Floral Biology and Pollination Ecology ofDesmos chinensis(Annonaceae): Assessing the Efficacy of Floral Synchrony for Promoting Xenogamy

Abstract

Editor: Elena M. KramerPremise of research. Early-divergent angiosperms typically possess hermaphroditic flowers but often lack any biochemically mediated self-incompatibility mechanism. Although outcrossing is generally promoted in these taxa by protogyny, which is effective for precluding autogamy (self-fertilization within a flower), other mechanisms are necessary to prevent geitonogamy (self-pollination between different flowers within an individual). In this article we investigate the occurrence and efficacy of inter-and intraindividual floral synchrony for preventing geitonogamy in the early-divergent angiosperm Desmos chinensis (Annonaceae) within the context of the overall floral biology and pollination ecology of the species.Methodology. We assess the floral phenology (at the flower, individual plant, and population levels), floral scent chemistry, pollination ecology, and breeding system of D. chinensis.Pivotal results. Desmos chinensis is pollinated by small Amystrops beetles (Nitidulidae) that are attracted by floral scent. Although the flowers are hermaphroditic and self-compatible, population genetic analysis indicates that the species is likely to be predominantly xenogamous (outcrossing): most of the genetic diversity occurs within populations, with evidence of extensive gene flow. The flowers are protogynous, with anthesis lasting ca. 27 h and with a 6-h nonsexual interim phase separating the functional pistillate and staminate phases. Although protogyny is an effective mechanism to prevent autogamy, it cannot prevent geitonogamy.Conclusions. We demonstrate the existence of inter-and intraindividual floral synchrony in D. chinensis, in which pistillate-and staminate-phase flowers rarely coexist within an individual, thereby largely precluding the possibility of geitonogamy. We suggest that inter-and intraindividual floral synchrony may be much more common than previous studies suggest. Since the phenomenon is known from several phylogenetically disparate lineages in the family and has possibly evolved independently, it may endow a significant selective advantage for promoting xenogamy.

Accelerated diversification correlated with functional traits shapes extant diversity of the early divergent angiosperm family Annonaceae

“…Although anthesis usually extends over 48 h in species of Annonaceae with hermaphroditic flowers [23,24], Artabotrys , Dasymaschalon , Friesodielsia , and Goniothalamus species, which all exhibit circadian trapping, also have an abbreviated anthesis of only 23–27 h [23,24,44]. A similarly brief anthesis ( c. 27 h) is reported for Desmos chinensis [22], although this species does not trap pollinators. Desmos is sister to the Dasymaschalon-Friesodielsia clade [18], and hence abbreviated anthesis is likely to be synapomorphic for the entire clade and can be inferred to have evolved prior to pollinator trapping [24].…”

“…Annonaceae species with abbreviated anthesis often display pistillate/staminate-phase floral synchrony, in which pistillate-phase and staminate-phase flowers are not borne concurrently on an individual, thereby minimizing opportunities for geitonogamy [22,23,24,44]. Lau et al [23] hypothesized that shortening of anthesis in species with this type of floral synchrony reduces the proportion of non-flowering days and hence increases seedset.…”

“…DNA sequences of nearly 1,000 species have been generated, enabling a good understanding of phylogenetic relationships and generic delimitation in the family. Considerable progress has also been made in understanding the distribution of morphological characters across the family and their possible roles in diversification, especially floral and fruit traits of ecological importance such as floral chambers [20], the role of stigmatic exudate as an extragynoecial compitum [21], staminate/pistillate-phase floral synchrony [22], the circadian trapping of pollinators [23,24], and seed dispersal units (discussed below; [25]). These advances in both molecular and morphological data accumulation and new analytical methods provide excellent opportunities to use recent comprehensive phylogenies to date divergence times in the family and to study diversification patterns in relation to key functional traits.…”

Contrasting pollination ecology ofDisepalumspecies (Annonaceae): evolutionary loss of the floral chamber and partial breakdown of protogyny associated with a shift in pollination system

“…There are diverse mechanisms by which species of Annonaceae with hermaphroditic flowers promote xenogamy (reviewed by Pang & Saunders, ). In addition to protogyny, which is effective in preventing autogamy as long as there is no temporal overlap between the pistillate and staminate phases, many species of Annonaceae display pistillate‐staminate‐phase synchrony, so that all the flowers borne on an individual concurrently are in the same sexual phase, hence preventing geitonogamy (Murray & Johnson, ; Rogstad, ; Webber, ; Lora et al ., ; Pang & Saunders, , ). The absence of this mechanism in Disepalum is not surprising, however, as the prolonged anthesis period would severely limit the number of flowers that could be produced by the tree and hence constrain seed set.…”

“…Protogyny is ubiquitous in species of Annonaceae with hermaphroditic flowers and is an effective mechanism to prevent autogamy in the absence of a biochemically mediated self‐incompatibility mechanism (Pang & Saunders, ; and references therein). Although protogyny is unable to prevent geitonogamy, many species of Annonaceae have evolved floral synchrony in which maturation of pistillate‐ and staminate‐phase flowers is synchronised so that they are not borne on the same individual concurrently (Murray & Johnson, ; Rogstad, ; Webber, ; Lora, Herrero & Hormaza, ; Pang & Saunders, , ). There is no evidence of such synchrony in D. pulchrum , although individuals bear few anthetic flowers concurrently and this would significantly reduce opportunities for geitonogamy.…”