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      Is There ‘Anther-Anther Interference’ within a Flower? Evidences from One-by-One Stamen Movement in an Insect-Pollinated Plant

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          Abstract

          The selective pressure imposed by maximizing male fitness (pollen dispersal) in shaping floral structures is increasingly recognized and emphasized in current plant sciences. To maximize male fitness, many flowers bear a group of stamens with temporally separated anther dehiscence that prolongs presentation of pollen grains. Such an advantage, however, may come with a cost resulting from interference of pollen removal by the dehisced anthers. This interference between dehisced and dehiscing anthers has received little attention and few experimental tests to date. Here, using one-by-one stamen movement in the generalist-pollinated Parnassia palustris, we test this hypothesis by manipulation experiments in two years. Under natural conditions, the five fertile stamens in P. palustris flowers elongate their filaments individually, and anthers dehisce successively one-by-one. More importantly, the anther-dehisced stamen bends out of the floral center by filament deflexion before the next stamen's anther dehiscence. Experimental manipulations show that flowers with dehisced anther remaining at the floral center experience shorter (1/3–1/2 less) visit durations by pollen-collecting insects (mainly hoverflies and wasps) because these ‘hungry’ insects are discouraged by the scant and non-fresh pollen in the dehisced anther. Furthermore, the dehisced anther blocks the dehiscing anther's access to floral visitors, resulting in a nearly one third decrease in their contact frequency. As a result, pollen removal of the dehiscing anther decreases dramatically. These results provide the first direct experimental evidence that anther-anther interference is possible in a flower, and that the selection to reduce such interferences can be a strong force in floral evolution. We also propose that some other floral traits, usually interpreted as pollen dispensing mechanisms, may function, at least partially, as mechanisms to promote pollen dispersal by reducing interferences between dehisced and dehiscing anthers.

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          Most cited references8

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          Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond.

          Comparisons of the causes and consequences of cross- and self-fertilization have dominated research on plant mating since Darwin's seminal work on plant reproduction. Here, I provide examples of these accomplishments, but also illustrate new approaches that emphasize the role of floral design and display in pollen dispersal and fitness gain through male function. Wide variation in outcrossing rate characterizes animal-pollinated plants. In species with large floral displays, part of the selfing component of mixed mating can arise from geitonogamy and be maladaptive because of strong inbreeding depression and pollen discounting. Floral strategies that separate the benefits of floral display from the mating costs associated with geitonogamy can resolve these conflicts by reducing lost mating opportunities through male function. The results from experiments with marker genes and floral manipulations provide evidence for the function of herkogamy and dichogamy in reducing self-pollination and promoting pollen dispersal. Evidence is also presented indicating that increased selfing resulting from changes to floral design, or geitonogamy in large clones, can act as a stimulus for the evolution of dioecy. The scope of future research on mating strategies needs to be broadened to include investigations of functional links among flowers, inflorescences and plant architecture within the framework of life-history evolution.
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            Sexual interference of the floral kind.

            Floral hermaphroditism results in conflicts and compromise in the parental roles of plants during pollination and mating. A potential cost of hermaphroditism is sexual interference between maternal and paternal functions resulting in gamete wastage and reduced fitness. Sexual interference may or may not be associated with self-pollination. In cases where self-pollination occurs, ovule or pollen discounting may reduce mating opportunities. Here I describe forms of sexual interference in flowering plants, distinguishing whether physical or biochemical interactions are involved and whether fitness costs associated with gamete wastage arise from intra-floral versus inter-floral processes. I review the limited experimental evidence for interference between sex functions and evaluate the hypothesis that some floral adaptations usually interpreted as anti-selfing mechanisms may serve an alternative function in reducing mating costs arising from this form of sexual conflict.
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              The role of theory in an emerging new plant reproductive biology.

              Recent empirical studies hint at an end to the historical solitude between pollination and mating system approaches to plant reproductive character evolution. Now is an opportune time to distill theoretical results into comprehensible insight, and to integrate these findings into the emerging new plant reproductive biology. We outline four theoretical insights for understanding the evolution of reproductive characters, and show how these allow researchers to dissect complex ecological scenarios into clear and evolutionarily relevant components.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                27 January 2014
                : 9
                : 1
                : e86581
                Affiliations
                [1 ]Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, China
                [2 ]Institute for Peat and Mire Research, Northeast Normal University, State Environmental Protection Key Laboratory of Wetland Ecology and Vegetation Restoration, Changchun, China
                Centro de Investigación y de Estudios Avanzados, Mexico
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MXR ZJB. Performed the experiments: MXR ZJB. Analyzed the data: MXR. Contributed reagents/materials/analysis tools: MXR. Wrote the paper: MXR.

                [¤]

                Current address: Department of Biology, University of Naples ‘Federico II’, Naples, Italy

                Article
                PONE-D-13-38732
                10.1371/journal.pone.0086581
                3903572
                24475150
                f2373921-6f4a-4308-94b3-94d01f940cae
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 20 September 2013
                : 16 December 2013
                Page count
                Pages: 7
                Funding
                Financial support was provided by the National Natural Science Foundation of China to M.X.R. (grant numbers 30970459 and 31170356) and Z.J.B. (grant numbers 40971036 and 41371103) ( www.nsfc.gov.cn). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Reproductive System
                Ecology
                Biodiversity
                Evolutionary Ecology
                Plant Ecology
                Plant Science
                Botany
                Plant Anatomy
                Plant Morphology
                Plants
                Flowers
                Plant Ecology
                Plant Physiology

                Uncategorized
                Uncategorized

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