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

Julien C Vieu,Darina Koubínová,Jason R Grant

doi:10.3390/biology10090825

Abstract

Simple SummaryThe 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.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.

Highlights

Understanding the evolutionary mechanisms responsible for the fact that some lineages are more species-rich than others is a fundamental aim of the research in evolutionary biology
Based on the traits investigated in this study, we found that it is unlikely that the radiation of Macrocarpaea in the Andes was associated with niche partitioning
We showed that it is unlikely that adaptive divergence fostered the main radiation of Macrocarpaea in the MMF

Summary

Introduction

Understanding the evolutionary mechanisms responsible for the fact that some lineages are more species-rich than others is a fundamental aim of the research in evolutionary biology. The ecological theory of adaptive radiation estimates that ecological opportunity is a primary factor regulating the tempo of lineage diversification [1]. Ecological opportunity can be perceived as the availability of under-exploited resources that can arise from the extinction of competitors, dispersal into new habitats or acquisition of a key innovation that allows organisms to explore new ecological niches [2,3]. During the phase of niche exploration, divergent selection is thought to promote bursts of species divergence (diversification), together with a rapid accumulation of phenotypic diversity (disparification [4]). Classical examples of adaptive radiations often involve organisms located on islands or island-like habitats (i.e., lake and mountaintops), such as Galapagos Darwin’s finches in the Galapagos Islands [6]; the Caribbean Anolis Daudin, 1802 lizards [7]; or the African rift lake cichlid fishes [8]; or even plants such as the Hawaiian silverswords [9]. More recently, cases of adaptive radiations on continents, e.g., in the vertebrates in North America, Neotropics or in the oceans, have been documented [10,11,12]

Methods

Results

Discussion

Conclusion