Phylogenomic and macroevolutionary evidence for an explosive radiation of a plant genus in the Miocene

Mountain systems harbor a substantial fraction of global biodiversity and,
thus, provide excellent opportunities to study rapid diversification and
to understand the historical processes underlying the assembly of
biodiversity hotspots. The rich biodiversity in mountains is widely
regarded as having arisen under the influence of geological and climatic
processes as well as the complex interactions among them. However, the
relative contribution of geology and climate in driving species radiation
is seldom explored. Here, we studied the evolutionary radiation of
Oreocharis (Gesneriaceae), which has diversified extensively throughout
East Asia, especially within the Hengduan Mountains (HDM), using
transcriptomic data and a time calibrated phylogeny for 88% (111/126) of
all species of the genus. In particular, we applied phylogenetic
reconstructions to evaluate the extent of incomplete lineage sorting
accompanying the early and rapid radiation in the genus. We then fit
macroevolutionary models to explore its spatial and diversification
dynamics in Oreocharis and applied explicit birth-death models to
investigate the effects of past environmental changes on its
diversification. Evidence from 574 orthologous loci suggest that
Oreocharis underwent an impressive early burst of speciation starting ca.
12 Ma in the Miocene, followed by a drastic decline in speciation toward
the present. Although we found no evidence for a shift in diversification
rate across the phylogeny of Oreocharis, we showed a difference in
diversification dynamics between the HDM and non-HDM lineages, with higher
diversification rates in the HDM. The diversification dynamic of
Oreocharis is most likely positively associated with temperature-dependent
speciation and dependency on the Asian monsoons. We suggest that the warm
and humid climate of the mid-Miocene was probably the primary driver of
the rapid diversification in Oreocharis, while mountain building of the
HDM might have indirectly affected species diversification of the HDM
lineage. This study highlights the importance of past climatic changes,
combined with mountain building, in creating strong environmental
heterogeneity and driving diversification of mountain plants, and suggests
that the biodiversity in the HDM cannot directly be attributed to mountain
uplift, contrary to many recent speculations.