Gynoecial diversity in the Annonaceae and the evolution of functional traits that overcome the limitations of apocarpy

Abstract Most species in the early divergent angiosperm family Annonaceae are apocarpous, with very diverse gynoecial morphologies. Although several Annonaceae genera with apocarpous flowers are known to possess an extragynoecial compitum (EGC) that enables intercarpellary pollen‐tube growth to enhance fertilization success, the occurrence of EGC across the whole family remains obscure. Twenty Annonaceae species from all four subfamilies (Anaxagoreoideae, Ambavioideae, Annonoideae, and Malmeoideae) are examined here, with anatomical evidence revealing the occurrence of stigmatic exudate‐mediated suprastylar EGC in all four subfamilies. Histological and ontogenetic studies furthermore indicate that trichomes in Cananga and Drepananthus form a confluent zone that connects adjacent stigmas, providing a structural premise for suprastylar EGC. Infrastylar EGC are reported in the Annonaceae for the first time in several genera, including Artabotrys , Annona , and Miliusa , associated with the opening on the ovary ventral groove and/or basal placentation. In addition to the sister genera Isolona and Monodora that are clearly syncarpous, flowers of the distantly related genus Cyathocalyx with a unicarpellate gynoecium have also been hypothesized to be syncarpous. Evidence of carpel vasculature and primordium development does not support that the solitary Cyathocalyx carpel is originated from carpel fusion, however, although the increased number of ovules renders it functionally similar to syncarpy. Gynoecial features, including the extensive occurrence of EGC and the increased number of ovules per carpel (consonant with reduction to a solitary carpel) in Cyathocalyx , may have evolved to overcome limitations associated with apocarpy and possibly contribute to the reproductive success and diversification of the family.