Orchid phylogenomics and multiple drivers of their extraordinary diversification
Orchids are the most diverse family of angiosperms, with over 25 000 species, more than mammals, birds and reptiles combined. Tests of hypotheses to account for such diversity have been stymied by the lack of a fully resolved broad-scale phylogeny. Here, we provide such a phylogeny, based on 75 chlo...
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| Published in | Proceedings of the Royal Society. B, Biological sciences Vol. 282; no. 1814; p. 20151553 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
The Royal Society
07.09.2015
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Orchids are the most diverse family of angiosperms, with over 25 000 species, more than mammals, birds and reptiles combined. Tests of hypotheses to account for such diversity have been stymied by the lack of a fully resolved broad-scale phylogeny. Here, we provide such a phylogeny, based on 75 chloroplast genes for 39 species representing all orchid subfamilies and 16 of 17 tribes, time-calibrated against 17 angiosperm fossils. A supermatrix analysis places an additional 144 species based on three plastid genes. Orchids appear to have arisen roughly 112 million years ago (Mya); the subfamilies Orchidoideae and Epidendroideae diverged from each other at the end of the Cretaceous; and the eight tribes and three previously unplaced subtribes of the upper epidendroids diverged rapidly from each other between 37.9 and 30.8 Mya. Orchids appear to have undergone one significant acceleration of net species diversification in the orchidoids, and two accelerations and one deceleration in the upper epidendroids. Consistent with theory, such accelerations were correlated with the evolution of pollinia, the epiphytic habit, CAM photosynthesis, tropical distribution (especially in extensive cordilleras), and pollination via Lepidoptera or euglossine bees. Deceit pollination appears to have elevated the number of orchid species by one-half but not via acceleration of the rate of net diversification. The highest rate of net species diversification within the orchids (0.382 sp sp−1 My−1) is 6.8 times that at the Asparagales crown. |
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| AbstractList | Orchids are the most diverse family of angiosperms, with over 25 000 species, more than mammals, birds and reptiles combined. Tests of hypotheses to account for such diversity have been stymied by the lack of a fully resolved broad-scale phylogeny. Here, we provide such a phylogeny, based on 75 chloroplast genes for 39 species representing all orchid subfamilies and 16 of 17 tribes, time-calibrated against 17 angiosperm fossils. A supermatrix analysis places an additional 144 species based on three plastid genes. Orchids appear to have arisen roughly 112 million years ago (Mya); the subfamilies Orchidoideae and Epidendroideae diverged from each other at the end of the Cretaceous; and the eight tribes and three previously unplaced subtribes of the upper epidendroids diverged rapidly from each other between 37.9 and 30.8 Mya. Orchids appear to have undergone one significant acceleration of net species diversification in the orchidoids, and two accelerations and one deceleration in the upper epidendroids. Consistent with theory, such accelerations were correlated with the evolution of pollinia, the epiphytic habit, CAM photosynthesis, tropical distribution (especially in extensive cordilleras), and pollination via Lepidoptera or euglossine bees. Deceit pollination appears to have elevated the number of orchid species by one-half but not via acceleration of the rate of net diversification. The highest rate of net species diversification within the orchids (0.382 sp sp
−1
My
−1
) is 6.8 times that at the Asparagales crown. Orchids are the most diverse family of angiosperms, with over 25 000 species, more than mammals, birds and reptiles combined. Tests of hypotheses to account for such diversity have been stymied by the lack of a fully resolved broad-scale phylogeny. Here, we provide such a phylogeny, based on 75 chloroplast genes for 39 species representing all orchid subfamilies and 16 of 17 tribes, time-calibrated against 17 angiosperm fossils. A supermatrix analysis places an additional 144 species based on three plastid genes. Orchids appear to have arisen roughly 112 million years ago (Mya); the subfamilies Orchidoideae and Epidendroideae diverged from each other at the end of the Cretaceous; and the eight tribes and three previously unplaced subtribes of the upper epidendroids diverged rapidly from each other between 37.9 and 30.8 Mya. Orchids appear to have undergone one significant acceleration of net species diversification in the orchidoids, and two accelerations and one deceleration in the upper epidendroids. Consistent with theory, such accelerations were correlated with the evolution of pollinia, the epiphytic habit, CAM photosynthesis, tropical distribution (especially in extensive cordilleras), and pollination via Lepidoptera or euglossine bees. Deceit pollination appears to have elevated the number of orchid species by one-half but not via acceleration of the rate of net diversification. The highest rate of net species diversification within the orchids (0.382 sp sp−1 My−1) is 6.8 times that at the Asparagales crown. Orchids are the most diverse family of angiosperms, with over 25 000 species, more than mammals, birds and reptiles combined. Tests of hypotheses to account for such diversity have been stymied by the lack of a fully resolved broad-scale phylogeny. Here, we provide such a phylogeny, based on 75 chloroplast genes for 39 species representing all orchid subfamilies and 16 of 17 tribes, time-calibrated against 17 angiosperm fossils. A supermatrix analysis places an additional 144 species based on three plastid genes. Orchids appear to have arisen roughly 112 million years ago (Mya); the subfamilies Orchidoideae and Epidendroideae diverged from each other at the end of the Cretaceous; and the eight tribes and three previously unplaced subtribes of the upper epidendroids diverged rapidly from each other between 37.9 and 30.8 Mya. Orchids appear to have undergone one significant acceleration of net species diversification in the orchidoids, and two accelerations and one deceleration in the upper epidendroids. Consistent with theory, such accelerations were correlated with the evolution of pollinia, the epiphytic habit, CAM photosynthesis, tropical distribution (especially in extensive cordilleras), and pollination via Lepidoptera or euglossine bees. Deceit pollination appears to have elevated the number of orchid species by one-half but not via acceleration of the rate of net diversification. The highest rate of net species diversification within the orchids (0.382 sp sp-1 My-1) is 6.8 times that at the Asparagales crown. Orchids are the most diverse family of angiosperms, with over 25 000 species,more than mammals, birds and reptiles combined. Tests of hypotheses to account for such diversity have been stymied by the lack of a fully resolved broad-scale phylogeny. Here,we provide such a phylogeny, based on 75 chloroplast genes for 39 species representing all orchid subfamilies and 16 of 17 tribes, time-calibrated against 17 angiosperm fossils. Asupermatrix analysis places an additional 144 species based on three plastid genes. Orchids appear to have arisen roughly 112 million years ago (Mya); the subfamilies Orchidoideae and Epidendroideae diverged from each other at the end of the Cretaceous; and the eight tribes and three previously unplaced subtribes of the upper epidendroids diverged rapidly from each other between 37.9 and 30.8 Mya. Orchids appear to have undergone one significant acceleration of net species diversification in the orchidoids, and two accelerations and one deceleration in the upper epidendroids. Consistent with theory, such accelerations were correlated with the evolution of pollinia, the epiphytic habit, CAM photosynthesis, tropical distribution (especially in extensive cordilleras),and pollination via Lepidoptera or euglossine bees. Deceit pollination appears to have elevated the number of orchid species by one-half but not via acceleration of the rate of net diversification. The highest rate of net species diversification within the orchids (0.382 sp sp(-1) My(-1)) is 6.8 times that at the Asparagales crown. |
| Author | Whitten, W. Mark Iles, William J. D. Williams, Norris H. Givnish, Thomas J. Leebens-Mack, James Kriebel, Ricardo Neubig, Kurt M. Arroyo, Mary T. K. Endara, Lorena Ames, Mercedes Zuluaga, Alejandro Hunter, Steven J. Spalink, Daniel Clements, Mark A. Cameron, Kenneth M. Lyon, Stephanie P. |
| AuthorAffiliation | 4 Institute of Ecology and Biodiversity, Facultad de Ciencias , Universidad de Chile , Santiago , Chile 1 Department of Botany , University of Wisconsin—Madison , Madison, WI 53706 , USA 6 Department of Biology , University of Florida , Gainesville, FL 32611 , USA 2 University and Jepson Herbaria, University of California—Berkeley , Berkeley, CA 94720 , USA 3 Centre for Australian National Biodiversity Research , Canberra, Australian Capital Territory 2601 , Australia 7 Florida Museum of Natural History , University of Florida , Gainesville, FL 32611 , USA 8 Department of Biology , Southern Illinois University at Carbondale , Carbondale, IL 62901 , USA 5 Department of Plant Biology , University of Georgia , Athens, GA 30602 , USA |
| AuthorAffiliation_xml | – name: 8 Department of Biology , Southern Illinois University at Carbondale , Carbondale, IL 62901 , USA – name: 4 Institute of Ecology and Biodiversity, Facultad de Ciencias , Universidad de Chile , Santiago , Chile – name: 7 Florida Museum of Natural History , University of Florida , Gainesville, FL 32611 , USA – name: 3 Centre for Australian National Biodiversity Research , Canberra, Australian Capital Territory 2601 , Australia – name: 2 University and Jepson Herbaria, University of California—Berkeley , Berkeley, CA 94720 , USA – name: 5 Department of Plant Biology , University of Georgia , Athens, GA 30602 , USA – name: 1 Department of Botany , University of Wisconsin—Madison , Madison, WI 53706 , USA – name: 6 Department of Biology , University of Florida , Gainesville, FL 32611 , USA |
| Author_xml | – sequence: 1 givenname: Thomas J. surname: Givnish fullname: Givnish, Thomas J. email: givnish@wisc.edu organization: Department of Botany, University of Wisconsin—Madison, Madison, WI 53706, USA – sequence: 2 givenname: Daniel surname: Spalink fullname: Spalink, Daniel organization: Department of Botany, University of Wisconsin—Madison, Madison, WI 53706, USA – sequence: 3 givenname: Mercedes surname: Ames fullname: Ames, Mercedes organization: Department of Botany, University of Wisconsin—Madison, Madison, WI 53706, USA – sequence: 4 givenname: Stephanie P. surname: Lyon fullname: Lyon, Stephanie P. organization: Department of Botany, University of Wisconsin—Madison, Madison, WI 53706, USA – sequence: 5 givenname: Steven J. surname: Hunter fullname: Hunter, Steven J. organization: Department of Botany, University of Wisconsin—Madison, Madison, WI 53706, USA – sequence: 6 givenname: Alejandro surname: Zuluaga fullname: Zuluaga, Alejandro organization: Department of Botany, University of Wisconsin—Madison, Madison, WI 53706, USA – sequence: 7 givenname: William J. D. surname: Iles fullname: Iles, William J. D. organization: University and Jepson Herbaria, University of California—Berkeley, Berkeley, CA 94720, USA – sequence: 8 givenname: Mark A. surname: Clements fullname: Clements, Mark A. organization: Centre for Australian National Biodiversity Research, Canberra, Australian Capital Territory 2601, Australia – sequence: 9 givenname: Mary T. K. surname: Arroyo fullname: Arroyo, Mary T. K. organization: Institute of Ecology and Biodiversity, Facultad de Ciencias, Universidad de Chile, Santiago, Chile – sequence: 10 givenname: James surname: Leebens-Mack fullname: Leebens-Mack, James organization: Department of Plant Biology, University of Georgia, Athens, GA 30602, USA – sequence: 11 givenname: Lorena surname: Endara fullname: Endara, Lorena organization: Department of Biology, University of Florida, Gainesville, FL 32611, USA – sequence: 12 givenname: Ricardo surname: Kriebel fullname: Kriebel, Ricardo organization: Department of Botany, University of Wisconsin—Madison, Madison, WI 53706, USA – sequence: 13 givenname: Kurt M. surname: Neubig fullname: Neubig, Kurt M. organization: Department of Biology, Southern Illinois University at Carbondale, Carbondale, IL 62901, USA – sequence: 14 givenname: W. Mark surname: Whitten fullname: Whitten, W. Mark organization: Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA – sequence: 15 givenname: Norris H. surname: Williams fullname: Williams, Norris H. organization: Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA – sequence: 16 givenname: Kenneth M. surname: Cameron fullname: Cameron, Kenneth M. organization: Department of Botany, University of Wisconsin—Madison, Madison, WI 53706, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26311671$$D View this record in MEDLINE/PubMed |
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| Snippet | Orchids are the most diverse family of angiosperms, with over 25 000 species, more than mammals, birds and reptiles combined. Tests of hypotheses to account... Orchids are the most diverse family of angiosperms, with over 25 000 species,more than mammals, birds and reptiles combined. Tests of hypotheses to account for... |
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| SubjectTerms | Andes Animals Bamm Bees Biological Evolution Bisse Chloroplasts - genetics Deception Genome, Plant Lepidoptera New Guinea Highlands Orchidaceae Orchidaceae - classification Orchidaceae - genetics Photosynthesis Phylogeny Pleurothallidinae Pollination - genetics Speciation Time Factors |
| Title | Orchid phylogenomics and multiple drivers of their extraordinary diversification |
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