Total-evidence dating analysis of Osmundaceae reveals long-term extinction amid global climatic and palaeogeographic changes

BACKGROUND AND AIMS: Research efforts have focused on assessing how diversification, morphological evolution, and biogeographic history drive diversity across a wide array of taxonomic groups; however, their interplay remains poorly understood in ferns. Here, we conduct total-evidence dating analyses of Osmundaceae-an iconic species-poor lineage that once dominated Mesozoic forest understories. Based on dense fossil sampling and a skyline fossilised birth-death model, we assess changes in diversification rates and morphological disparity through time. Further, by using a novel diffusion-based approach, we reconstruct the biogeographic history of Osmundaceae under a dynamic palaeogeographic context. METHODS: To perform dating analyses, we combined a novel morphological dataset of 31 characters with seven plastid markers, covering 17 extant taxa and 27 fossils. Divergence times were inferred across alternative variations of skyline fossilised birth-death (sFBD) tree model. Disparity-through-time analyses were performed by reconstructing ancestral character states in the dated phylogeny inferred using the best-fit model. Biogeographic diffusion models were reconstructed by estimating presence probabilities for each pixel across a dynamic paleogeographic landscape, and considering Earth's sphericity. KEY RESULTS: Our analyses support an Early Permian radiation of fertile leptopteroids (289.32 Ma). We identified low diversification and elevated relative extinction rates, and a contraction of the morphospace, following the Toarcian Oceanic Anoxic (TOA) event. High extinction rates persisted throughout the Mesozoic, delaying recovery until the Miocene. Character change rates decelerated after the Early Jurassic, coinciding with a long-term decline in lineage number and morphospace contraction. Antarctica is reconstructed as the primary centre of radiation for crown leptopteroids. CONCLUSIONS: The evolutionary history of Osmundaceae is marked by prolonged high extinction, decelerated character change rates, and morphospace contraction following the TOA event. Our analyses reveal that Antarctica served as the primary centre of radiation for crown leptopteroids, which diversified from an Antarctic relict population rather than via dispersal through the continent.