Developmental constraints on bisexuality in compound cones of Ephedra (Gnetales) and implications on the independent origin of bisexual flowers

BACKGROUND AND AIMS: In Ephedra foeminea, Welwitschia and Gnetum spp. (representing all genera of extant Gnetales) male cones have sterile ovules releasing pollination drops to attract pollinators. This condition is unknown in other gymnosperms and resembles the independently evolved bisexuality of angiosperm flowers. Patterns of bisexuality are insufficiently documented in Ephedra, despite their historical importance in Wettstein's pseudanthial theory of the origin of angiosperm flowers. METHODS: We combine original light and scanning electron microscopy data on cone structure and development in Ephedra, field observations in Israel and the USA, and a literature review. KEY RESULTS: Structurally bisexual cones are reported for more than ten of the 57 extant species of Ephedra. Sterile ovules of E. foeminea, Welwitschia and Gnetum exhibit strong and taxon-specific differences from fertile ovules. Occasional bisexual cones of other Ephedra species do not show a functional link to entomophily and have no constraints against male or female fertility. Male organ development is delayed or fully suppressed in the node preceding the ovule(s) in bisexual cones of Ephedra. A terminal reproductive unit rarely develops in bisexual cones. CONCLUSIONS: Cone bisexuality, monoecy and possibly insect pollination are homoplastic in Ephedra. Ovule dimorphism in E. foeminea provides a system to study how key morphological characteristics are regulated in the Gnetales. The suppression or developmental retardation of the uppermost male organs in bisexual cones may be related to the compound nature of the cone and branching suppression below the female zone. In addition to theories interpreting the angiosperm flower as a simple or compound strobilus homologue, the present study highlights the need to test an inverted branching hypothesis, namely, that angiosperm flowers are homologous to a simple strobilus in the androecium, but to a compound cone in the gynoecium.