The sequential direct and indirect effects of mountain uplift, climatic niche and floral trait evolution on diversification dynamics in an Andean plant clade

Syst Biol. 2024 Mar 30:syae011. doi: 10.1093/sysbio/syae011. Online ahead of print.

Abstract

Why and how organismal lineages radiate is commonly studied through either assessing abiotic factors (biogeography, geomorphological processes, climate) or biotic factors (traits, interactions). Despite increasing awareness that both abiotic and biotic processes may have important joint effects on diversification dynamics, few attempts have been made to quantify the relative importance and timing of these factors, and their potentially interlinked direct and indirect effects, on lineage diversification. We here combine assessments of historical biogeography, geomorphology, climatic niche, vegetative and floral trait evolution to test whether these factors jointly, or in isolation, explain diversification dynamics of a Neotropical plant clade (Merianieae, Melastomataceae). After estimating ancestral areas and the changes in niche and trait disparity over time, we employ Phylogenetic Path Analyses as a synthesis tool to test eleven hypotheses on the individual direct and indirect effects of these factors on diversification rates. We find strongest support for interlinked effects of colonization of the uplifting Andes during the mid-Miocene and rapid abiotic climatic niche evolution in explaining a burst in diversification rate in Merianieae. Within Andean habitats, later increases in floral disparity allowed for the exploitation of wider pollination niches (i.e., shifts from bee to vertebrate pollinators), but did not affect diversification rates. Our approach of including both vegetative and floral trait evolution, rare in assessments of plant diversification in general, highlights that the evolution of woody habit and larger flowers preceded the colonization of the Andes, but was likely critical in enabling the rapid radiation in montane environments. Overall, and in concert with the idea that ecological opportunity is a key element of evolutionary radiations, our results suggest that a combination of rapid niche evolution and trait shifts were critical for the exploitation of newly available niche space in the Andes in the mid-Miocene. Further, our results emphasize the importance of incorporating both abiotic and biotic factors into the same analytical framework if we aim to quantify the relative and interlinked effects of these processes on diversification.

Keywords: Adaptive radiation; Disparity through time; Diversification rates; Ecological opportunity; Historic biogeography; Mountain uplift; Paleoenvironment; Phylogenetic path analysis; Trait evolution.