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.

Automated summary

The study investigates the diversification patterns of the Macrocarpaea plant lineage in the humid mid-elevation montane forests of the tropical Andes, revealing a rapid radiation and range expansion primarily driven by allopatric founder-event speciation. This rapid diversification is suggested to have been triggered by the establishment of suitable habitats in the late Miocene, leading to colonization and expansion through repeated founder-events. The study also indicates that the diversification rate slowed as the montane forests became progressively occupied, supporting the notion that plant radiations in these forests are older and more slowly evolving compared to lineages in high-elevation grasslands in the recent Andean region.