Correlated evolution of fruit and seed traits in Artabotrys (Annonaceae) and the potential role of frugivore-mediated selection

Abstract

The existence of dispersal syndromes remains contentious: only a subset of studies have found evidence for sets of fruit traits that are associated with distinct frugivore guilds. The relationship between seed traits and dispersal agent is furthermore often neglected. Artabotrys (Annonaceae), a palaeotropical genus of lianas with substantial variation in fruit and seed morphology, is an excellent study group for evaluating correlated evolution of seed traits in association with climatic variables and dispersal-related traits. Seed and fruit functional traits were evaluated for 43 Artabotrys species, with locality data gathered from herbarium records and GBIF. The values of WorldClim bioclimatic variables were in turn extracted for each locality. Bayesian phylogenetic reconstruction and divergence time estimation were based on ca. 15.7 kb of chloroplast and nuclear DNA sequence data. The functional trait data were fitted to various Brownian motion and Ornstein-Uhlenbeck models, in order to assess whether testa thickness and seed volume evolved towards distinct optima in lineages with different combinations of dispersal-related traits and/or lineages with different precipitation regimes. The modelling results unequivocally rejected non-adaptive explanations for both seed traits and suggest a potential role of frugivore-mediated selection. Lineages with slippery testa and thin pericarp (SP) have evolved towards smaller seeds and a thinner testa, whereas lineages with other combinations of pericarp thickness and testa texture have evolved towards larger seeds and a thicker testa. The lower seed physical defence in SP lineages may be because a slippery testa facilitates spitting and/or swallowing of intact seeds by primates while birds (which swallow fruits whole) generally prefer fruits with thin pericarp. The two distinct trait optima may therefore correspond to two seed dispersal regimes in Artabotrys: (1) birds and primates with seed-swallowing and seed-spitting behaviours that disperse SP lineages; and (2) primates with more destructive oral processing habits that disperse other lineages.