Which frugivory‐related traits facilitated historical long‐distance dispersal in the custard apple family (Annonaceae) ?

AimLong‐distance dispersal has contributed to the disjunct biogeographical distribution of rain forest plants—something that has fascinated biogeographers since Humboldt's time. However, the dispersal agent for these tropical plant lineages remains puzzling. Here, we investigate which frugivory‐related traits may have facilitated past intercontinental long‐distance dispersal in the custard apple family (Annonaceae), a major vertebrate‐dispersed tropical plant family. We hypothesize that long‐distance dispersal was associated with the evolution of traits related to dispersal by large‐bodied mammals (e.g., large, dull‐coloured, “megafaunal” fruits) and strong‐flying, ocean‐crossing birds and bats (e.g., dehiscent, moniliform or cauliflorous fruits).LocationGlobal.TaxonAnnonaceae.MethodsWe used a fossil‐calibrated phylogenetic framework to infer the biogeographic history of 234 Annonaceae species (10%, covering nearly all genera) in relation to the evolution of 15 frugivory‐related traits, using maximum likelihood and Bayesian inferences. Furthermore, we used linear and generalized linear models and phylogenetic simulations to test whether ancestral fruit traits during intercontinental dispersal were different from those of other lineages not involved in long‐distance dispersal.ResultsWe inferred the ancestral Annonaceae fruits to be small with a single or few small seeds and a small number of fruitlets. These fruits were most probably apocarpous, indehiscent and/or moniliform (i.e., long beads of fruitlets). Furthermore, most of the long‐distance dispersal events in Annonaceae occurred via the expanded tropical forests in the Early Cenozoic (“geodispersal”), and were significantly associated with large (c. 3 cm long), dull‐coloured fruits and short stipes. Additionally, long‐distance dispersal was also facilitated by dehiscent, moniliform and non‐cauliflorous fruits.Main conclusionsWe suggest that the evolution of frugivory‐related traits associated with dispersal by frugivores that frequently move across large distances and/or barriers, such as large‐bodied mammals and strong‐flying birds, has contributed to the disjunct tropical biogeographical distribution of Annonaceae, and probably of tropical rain forest plants more generally.