Phylogenetic signatures of ecological divergence and leapfrog adaptive radiation in Espeletia.

ABSTRACT

PREMISE Events of accelerated species diversification represent one of Earth's most celebrated evolutionary outcomes. Northern Andean high-elevation ecosystems, or páramos, host some plant lineages that have experienced the fastest diversification rates, likely triggered by ecological opportunities created by mountain uplifts, local climate shifts, and key trait innovations. However, the mechanisms behind rapid speciation into the new adaptive zone provided by these opportunities have long remained unclear. METHODS: We address this issue by studying the Venezuelan clade of Espeletia, a species-rich group of páramo-endemics showing a dazzling ecological and morphological diversity. We performed several comparative analyses to study both lineage and trait diversification, using an updated molecular phylogeny of this plant group. RESULTS: We showed that sets of either vegetative or reproductive traits have conjointly diversified in Espeletia along different vegetation belts, leading to adaptive syndromes. Diversification in vegetative traits occurred earlier than in reproductive ones. The rate of species and morphological diversification showed a tendency to slow down over time, probably due to diversity dependence. We also found that closely related species exhibit significantly more overlap in their geographic distributions than distantly related taxa, suggesting that most events of ecological divergence occurred at close geographic proximity within páramos. CONCLUSIONS: These results provide compelling support for a scenario of small-scale ecological divergence along multiple ecological niche dimensions, possibly driven by competitive interactions between species, and acting sequentially over time in a leapfrog pattern.