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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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The five species of sect. Armerina which showed mainly incongruence between the two trees. (a) P. fasciculata with linear and non-pouched bracts, (b) P. fasciculata without bracts, (c) one photo of P. fasciculata collected from populations of clade F2 (see Results), (d) P. tibetica with oblong and pouched bracts at low altitude, (e) and (f) P. tibetica with and without bracts at high altitude, respectively, (g) P. nutans, (h) P. gemmifera, (i) P. conspersa. Bracts for P. fasciculata and P. tibetica are indicated by red arrows. All photos were taken by the first author in the field
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Fig1: The five species of sect. Armerina which showed mainly incongruence between the two trees. (a) P. fasciculata with linear and non-pouched bracts, (b) P. fasciculata without bracts, (c) one photo of P. fasciculata collected from populations of clade F2 (see Results), (d) P. tibetica with oblong and pouched bracts at low altitude, (e) and (f) P. tibetica with and without bracts at high altitude, respectively, (g) P. nutans, (h) P. gemmifera, (i) P. conspersa. Bracts for P. fasciculata and P. tibetica are indicated by red arrows. All photos were taken by the first author in the field

Mentions: In this study, we include several samples per species to investigate the historical biogeography of Primula sect. Armerina Lindley (Primulaceae), which exhibits a typical Sino-Himalayas distribution. According to the most recent global monographic treatment of the genus, Primula sect. Armerina comprises 14 species [26]. Eight species (P. fasciculata, P. tibetica, P. conspersa, P. gemmifera, P. zambalensis, P. pumilio. P. pamirica and P. involucrata; Fig. 1) are endemic to the QTP, with different geographic distributions [26, 27]. Among them, there has been some confusion between P. tibetica and P. fasciculata because of their morphological similarities at high altitude ([26, 27]; field observation). The two species can be easily distinguished when bracts are present. Primula tibetica has oblong and pouched bracts, while the bracts of P. fasciculata are linear and non-pouched (Fig. 1a, d). However, at high altitude, bracts are usually missing in P. fasciculata (Fig. 1b, c), while in P. tibetica, they can also be absent in small individuals with single flower (Fig. 1e, f). Both species have wide altitude distributions, ranging from 2900 m to 5000 m [26, 27] and the use of molecular data combined with macro-evolutionary modeling may provide useful insights into the dynamics of their range evolution. The four remaining species of this section (P. iljinskyii, P. chrysostoma, P. knorringiana and P. valentinae) have very restricted areas in regions adjacent to the QTP. Primula nutans has the most widespread distribution in the section, including N Europe, W & E Siberia, NW America to N Mongolia, NW China and NW QTP. All species from sect. Armerina are considered to be diploid (2n = 18, 20 or 22) [26, 27], except P. egaliksensis, which is the only tetraploid species (2n = 36, 40) and occurs mainly in North America. It was assigned to sect. Armerina based on morphological features [33, 34], and might be of hybrid origin between P. mistassinica (sect. Aleuritia) and P. nutans [35–37].Fig. 1


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)

The five species of sect. Armerina which showed mainly incongruence between the two trees. (a) P. fasciculata with linear and non-pouched bracts, (b) P. fasciculata without bracts, (c) one photo of P. fasciculata collected from populations of clade F2 (see Results), (d) P. tibetica with oblong and pouched bracts at low altitude, (e) and (f) P. tibetica with and without bracts at high altitude, respectively, (g) P. nutans, (h) P. gemmifera, (i) P. conspersa. Bracts for P. fasciculata and P. tibetica are indicated by red arrows. All photos were taken by the first author in the field
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig1: The five species of sect. Armerina which showed mainly incongruence between the two trees. (a) P. fasciculata with linear and non-pouched bracts, (b) P. fasciculata without bracts, (c) one photo of P. fasciculata collected from populations of clade F2 (see Results), (d) P. tibetica with oblong and pouched bracts at low altitude, (e) and (f) P. tibetica with and without bracts at high altitude, respectively, (g) P. nutans, (h) P. gemmifera, (i) P. conspersa. Bracts for P. fasciculata and P. tibetica are indicated by red arrows. All photos were taken by the first author in the field
Mentions: In this study, we include several samples per species to investigate the historical biogeography of Primula sect. Armerina Lindley (Primulaceae), which exhibits a typical Sino-Himalayas distribution. According to the most recent global monographic treatment of the genus, Primula sect. Armerina comprises 14 species [26]. Eight species (P. fasciculata, P. tibetica, P. conspersa, P. gemmifera, P. zambalensis, P. pumilio. P. pamirica and P. involucrata; Fig. 1) are endemic to the QTP, with different geographic distributions [26, 27]. Among them, there has been some confusion between P. tibetica and P. fasciculata because of their morphological similarities at high altitude ([26, 27]; field observation). The two species can be easily distinguished when bracts are present. Primula tibetica has oblong and pouched bracts, while the bracts of P. fasciculata are linear and non-pouched (Fig. 1a, d). However, at high altitude, bracts are usually missing in P. fasciculata (Fig. 1b, c), while in P. tibetica, they can also be absent in small individuals with single flower (Fig. 1e, f). Both species have wide altitude distributions, ranging from 2900 m to 5000 m [26, 27] and the use of molecular data combined with macro-evolutionary modeling may provide useful insights into the dynamics of their range evolution. The four remaining species of this section (P. iljinskyii, P. chrysostoma, P. knorringiana and P. valentinae) have very restricted areas in regions adjacent to the QTP. Primula nutans has the most widespread distribution in the section, including N Europe, W & E Siberia, NW America to N Mongolia, NW China and NW QTP. All species from sect. Armerina are considered to be diploid (2n = 18, 20 or 22) [26, 27], except P. egaliksensis, which is the only tetraploid species (2n = 36, 40) and occurs mainly in North America. It was assigned to sect. Armerina based on morphological features [33, 34], and might be of hybrid origin between P. mistassinica (sect. Aleuritia) and P. nutans [35–37].Fig. 1

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