The Evolution of Trait Disparity during the Radiation of the Plant Genus Macrocarpaea (Gentianaceae) in the Tropical Andes

SIMPLE SUMMARY: The evolutionary radiation of lineages can be caused by several mechanisms. We investigated the evolutionary history of the plant genus Macrocarpaea (Gentianaceae) from the middle elevation montane forests of the Tropical Andes, one of the most species-rich areas of the world. We tested several evolutionary hypotheses based on molecular, morphological and climatic data, using phylogenetic comparative methods. In this paper, we identify the processes dominating the diversification history of Macrocarpaea, especially the M. micrantha clade. ABSTRACT: The evolutionary processes responsible for the extraordinary diversity in the middle elevation montane forests of the Tropical Andes (MMF; 1000–3500 m) remain poorly understood. It is not clear whether adaptive divergence, niche conservatism or geographical processes were the main contributors to the radiation of the respective lineages occurring there. We investigated the evolutionary history of plant lineages in the MMF. We used the vascular plant genus Macrocarpaea (Gentianaceae) as a model, as it consists of 118 morphologically diverse species, a majority of which are endemic to the MMF. We used a time-calibrated molecular phylogeny and morphological and climatic data to compare a set of evolutionary scenarios of various levels of complexity in a phylogenetic comparative framework. In this paper, we show that the hypothesis of adaptive radiation for Macrocarpaea in the MMF is unlikely. The genus remained confined to the upper montane forests (UMF > 1800 m) during more than a half of its evolutionary history, possibly due to evolutionary constraints. Later, coinciding with the beginning of the Pleistocene (around 2.58 Ma), a phylogenetically derived (recently branching) clade, here referred to as the M. micrantha clade (25 species), successfully colonized and radiated in the lower montane forests (LMF < 1800 m). This colonization was accompanied by the evolution of a new leaf phenotype that is unique to the species of the M. micrantha clade that likely represents an adaptation to life in this new environment (adaptive zone). Therefore, our results suggest that niche conservatism and geographical processes have dominated most of the diversification history of Macrocarpaea, but that a rare adaptive divergence event allowed a transition into a new adaptive zone and enabled progressive radiation in this zone through geographical processes.