LETTERS TO NATURE Functional androdioecy in the flowering plant Datisca glomerata

THE role of androdioecy (the presence of male and hermaphrodite individuals in a breeding population) in the evolution of dioecy has long been the subject of much interest and discussion1-9. But no functionally androdioecious species has been previously documented2 and recent studies have even raised doubt about whether the phenomenon exists at all3. Although many cases of androdioecy have been reported, most of these are based on morphological data alone and, when examined in detail, are actually found to be functionally dioecioue-12. Here we describe functional androdioecy in the flowering plant Datisca glomerata (Presl.) Baill. (Datiscaceae). We suggest that the condition evolved from a dioecious precursor, and not from hermaphroditism as is commonly postulated for the evolution of androdioecy' -9. Androdioecy in this case could be a transitional state in the breakdown of a dioecious breeding system towards hermaphroditism. Datisca glomerata is distributed from northern California to northern Baja California, Mexico. Plants are long-lived tall (1-2.5 m) herbaceous perennials of riparian habitats. Flowering and fruiting occur throughout the summer months. The floral morphology of the species is relatively simple13'4. Flowers are apetalous. Calyx lobes are short (1-1.5 mm) and inconspicuous. Male flowers have from six to twenty anthers. At anthesis, the pedicels of male flowers elongate, often reaching lengths of 2 cm or more. In hermaphrodite flowers the ovary is a three-sided capsule with three branched styles. They are protogynous and usually have three anthers. Nectaries are absent. The pendulous male flowers, large styles of the female and hermaphrodite flowers, unornamented pollen1'4 and the otherwise reduced flowers without nectar, are characteristic of an anemophilous pollination syndrome". Likewise, the height and growth of the plant in an exposed riparian habitat are consistent with anemophily. We verified the existence of functional androdioecy in D. glomerata. Hermaphrodite flowers in this species have fertile pollen (>95% reactive with an enzyme-specific pollen viability stain"), dehiscent anthers, and are self-compatible producing as many viable seeds on self-pollination as open pollinated flowers. Hermaphrodite flowers that we emasculated and bagged set no seed, indicating that non-pseudogamous apomixis does not occur. In addition, we examined 23 populations of D. glomerata for electrophoretically detectable genetic variation, revealing an inbreeding coefficient of F=0.617 (P< 0.001)'7 for six variable loci, indicating high inbreeding". By contrast, we found no deviation from random mating (F = 0.005 (P> 0.995) for four variable loci) for three populations of the congeneric dioecious species D. cannabina L., native to southwestern Asia'''. To confirm androdioecy in Datisca, it must be shown that individual plants are not sexually labile, that is, able to vary their sex according to their physiological condition or environment19-21. In a perennial plant with a prolonged flowering season such changes can be temporary and therefore difficult to detect. But flowers of Datisca do not abcise after anthesis, and their sex can be readily distinguished in the dry state. A mature inflorescence therefore contains a complete record of the sex of the flowers from the entire growing season. By observing all branches and inflorescences of 397 flowering plants at the end of the 1989 growing season, we found that plants remained