Adaptive function of duodichogamy: Why do chestnut trees have two pollen emission phases?

Abstract

PremiseIntersexual mating facilitation in flowering plants has been largely underexplored. Duodichogamy is a rare flowering system in which individual plants flower in the sequence male‐female‐male. We studied the adaptive advantages of this flowering system using chestnuts (Castanea spp., Fagaceae) as models. These insect‐pollinated trees produce many unisexual male catkins responsible for a first staminate phase and a few bisexual catkins responsible for a second staminate phase. We hypothesized that duodichogamy increases female mating success by facilitating pollen deposition on stigmas of the rewardless female flowers through their proximity with attractive male flowers responsible for the minor staminate phase.MethodsWe monitored insect visits to 11 chestnut trees during the entire flowering period and explored reproductive traits of all known duodichogamous species using published evidence.ResultsIn chestnuts, insects visited trees more frequently during the first staminate phase but visited female flowers more frequently during the second staminate phase. All 21 animal‐pollinated duodichogamous species identified are mass‐flowering woody plants at high risk of self‐pollination. In 20 of 21 cases, gynoecia (female flower parts) are located close to androecia (male flower parts), typically those responsible for the second minor staminate phase, whereas androecia are often distant from gynoecia.ConclusionsOur results suggest that duodichogamy increases female mating success by facilitating pollen deposition on stigmas by means of the attractiveness of the associated male flowers while effectively limiting self‐pollination.

Harmful self‐pollination drives gynodioecy in European chestnut, a self‐incompatible tree

“…These findings show that, in cosexual trees, the positive effect of emasculation caused by reduced self‐pollination outweighs the negative effect of decreased pollinator attraction caused by eliminating rewarding male inflorescences. The partial emasculation experiment further suggests that it is the pollen produced by the numerous early‐flowering male catkins that drive the decreased fruit set, whereas late‐flowering nectar‐producing male inflorescences from bisexual catkins play a key role in attracting insects close to female flowers (Pauly et al, 2023).…”

“…Non‐rewarding female flowers then become receptive. Finally, male inflorescences from bisexual catkins start producing nectar and emitting pollen, generating a second, much smaller pollen emission phase involved in pollinator attraction and in pollen receipt on nearby female flowers (Pauly et al, 2023). This reduces but does not eliminate the risk of self‐pollination (Hasegawa et al, 2017).…”

“…All flowers on a tree and all grafted copies from a given clone have the same type of male flowers (Larue et al, 2021b, 2022). Male‐sterile inflorescences continue to produce nectar and attract insects such as flies and beetles but not pollen‐seeking insects such as hoverflies and bees (Larue et al, 2021a; Pauly et al, 2023). In crosses between European chestnut ( C. sativa ) and Japanese chestnut ( C. crenata ), only crosses with European chestnut as the mother generate female individuals (Bolvanský and Mendel, 1999; Sisco et al, 2014; Larue, 2021).…”

“…For instance, self‐pollination can have either positive or negative consequences on plant fitness depending on the degree of self‐compatibility (Wells, 1979). Similarly, either sexual conflicts or sexual facilitation can take place in hermaphrodite flowers or bisexual inflorescences (Tonnabel, 2021; Pauly et al, 2023). In particular, pollinator attraction is often attributable to male organs, resulting in intersexual mating facilitation (Darwin, 1877; Lloyd, 1975; Wise et al, 2011; van Etten and Chang, 2014; Pauly et al, 2023).…”