Sexual interference revealed by joint study of male and female pollination success in chestnut

Larue, Clément; Klein, Etienne K.; Petit, Rémy J.

doi:10.1111/mec.16820

Cited by 11 publications

(32 citation statements)

References 105 publications

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“…Self-pollination in cosexual chestnut trees is massive, a likely consequence of huge pollen production and frequent geitonogamy in this large mass-flowering tree. In the study site, we previously estimated, using a spatially explicit mixed mating model, that the self-pollination rate is 74% (Larue et al 2022). Hasegawa et al (2009) found even higher values of self-pollination in Japanese chestnut by genotyping pollen grains directly collected on stigmas.…”

Section: Discussionmentioning

confidence: 99%

“…Chestnut trees are monoecious, self-incompatible, and duodichogamous, all mechanisms frequently interpreted as adaptations to promote outcrossing (Lloyd & Webb, 1986; Webb & Lloyd, 1986; Bertin & Newman, 1993; Routley et al ., 2004; Koelling & Karoly, 2007). In a previous study, we found self-fertilization rates of 5% in chestnut trees with fully developed stamens and 1% in trees with dysfunctional stamens (Larue et al ., 2022). Even with strong inbreeding depression, this difference cannot explain the maintenance of gender dimorphism.…”

Section: Introductionmentioning

confidence: 87%

“…Third, chestnuts are self-incompatible (Xiong et al, 2019). In European chestnuts and in its hybrids, two genders can be distinguished: cosexual trees, which are fully male-fertile; and female trees, which are completely or largely male-sterile (Solignat and Chapa, 1975;Larue et al, 2022;Fig. 1).…”

Section: Chestnut Floral Biologymentioning

confidence: 99%

“…Interestingly, male-sterile catkins 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). All flowers on a tree and all trees from a clone have the same type of male flowers (Larue et al, 2021b(Larue et al, , 2022. In interspecific crosses, male sterility is expressed only in some cytoplasmic backgrounds (Bolvanský & Mendel, 1999;Sisco et al, 2014;Larue, 2021).…”

Section: Chestnut Floral Biologymentioning

confidence: 99%

“…Specifically, we compared five key components of female fitness between genders in a chestnut experimental stand: basal area (a proxy for tree size), flower density, burr set, fruit set and fruit weight. Both genders harbour nectar-producing male catkins that attract pollinators; the only visible difference is that the stamens are aborted or greatly reduced in female trees (Larue et al, 2021a(Larue et al, , 2022. We took advantage of this feature to assess the importance of self-pollen avoidance in an experiment where we removed male catkins not only from cosexual but also from female chestnut trees.…”

Section: Introductionmentioning

confidence: 99%

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

Larue

Petit

2022

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Background and Aim: In gynodioecious plants, male-sterile individuals must have a female advantage to coexist with bisexual individuals. In European chestnuts, characterized by a form of late-acting self-incompatibility, male-fertile trees produce large amounts of pollen when female flowers are receptive, resulting in abundant self-pollination. Here we study whether male-sterile chestnut trees have an increased fruit set compared to male-fertile trees because they escape from the negative consequences of self-pollination on ovules, a case of self-interference. Methods: We measured fruit set of 242 male-fertile and male-sterile trees during three consecutive years. To test experimentally the hypothesis of negative interference of self-pollen on ovules as the origin of the female advantage of male-sterile trees, we emasculated male-fertile trees and compared their fruit set with that of control male-fertile trees. We performed the same experiment on male-sterile trees by removing the sterile but rewarding male catkins as a natural control to test for the effect of decreased insect attractiveness on fruit set. Key Results: The fruit set of male-sterile trees is higher than that of male-fertile trees by a factor of two in some years. Following emasculation, male-fertile trees have a higher fruit set than control male-fertile trees, pointing to a negative effect of the massive amount of self-pollen produced by fertile male catkins on fertilization probability of female flowers. In contrast, emasculated male-sterile trees had a lower fruit set than control male-sterile trees, pointing to a decrease in insect attractiveness after removing nectar-producing male catkins. Conclusions: Our emasculation experiment showed that sexual interference results in massive ovule discounting in male-fertile trees, sufficient for accounting for the persistence of female trees in natural populations of European chestnut trees.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 87%

Section: Chestnut Floral Biologymentioning

confidence: 99%

Section: Chestnut Floral Biologymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Larue

Petit

2022

Preprint

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

Pauly

Larue

Petit

2023

American J of Botany

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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.

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

Larue,

Petit

2024

American J of Botany

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PremiseGynodioecy is a rare sexual system in which two genders (sensu Lloyd, 1980), cosexuals and females, coexist. To survive, female plants must compensate for their lack of siring capacity and male attractiveness. In European chestnut (Castanea sativa), an outcrossing tree, self‐pollination reduces fruit set in cosexual individuals because of late‐acting self‐incompatibility and early inbreeding depression. Could this negative sexual interaction explain the presence of females in this species?MethodsWe studied gender variation in wild populations of European chestnut. In addition, we compared fruit set (the proportion of flowers giving fruits) and other key female fitness components as well as reproductive allocation between genders. We then performed emasculation experiments in cosexual trees, by removing nectar‐producing fertile male inflorescences. We also removed sterile but nectar‐producing male inflorescences from female trees, as a control.ResultsWe found a highly variable proportion of male‐sterile individuals in the wild in European chestnut. In the experimental plot, trees from each gender had similar size, flower density, and burr set, but different fruit set. Removing nectar‐producing male inflorescences from branches or entire trees increased fruit set in cosexual but not in female trees.ConclusionsThese results show that self‐pollination impairs fruit set in cosexual trees. Female trees avoid these problems as they do not produce pollen but continue to attract pollinators thanks to their rewarding male‐sterile inflorescences, resulting in a much higher fruit set than in cosexuals. This demonstrates that even outcrossed plants can benefit from the cessation of self‐pollination, to the point that unisexuality can evolve.

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Sexual interference revealed by joint study of male and female pollination success in chestnut

Cited by 11 publications

References 105 publications

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

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

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

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

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