Out‐of‐Tibet: the spatio‐temporal evolution of Gentiana (Gentianaceae)

Abstract

Aim We investigated the historical biogeography and diversification of Gentiana L. (Gentianaceae). Our study depicts the origin and dispersal routes of this alpine genus, and the role of the uplift of the Qinghai–Tibet Plateau (QTP) and past climate changes as triggers for its diversification. Location Tibeto‐Himalayan region and world‐wide mountain habitats. Methods Our sampling represents more than 50% of the extant Gentiana species, including all sections across their entire geographical ranges. We investigated the evolutionary history of Gentiana using phylogenetic reconstructions (maximum likelihood and Bayesian inference) of ITS, atpB–rbcL and trnL–trnF sequences, as well as molecular dating with beast. We tested two approaches of ancestral area reconstructions (DEC, DIVA) in BioGeoBEARS and investigated diversification rates using BAMM. Results The common ancestor of Gentiana and subtribe Gentianinae lived in the QTP region at around 34 (25–45) million years ago (Ma), and 40 (29–52) Ma respectively. From the surroundings of the QTP, Gentiana lineages dispersed to eastern China, Taiwan, Europe, North and South America, Australia and New Guinea, from mid‐Miocene onward (c. 15 Ma–present), with only one older dispersal event to Europe (c. 37–21 Ma). Diversification rates gradually increased over time, and two switches of diversification rates were identified in Gentianinae (c. 7 Ma, simultaneously in the Pneumonanthe/Cruciata lineage and in Tripterospermum). Main conclusions Gentiana existed in the QTP region throughout most of its uplift history following the India‐Asia collision. This region acted as the primary source area for dispersals to many areas of the world. Because steady increase in diversification rates coincides with the extension of the QTP, we argue that the museum theory rather than the explosive radiation theory prevails for gentians in this region, although rare shifts of diversification rates are associated with niche shifts across the alpine/subalpine ecotone.

Testing multiple hypotheses for the high endemic plant diversity of the Tibetan Plateau

“…The additional time for speciation and the accumulation and persistence of lineages after the early Neogene ( c. 20 Ma) would explain the currently observed patterns. This is consistent with the montane museum hypothesis, which explained the greatest amount of variation in our analysis and has prior support in the TP (Favre et al, ; Li et al, ) and other montane regions (e.g., Hutter, Guayasamin, & Wiens, ).…”

“…Based on lineage divergence times of (sub‐)alpine plants in the TP, there is a general consensus that the diversification of genera occurred mainly during the rapid and extensive uplift of the Neogene period (e.g., Saxifraga , Ebersbach et al, ; Gentiana , Favre et al, ; Rhodiola , Zhang, Meng, Allen, Wen, & Rao, ). At the species level, however, the divergence of main clades happened largely during the late Pliocene and Pleistocene (e.g., Pomatosace filicula , Wang, He, Miehe, & Mao, ; Bupleurum smithii , Zhao, Ma, Liang, Wang, & He, ).…”

The grass subfamily Pooideae: Cretaceous–Palaeocene origin and climate‐driven Cenozoic diversification

“…Nevertheless, our reconstruction of ancestral niches (based on bioclimatic variables) indicates that ancestors of all major Pooideae lineages experienced and could withstand frosts and mild winters in a seasonal climate (Figures and b–d). Thus, we hypothesize that Pooideae were adapted to temperate‐like climates long before the expansion of temperate biomes, contrary to many other temperate plant lineages (Favre et al, ; Kerkhoff et al, ; Meseguer et al, , ). This hypothesis is supported by two recent studies.…”

“…Pooideae might not be unique in this regard. Several radiations after the appearance of temperate biomes have been identified in other plant groups (Favre et al, ; Meseguer et al, ). The temperature‐dependent model was not significantly better than a constant birth–death diversification model based on the analysis of the posterior sample of trees.…”

“…Many temperate‐adapted lineages evolved around and after the Eocene–Oligocene (E–O) transition, c . 34 Ma, along with the expansion of cold temperate biomes, especially in the Northern Hemisphere (Favre et al, ; Kerkhoff, Moriarty, & Weiser, ; Marcussen, Heier, Brysting, Oxelman, & Jakobsen, ; Meseguer et al, ; Meseguer, Lobo, Ree, Beerling, & Sanmartín, ; Near et al, ). The concurrence of the E–O transition and diversification into temperate climates suggests that global cooling c .…”