Go and grow: coordinated evolution of vegetative and reproductive traits facilitated niche diversification in Thymelaeaceae

Abstract Background and Aims: Macroevolutionary studies of species-rich plant lineages have often focused on processes behind either their large distribution or their morphological and functional diversity. Integrating these two evolutionary mechanisms is essential to capture the full picture of how evolutionary and ecological processes shape the biogeographical history of major plant lineages. We investigate whether reproductive and vegetative traits are associated across the evolutionary history of Thymelaeaceae and whether they facilitated dispersal and establishment of lineages across continents and ecological niches. Methods: We use an integrative framework combining: (1) phylogenomics with the Angiosperms353 probe set; (2) detailed characterisation of vegetative architectures and diaspore traits; (3) extraction of species distribution and pedoclimatic data from global databases; (4) multivariate analyses to assess trait-environment associations; (5) correlated evolution tests; (6) ancestral state reconstructions of four vegetative and reproductive traits; and (7) inferences of ancestral ranges and ecological niches, explicitly accounting for dispersal effects. Key Results: Architectural models and fruit types were significantly associated with canopy openness, with basitonic architectures associated with open habitats. The biogeographical reconstructions suggest an evolutionary history shaped by both vicariance and long-distance dispersal. Red, fleshy fruits evolved repeatedly but played little role in intercontinental dispersal; they instead support a c. 13-fold increase in the probability of transition between pedoclimatic niches. Additionally, major biome shifts consistently coincided with changes in architectural models. Conclusions: Throughout the evolutionary history of Thymelaeaceae, our study demonstrates that large plant lineages occupying various vegetation types worldwide possess reproductive and vegetative strategies influenced by different ecological drivers, with reproductive traits primarily shaped by dispersal agents and vegetative traits by abiotic environmental factors. Our study provides evolutionary scenarios supporting the coordinated, but not correlated, evolution of reproductive and vegetative adaptations that enable lineages to diversify into different habitats and partly circumvent phylogenetic niche conservatism.