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

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.

Fig. 1

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

Fig. 2

The maximum clade credibility (MCC) tree derived from BEAST analyses of five chloroplast genes. Maximum likelihood (ML) bootstrap values and Bayesian posterior probabilities (PP) are indicated at major nodes. Bootstrap values ≥ 80 and PP ≥ 0.95 are indicated with thicker branches. Outgroup species are shown in bold

Fig. 3

The maximum clade credibility (MCC) tree derived from MrBayes analyses of the nuclear dataset. Maximum likelihood (ML) bootstrap values and Bayesian posterior probabilities (PP) are indicated at major nodes. Bootstrap values ≥ 80 and PP ≥ 0.95 are indicated with thicker branches. Outgroup species are shown in bold. Two nuclear gene copies for some samples are indicated with “-1” or “-2”

Fig. 4

Dispersal–vicariance scenarios for sect. Armerina and the outgroup speices based on the chloroplast dataset reconstructed by Statistical Dispersal–Vicariance Analysis (S-DIVA) optimization with the maximum number of area units set to two. Triangle: dispersal event; diamond: vicariance event. Letters denoting area units are indicated on the map. Pie charts at internal nodes represent the marginal probabilities for each alternative ancestral area. Alternative ancestral areas (letters on nodes) are indicated for the major nodes. The grey bars on the nodes represent the 95 % highest posterior density intervals of the dates obtained from BEAST analyses. Time scale is shown at the bottom. Three groups (F1, F2 and NT) are used for the evolutionary niche models: groups F1 and F2 are two clades of P. fasciculata in the chloroplast tree; group NT includes all samples of P. tibetica and samples of P. nutans that were only collected from the QTP

Fig. 5

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)