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

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 disparification over time in climate and trait space, 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 disparification in floral trait space 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 important pre-adaptations to mountain colonization, specifically woody habit and larger flowers. 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 pre-adapted traits 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.

Methods
phylogenetic hypothesis for Merianieae stems from Reginato et al. 2022 (https://doi.org/10.1007/978-3-030-99742-7_4) and was pruned to 139 species for which we could score floral trait data

floral trait data stems from Dellinger et al. 2021 (https://doi.org/10.1111/nph.17390)

vegetative trait data (growth form, leaf area, leaf thickness, leaf margin) was collected for this study from herbarium specimens and descriptions

climatic niche data was collected by extracting bioclimatic variables (from Chelsa v2) at carefully pruned gbif occurrence records all analyses are based on these four basic datasets; for several phylogenetic analyses, we used scores from morphospace analyses and diversification estimates, all of which can be obtained through the R scripts we have provided on Zenodo

the only other software you will need if you want to obtain initial diversification rates for Merianieae (which we have provided as .csv which you can readily open in R) is BAMM, which you will need to run through your computer's command line as specified here: http://bamm-project.org/