllum, Orchidaceae): Insights From the Evolutionary Dynamics of Crassulacean Acid Metabolism |
| title_full_unstemmed | Diversification Slowdown in the Cirrhopetalum Alliance (Bulbophyllum, Orchidaceae): Insights From the Evolutionary Dynamics of Crassulacean Acid Metabolism |
| title_short | Diversification Slowdown in the Cirrhopetalum Alliance (Bulbophyllum, Orchidaceae): Insights From the Evolutionary Dynamics of Crassulacean Acid Metabolism |
| title_sort | diversification slowdown in the cirrhopetalum alliance bulbophyllum orchidaceae insights from the evolutionary dynamics of crassulacean acid metabolism |
| topic | CAM diversification slowdown evolutionary dead-end key innovation pCO2 |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.794171/full |
| work_keys_str_mv | AT aiqunhu diversificationslowdowninthecirrhopetalumalliancebulbophyllumorchidaceaeinsightsfromtheevolutionarydynamicsofcrassulaceanacidmetabolism AT aiqunhu diversificationslowdowninthecirrhopetalumalliancebulbophyllumorchidaceaeinsightsfromtheevolutionarydynamicsofcrassulaceanacidmetabolism AT aiqunhu diversificationslowdowninthecirrhopetalumalliancebulbophyllumorchidaceaeinsightsfromtheevolutionarydynamicsofcrassulaceanacidmetabolism AT stephanwgale diversificationslowdowninthecirrhopetalumalliancebulbophyllumorchidaceaeinsightsfromtheevolutionarydynamicsofcrassulaceanacidmetabolism AT zhongjianliu diversificationslowdowninthecirrhopetalumalliancebulbophyllumorchidaceaeinsightsfromtheevolutionarydynamicsofcrassulaceanacidmetabolism AT gunterafischer diversificationslowdowninthecirrhopetalumalliancebulbophyllumorchidaceaeinsightsfromtheevolutionarydynamicsofcrassulaceanacidmetabolism AT richardmksaunders diversificationslowdowninthecirrhopetalumalliancebulbophyllumorchidaceaeinsightsfromtheevolutionarydynamicsofcrassulaceanacidmetabolism |