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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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Fossil-calibrated molecular chronogram of the family Orchidaceae based on combined matK+rbcL sequences.Red circles indicate age-constrained nodes, and arrows indicate the crown ages of the five subfamilies of Orchidaceae.
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pone-0038788-g003: Fossil-calibrated molecular chronogram of the family Orchidaceae based on combined matK+rbcL sequences.Red circles indicate age-constrained nodes, and arrows indicate the crown ages of the five subfamilies of Orchidaceae.

Mentions: The LRT test rejected a clock-like evolution of combined matK+rbcL (δ = 1815.1177, df = 198, P<0.001) and combined six chloroplast genes (δ = 5839.3257, df = 33, P<0.001). Therefore, we used NPRS and PL in r8s and Bayesian methods to estimate the divergence times. The family-level analysis (200 taxa) showed that the crown ages of Orchidaceae and its five subfamilies are older than the estimates by previous studies [40], [42], although the BEAST estimates showed a wide range (Table 3, Fig. 3). It is interesting that the crown ages of the subfamily Cypripedioideae estimated by NPRS and PL in the present study are very close, not as in Ramírez et al. [40] that obtained very different estimates by the two methods. This implys that a good sampling is important for molecular dating. The divergence times within Cypripedioideae estimated from the combined six chloroplast genes are generally congruent with those from the family-level analysis (Table 3). According to the age estimate, the genus Selenipedium originated in Palaeocene, while the most recent common ancestors of conduplicate slipper orchids (Mexipedium, Phragmipedium and Paphiopedilum) and of Cypripedium could be dated back to the Eocene (Table 3, Figs. 3, 4). Since the divergence times estimated with NPRS and PL are very close (Table 3), and thus only the PL estimates were used in the discussion. The ancestral area reconstruction suggests a New World origin or a wide ancestral distribution of slipper orchids, and indicates that vicariance is responsible for the disjunct distribution of conduplicate slipper orchids in palaeotropical and neotropical regions (Fig. 4).


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)

Fossil-calibrated molecular chronogram of the family Orchidaceae based on combined matK+rbcL sequences.Red circles indicate age-constrained nodes, and arrows indicate the crown ages of the five subfamilies of Orchidaceae.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0038788-g003: Fossil-calibrated molecular chronogram of the family Orchidaceae based on combined matK+rbcL sequences.Red circles indicate age-constrained nodes, and arrows indicate the crown ages of the five subfamilies of Orchidaceae.
Mentions: The LRT test rejected a clock-like evolution of combined matK+rbcL (δ = 1815.1177, df = 198, P<0.001) and combined six chloroplast genes (δ = 5839.3257, df = 33, P<0.001). Therefore, we used NPRS and PL in r8s and Bayesian methods to estimate the divergence times. The family-level analysis (200 taxa) showed that the crown ages of Orchidaceae and its five subfamilies are older than the estimates by previous studies [40], [42], although the BEAST estimates showed a wide range (Table 3, Fig. 3). It is interesting that the crown ages of the subfamily Cypripedioideae estimated by NPRS and PL in the present study are very close, not as in Ramírez et al. [40] that obtained very different estimates by the two methods. This implys that a good sampling is important for molecular dating. The divergence times within Cypripedioideae estimated from the combined six chloroplast genes are generally congruent with those from the family-level analysis (Table 3). According to the age estimate, the genus Selenipedium originated in Palaeocene, while the most recent common ancestors of conduplicate slipper orchids (Mexipedium, Phragmipedium and Paphiopedilum) and of Cypripedium could be dated back to the Eocene (Table 3, Figs. 3, 4). Since the divergence times estimated with NPRS and PL are very close (Table 3), and thus only the PL estimates were used in the discussion. The ancestral area reconstruction suggests a New World origin or a wide ancestral distribution of slipper orchids, and indicates that vicariance is responsible for the disjunct distribution of conduplicate slipper orchids in palaeotropical and neotropical regions (Fig. 4).

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