Pre-adaptation and adaptation shape trait-environment matching in the Neotropics

Aim: Functional traits shape the distribution of taxa across environments. However, it remains unclear whether trait and environmental niche evolution are correlated, and what happened first: trait change facilitating environment shifts (pre-adaptation) or environmental change leading to trait change (adaptation). We focus on a species-rich Neotropical legume radiation to shed light on this enigma. Location: Neotropics. Time Period: Cenozoic. Major Taxa Studied: Fabaceae: Papilionoidae: Swartzia. Methods: We assembled leaflet, fruit and petal size data from monographs and herbarium collections for 86 to 96% of the c. 180 Swartzia species, inferred a dated Swartzia phylogenetic tree from existing DNA sequences covering 38% of the species and integrated these with distribution, soil and climate data. We used phylogenetic linear regression to quantify trait–environment relationships and applied comparative methods to evaluate modes of correlated evolution between traits and environments. Results: Leaflet and petal size were strongly linked to climate, while fruit size was not associated with climate or soil characteristics. Evolutionary transitions to relatively low rainfall and low temperature environments were conditional on the evolution of small leaflets, whereas transitions to wet and warm environments were preceded by the evolution of larger leaflets. In contrast, transitions to the warmest or coldest environments were followed, rather than preceded, by petal loss. Main Conclusion: Our results show that the macroevolution of functional traits has influenced the broad-scale distribution of Swartzia across Neotropical rainforest, seasonally dry, montane and inundated habitats. We suggest that trait evolution is conditional on environmental change but both pre-adaptive and adaptive processes may occur. These processes are important to understand the distribution of diversity at both regional (e.g. Amazonia) and global biogeographical scales.