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Phylogeny and biogeography of Primula sect. Armerina: implications for plant evolution under climate change and the uplift of the Qinghai-Tibet Plateau.

Ren G, Conti E, Salamin N - BMC Evol. Biol. (2015)

Bottom Line: However, their effects on dispersal, differentiation and evolution of many groups of plants are still unknown.Our results support the hypothesis that geologic and climatic events play important roles in driving biological diversification of organisms in the QTP area.Armerina.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolution, Biophore, University of Lausanne, 1015, Lausanne, Switzerland. guangpeng.ren@unil.ch.

ABSTRACT

Background: The historical orogenesis and associated climatic changes of mountain areas have been suggested to partly account for the occurrence of high levels of biodiversity and endemism. However, their effects on dispersal, differentiation and evolution of many groups of plants are still unknown. In this study, we examined the detailed diversification history of Primula sect. Armerina, and used biogeographic analysis and macro-evolutionary modeling to investigate a series of different questions concerning the evolution of the geographical and ecological distribution of the species in this section.

Results: We sequenced five chloroplast and one nuclear genes for species of Primula sect. Armerina. Neither chloroplast nor nuclear trees support the monophyly of the section. The major incongruences between the two trees occur among closely related species and may be explained by hybridization. Our dating analyses based on the chloroplast dataset suggest that this section began to diverge from its relatives around 3.55 million years ago, largely coinciding with the last major uplift of the Qinghai-Tibet Plateau (QTP). Biogeographic analysis supports the origin of the section in the Himalayan Mountains and dispersal from the Himalayas to Northeastern QTP, Western QTP and Hengduan Mountains. Furthermore, evolutionary models of ecological niches show that the two P. fasciculata clades have significantly different climatic niche optima and rates of niche evolution, indicating niche evolution under climatic changes and further providing evidence for explaining their biogeographic patterns.

Conclusion: Our results support the hypothesis that geologic and climatic events play important roles in driving biological diversification of organisms in the QTP area. The Pliocene uplift of the QTP and following climatic changes most likely promoted both the inter- and intraspecific divergence of Primula sect. Armerina. This study also illustrates how niche evolution under climatic changes influences biogeographic patterns.

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Parameter estimates of models of niche evolution for the three groups (F1, F2 and NT). For PC1, averaged parameters are obtained based on three supported models (OUM, OUMV and OUMA). The averaged strength of selection (α) estimated across models for the three groups is similar and not shown. For PC2, parameter estimates are from the only supported OUMV model (different rates σ2 and niche optima θ among the three groups)
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Fig5: Parameter estimates of models of niche evolution for the three groups (F1, F2 and NT). For PC1, averaged parameters are obtained based on three supported models (OUM, OUMV and OUMA). The averaged strength of selection (α) estimated across models for the three groups is similar and not shown. For PC2, parameter estimates are from the only supported OUMV model (different rates σ2 and niche optima θ among the three groups)

Mentions: The parameters (niche optimum θ, rate of niche evolution σ2 and strength of selection α) estimated for the three species groups (F1, F2 and NT) from all supported models based on the four group sets were congruent (Additional file 4) and we showed the parameters estimated based on SET2 (Fig. 5). We used model averaging to estimate the parameter values for PC1 over the supported models OUMV, OUMA and OUM. The averaged niche optima (θ) across models for group F1, F2 and NT were −0.17, −2.0 and 0.55, respectively (Fig. 5). The averaged rate parameter (σ2) across models for group F2 was two times slower than that for the groups F1 and NT (59 vs. 131 and 112). Finally, the averaged strength of selection estimated across models for the three groups was similar (6.9, 6.3, 6.9). For PC2, model OUMV, which allows for different niche optima and rates of niche evolution among groups, was the only supported model. The optimum values estimated based on this model for the three groups were also different from each other (F1: 0.2, F2: −0.99, NT: −0.33). The group F2 still exhibited the slowest rate of niche evolution (F1: 228, F2: 94, NT: 1723; Fig. 5).Fig. 5


Phylogeny and biogeography of Primula sect. Armerina: implications for plant evolution under climate change and the uplift of the Qinghai-Tibet Plateau.

Ren G, Conti E, Salamin N - BMC Evol. Biol. (2015)

Parameter estimates of models of niche evolution for the three groups (F1, F2 and NT). For PC1, averaged parameters are obtained based on three supported models (OUM, OUMV and OUMA). The averaged strength of selection (α) estimated across models for the three groups is similar and not shown. For PC2, parameter estimates are from the only supported OUMV model (different rates σ2 and niche optima θ among the three groups)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4537560&req=5

Fig5: Parameter estimates of models of niche evolution for the three groups (F1, F2 and NT). For PC1, averaged parameters are obtained based on three supported models (OUM, OUMV and OUMA). The averaged strength of selection (α) estimated across models for the three groups is similar and not shown. For PC2, parameter estimates are from the only supported OUMV model (different rates σ2 and niche optima θ among the three groups)
Mentions: The parameters (niche optimum θ, rate of niche evolution σ2 and strength of selection α) estimated for the three species groups (F1, F2 and NT) from all supported models based on the four group sets were congruent (Additional file 4) and we showed the parameters estimated based on SET2 (Fig. 5). We used model averaging to estimate the parameter values for PC1 over the supported models OUMV, OUMA and OUM. The averaged niche optima (θ) across models for group F1, F2 and NT were −0.17, −2.0 and 0.55, respectively (Fig. 5). The averaged rate parameter (σ2) across models for group F2 was two times slower than that for the groups F1 and NT (59 vs. 131 and 112). Finally, the averaged strength of selection estimated across models for the three groups was similar (6.9, 6.3, 6.9). For PC2, model OUMV, which allows for different niche optima and rates of niche evolution among groups, was the only supported model. The optimum values estimated based on this model for the three groups were also different from each other (F1: 0.2, F2: −0.99, NT: −0.33). The group F2 still exhibited the slowest rate of niche evolution (F1: 228, F2: 94, NT: 1723; Fig. 5).Fig. 5

Bottom Line: However, their effects on dispersal, differentiation and evolution of many groups of plants are still unknown.Our results support the hypothesis that geologic and climatic events play important roles in driving biological diversification of organisms in the QTP area.Armerina.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolution, Biophore, University of Lausanne, 1015, Lausanne, Switzerland. guangpeng.ren@unil.ch.

ABSTRACT

Background: The historical orogenesis and associated climatic changes of mountain areas have been suggested to partly account for the occurrence of high levels of biodiversity and endemism. However, their effects on dispersal, differentiation and evolution of many groups of plants are still unknown. In this study, we examined the detailed diversification history of Primula sect. Armerina, and used biogeographic analysis and macro-evolutionary modeling to investigate a series of different questions concerning the evolution of the geographical and ecological distribution of the species in this section.

Results: We sequenced five chloroplast and one nuclear genes for species of Primula sect. Armerina. Neither chloroplast nor nuclear trees support the monophyly of the section. The major incongruences between the two trees occur among closely related species and may be explained by hybridization. Our dating analyses based on the chloroplast dataset suggest that this section began to diverge from its relatives around 3.55 million years ago, largely coinciding with the last major uplift of the Qinghai-Tibet Plateau (QTP). Biogeographic analysis supports the origin of the section in the Himalayan Mountains and dispersal from the Himalayas to Northeastern QTP, Western QTP and Hengduan Mountains. Furthermore, evolutionary models of ecological niches show that the two P. fasciculata clades have significantly different climatic niche optima and rates of niche evolution, indicating niche evolution under climatic changes and further providing evidence for explaining their biogeographic patterns.

Conclusion: Our results support the hypothesis that geologic and climatic events play important roles in driving biological diversification of organisms in the QTP area. The Pliocene uplift of the QTP and following climatic changes most likely promoted both the inter- and intraspecific divergence of Primula sect. Armerina. This study also illustrates how niche evolution under climatic changes influences biogeographic patterns.

Show MeSH