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.

Typifications and nomenclatural notes in Physalis (Solanaceae) from the United States

“…Many of these taxa were merged into only 75 species by D'Arcy (), but today, approximately 90 species are accepted in the genus (Martínez, ; Martínez & al., ; Sullivan, in press). Previously, the type for this genus was the Eurasian Physalis alkekengi L., a taxon that does not form a clade with the other mostly American species of Physalis (Whitson & Manos, ; Deanna & al., ). Resolving this conflict required conserving Physalis with a conserved type ( P. pubescens L.) and transferring Physalis alkekengi to a new genus (Whitson, ; Applequist, ).…”

“…This is an example of one of many taxonomic re‐arrangements, which have impacted taxa within Physalis (e.g., Gray, ; Rydberg, ; Waterfall, , ,b,c, ; Martínez, , ; Sullivan, , , in press; Averett & Martínez, ; Whitson, ). Even in light of molecular data, there is no clear consensus regarding species relationships and their boundaries (Whitson & Manos, ; Zamora‐Tavares & al., ; Deanna & al., ). However, these works provide insight into the circumscription of the genus.…”

“…due to its atypical urceolate corolla (Fig. A–C), it has consistently been found to be embedded within Physalis in molecular phylogenetic studies (Whitson & Manos, ; Zamora‐Tavares & al., ; Deanna & al., ). In sum, we recognize there has been a vast amount of taxonomic work in Physalis but here we will focus on nomenclature and typifications of the species inhabiting the United States.…”

Phylogeny of the AustralianSolanum dioicumgroup using seven nuclear genes: Testing Symon’s fruit and seed dispersal hypotheses

“…The evolutionary development of calyx morphology is one of many exciting areas of current research in Solanaceae [53,54], especially in the context of seed dispersal biology. Among our Solanum study species, calyx form exhibits particular lability – with broad occurrence of derived accrescence/enclosure plus a reversal to the Solanum ancestral state of a non-enveloping calyx associated with fleshy berries.…”

Karyotype asymmetry shapes diversity within the physaloids (Physalidinae, Physalideae, Solanaceae)

“…The ancestral states were inferred under a model where all the transition rates are different ("ARD"). Bayesian stochastic mapping (Nielsen, 2001;Huelsenbeck, Nielsen & Bollback, 2003), was performed with 1,000 simulations on the MCC tree obtained from Deanna et al (2019). The reconstruction was applied to all species considering the unknown data as ambiguous and inferring the states of these species during reconstruction.…”