Rampant convergent evolution of vascular oddities and a synnovation characterize the rapid radiation of Paullinieae lianas
Abstract
Climbing plants have independently evolved thousands of times and are particularly successful in tropical forests, yet their anatomical and evolutionary distinctiveness remains poorly understood. Among the most striking innovations in woody climbers—or “lianas”—are vascular variants: modifications to xylem and phloem that depart from the typical growth found in trees and shrubs. In this work, we leverage the fourth largest lineage of neotropical lianas, Paullinieae (Sapindaceae), to elucidate the evolution of development of vascular variants, and to test key innovation hypotheses in this megadiverse group. We reconstruct the largest phylogeny of any liana lineage to date (227 species, 351 nuclear genes), revealing a rapid radiation in the Miocene. Our anatomical evaluation of 462 species uncovered six patterns of vascular variants spanning three developmental categories—procambial, cambial, and ectopic cambia—which evolved repeatedly across the tree. Using stochastic mapping and a developmental complexity framework, we show that evolutionary transitions from typical growth disproportionately favored developmentally simple variants, suggesting that developmental accessibility constrains macroevolutionary trajectories. Despite the temporal overlap between the disparification of vascular variants, and the diversification rate shift, we find no evidence that vascular variants alone drive species diversification. Instead, diversification rates correlate with the presence of tendrils, climbing growth forms, and zygomorphic flowers. These results suggest a synnovation— a suite of synergistic innovations rather than a single trait—as the driver of lineage radiation in Paullinieae. Our study highlights how integrating phylogenomics, developmental anatomy, and trait evolution can illuminate the evolutionary mechanisms shaping plant diversity.
Significance Statement
Lianas are functionally distinct from trees and are rising in abundance across neotropical forests. Yet, it remains poorly understood how these plants are developmentally constructed, and what traits underlie their success. Here, we present the largest molecular phylogeny of any climbing plant lineage and show that vascular variants—unusual stem anatomies that enhance flexibility— are remarkably diverse and have evolved repeatedly in Paullinieae. However, these striking modifications are not linked to species diversification. Instead, we find that the combination of three traits—the climbing habit, coiling tendrils, and zygomorphic flowers—collectively drove the diversification of Paullinieae. Our findings challenge traditional views of key innovations, showing that synergistic trait combinations, rather than any single trait, can catalyze evolutionary radiations and shape biodiversity.
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