Repeated evolution of a morphological novelty: a phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)

Abstract

PREMISE OF THE STUDYThe evolution of novel fruit morphologies has been integral to the success of angiosperms. The inflated fruiting calyx, in which the balloon-like calyx swells to completely surround the fruit, has evolved repeatedly across angiosperms and is postulated to aid in protection and dispersal. Here we investigate the evolution of this trait in the tomatillos and their allies (Physalideae, Solanaceae), using a newly estimated phylogeny and a suite of comparative methods to infer evolutionary gains and losses.METHODSThe Physalideae phylogeny was estimated using DNA sequences from four regions (ITS, LEAFY, trnL-F, waxy) using maximum likelihood and Bayesian Inference. Maximum likelihood model selection was used to determine the best fitting model of trait evolution. Using this model, we estimated ancestral states along with the numbers of gains and losses of fruiting calyx accrescence and inflation with Bayesian stochastic mapping. Also, phylogenetic signal in calyx morphology was examined with two metrics (parsimony score and Fritz and Purvis’ D).KEY RESULTSThe well resolved phylogeny points to multiple taxa in need of revision, including the eight genera that are non-monophyletic as presently circumscribed. Model fitting indicated that calyx evolution has proceeded in stepwise fashion, from non-accrescent, to accrescent, to inflated. Moreover, these transitions appear to be largely irreversible. Among the 215 sampled Physalideae, we inferred 24 gains of fruiting calyx accrescence, 24 subsequent transitions to a fully inflated calyx and only two reversals. A median of 50 shifts were estimated in total across the clade from the ancestral non-accrescent calyx. Nonetheless, fruiting calyx accrescence and inflation show strong phylogenetic signal.CONCLUSIONSOur phylogeny greatly improves the resolution of Physalideae and highlights the need for taxonomic work. The analyses of trait evolution reveal that the inflated fruiting calyx has evolved many times and that the trajectory towards this phenotype is generally stepwise and directional. These results provide a strong foundation for studying the genetic and developmental mechanisms responsible for the repeated origins of this charismatic fruit trait.