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Evolution and biogeography of the slipper orchids: Eocene vicariance of the conduplicate genera in the Old and New World Tropics.

Guo YY, Luo YB, Liu ZJ, Wang XQ - PLoS ONE (2012)

Bottom Line: We found that the genus Cypripedium with a wide distribution in the northern temperate and subtropical zones diverged first, followed by Selenipedium endemic to South America, and finally conduplicate-leaved genera in the Tropics.Our study sheds some light on mechanisms underlying generic and species diversification in the orchid family and tropical disjunctions of herbaceous plant groups.In addition, we suggest that the biogeographical study should sample both regional endemics and their widespread relatives.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, the Chinese Academy of Sciences, Beijing, China.

ABSTRACT
Intercontinental disjunctions between tropical regions, which harbor two-thirds of the flowering plants, have drawn great interest from biologists and biogeographers. Most previous studies on these distribution patterns focused on woody plants, and paid little attention to herbs. The Orchidaceae is one of the largest families of angiosperms, with a herbaceous habit and a high species diversity in the Tropics. Here we investigate the evolutionary and biogeographical history of the slipper orchids, which represents a monophyletic subfamily (Cypripedioideae) of the orchid family and comprises five genera that are disjunctly distributed in tropical to temperate regions. A relatively well-resolved and highly supported phylogeny of slipper orchids was reconstructed based on sequence analyses of six maternally inherited chloroplast and two low-copy nuclear genes (LFY and ACO). We found that the genus Cypripedium with a wide distribution in the northern temperate and subtropical zones diverged first, followed by Selenipedium endemic to South America, and finally conduplicate-leaved genera in the Tropics. Mexipedium and Phragmipedium from the neotropics are most closely related, and form a clade sister to Paphiopedilum from tropical Asia. According to molecular clock estimates, the genus Selenipedium originated in Palaeocene, while the most recent common ancestor of conduplicate-leaved slipper orchids could be dated back to the Eocene. Ancestral area reconstruction indicates that vicariance is responsible for the disjunct distribution of conduplicate slipper orchids in palaeotropical and neotropical regions. Our study sheds some light on mechanisms underlying generic and species diversification in the orchid family and tropical disjunctions of herbaceous plant groups. In addition, we suggest that the biogeographical study should sample both regional endemics and their widespread relatives.

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The distribution of slipper orchids modified from Pridgeon et al. [165].Shaded areas show the current species distribution, with different colors to represent the five genera. The tree topology indicates the phylogenetic relationships of slipper orchids reconstructed in this study.
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pone-0038788-g001: The distribution of slipper orchids modified from Pridgeon et al. [165].Shaded areas show the current species distribution, with different colors to represent the five genera. The tree topology indicates the phylogenetic relationships of slipper orchids reconstructed in this study.

Mentions: The slipper orchids are widely distributed in temperate to tropical regions of Eurasia and America. The genus Cypripedium occurs in temperate and subtropical areas of the North Hemisphere, with some species extending to tropical North America. The two conduplicate-leaved genera Mexipedium and Phragmipedium and the plicate-leaved genus Selenipedium are restricted to the neotropics, whereas Paphiopedilum is confined to the palaeotropics (Fig. 1). Atwood [62] and Albert [63] supported the boreotropical hypothesis [66], and considered that fragmentation of continents and the following climatic cooling in the Ice Ages caused the present disjunct distribution of slipper orchids. While the ITS analysis supports southern North America/Mesoamerica as the origin center of slipper orchids [64], the sister relationship between Mexipedium and Paphiopedilum revealed in the low copy nuclear Xdh gene phylogeny [48], although with weak support and based on a limited sampling, seems to suggest a long distance dispersal from palaeotropical to neotropical regions. Therefore, the biogeographical history of slipper orchids is far from being resolved.


Evolution and biogeography of the slipper orchids: Eocene vicariance of the conduplicate genera in the Old and New World Tropics.

Guo YY, Luo YB, Liu ZJ, Wang XQ - PLoS ONE (2012)

The distribution of slipper orchids modified from Pridgeon et al. [165].Shaded areas show the current species distribution, with different colors to represent the five genera. The tree topology indicates the phylogenetic relationships of slipper orchids reconstructed in this study.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3369861&req=5

pone-0038788-g001: The distribution of slipper orchids modified from Pridgeon et al. [165].Shaded areas show the current species distribution, with different colors to represent the five genera. The tree topology indicates the phylogenetic relationships of slipper orchids reconstructed in this study.
Mentions: The slipper orchids are widely distributed in temperate to tropical regions of Eurasia and America. The genus Cypripedium occurs in temperate and subtropical areas of the North Hemisphere, with some species extending to tropical North America. The two conduplicate-leaved genera Mexipedium and Phragmipedium and the plicate-leaved genus Selenipedium are restricted to the neotropics, whereas Paphiopedilum is confined to the palaeotropics (Fig. 1). Atwood [62] and Albert [63] supported the boreotropical hypothesis [66], and considered that fragmentation of continents and the following climatic cooling in the Ice Ages caused the present disjunct distribution of slipper orchids. While the ITS analysis supports southern North America/Mesoamerica as the origin center of slipper orchids [64], the sister relationship between Mexipedium and Paphiopedilum revealed in the low copy nuclear Xdh gene phylogeny [48], although with weak support and based on a limited sampling, seems to suggest a long distance dispersal from palaeotropical to neotropical regions. Therefore, the biogeographical history of slipper orchids is far from being resolved.

Bottom Line: We found that the genus Cypripedium with a wide distribution in the northern temperate and subtropical zones diverged first, followed by Selenipedium endemic to South America, and finally conduplicate-leaved genera in the Tropics.Our study sheds some light on mechanisms underlying generic and species diversification in the orchid family and tropical disjunctions of herbaceous plant groups.In addition, we suggest that the biogeographical study should sample both regional endemics and their widespread relatives.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, the Chinese Academy of Sciences, Beijing, China.

ABSTRACT
Intercontinental disjunctions between tropical regions, which harbor two-thirds of the flowering plants, have drawn great interest from biologists and biogeographers. Most previous studies on these distribution patterns focused on woody plants, and paid little attention to herbs. The Orchidaceae is one of the largest families of angiosperms, with a herbaceous habit and a high species diversity in the Tropics. Here we investigate the evolutionary and biogeographical history of the slipper orchids, which represents a monophyletic subfamily (Cypripedioideae) of the orchid family and comprises five genera that are disjunctly distributed in tropical to temperate regions. A relatively well-resolved and highly supported phylogeny of slipper orchids was reconstructed based on sequence analyses of six maternally inherited chloroplast and two low-copy nuclear genes (LFY and ACO). We found that the genus Cypripedium with a wide distribution in the northern temperate and subtropical zones diverged first, followed by Selenipedium endemic to South America, and finally conduplicate-leaved genera in the Tropics. Mexipedium and Phragmipedium from the neotropics are most closely related, and form a clade sister to Paphiopedilum from tropical Asia. According to molecular clock estimates, the genus Selenipedium originated in Palaeocene, while the most recent common ancestor of conduplicate-leaved slipper orchids could be dated back to the Eocene. Ancestral area reconstruction indicates that vicariance is responsible for the disjunct distribution of conduplicate slipper orchids in palaeotropical and neotropical regions. Our study sheds some light on mechanisms underlying generic and species diversification in the orchid family and tropical disjunctions of herbaceous plant groups. In addition, we suggest that the biogeographical study should sample both regional endemics and their widespread relatives.

Show MeSH