Evolutionary diversification in the hyper-diverse montane forests of the tropical Andes: radiation of Macrocarpaea (Gentianaceae) and the possible role of range expansion

The humid mid-elevation montane forests (MMF) of the tropical Andes harbour high levels of plant species diversity,
contributing to the exceptional overall diversity of the tropical Andean biodiversity hotspot. However, little is known
about the diversification dynamics of MMF plant lineages compared to lineages in other Andean biomes. Here, we
use Macrocarpaea (Gentianaceae) to investigate patterns of plant diversification in the MMF, using molecular dating
with fossils and secondary calibration (from a family-wide phylogenetic analysis of Gentianaceae). We sequenced 76
of 118 recognized Macrocarpaea spp. for six markers to reconstruct a time-calibrated phylogenetic tree and infer
the historical biogeography of Macrocarpaea using maximum-likelihood methods implemented in BioGeoBEARS,
estimating diversification rates through time and among lineages with BAMM. We document a rapid radiation of
Macrocarpaea in Andean MMF coinciding with rapid colonization and range expansion across the entire distribution
of the genus in the Andes starting 7.2 Mya. Our results support allopatric founder-event speciation as the dominant
process contributing to geographical phylogenetic structure across the genus. We propose that establishment of the
MMF in the late Miocene, when the Andes attained critical elevation to modify regional climates, provided large
new areas of suitable habitat for Macrocarpaea to quickly colonize and expand through repeated founder-events.
We suggest that this wave of colonization and range expansion triggered rapid diversification, and, as the MMF
became progressively occupied, the diversification rate slowed. Our study also supports the idea that MMF plant
radiations are older and more slowly evolving than the quickly evolving lineages in the recent Andean high-elevation
grasslands.