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      What are the drivers of female success in food‐deceptive orchids?

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          Abstract

          A large suite of floral signals, and environmental and biotic characteristics influence the behavior of pollinators, affecting the female success of food‐deceptive orchids. In this study, we examined the many factors shaping the reproductive output of three orchid taxa: Dactylorhiza majalis, D. incarnata var. incarnata, and D. fuchsii. We applied a statistical model to correlate female success (number of fruit sets) with individual characteristics (plant and inflorescence height, number of flowers, and spur length), number of pollinaria removed, flowering time, and density of floral units of co‐flowering rewarding plants. Our findings suggested that the broad spectrum of variations in Dactylorhiza's morphological traits, floral display, and flowering phenology within different environmental contexts has a significant impact on their reproductive success. The number of fruits increased with an increase in the number of pollinaria removed in the studied Dactylorhiza taxa. In contrast, a higher number of flowers per inflorescence and higher inflorescences in relation to individual height always decreased fruit set. We observed that low number of co‐flowering rewarding plants in populations could affect the Dactylorhiza reproductive output as magnets and competitor plants. The synchronization of flowering, or lack thereof, between Dactylorhiza and rewarding plants can limit reproductive success. This demonstrates that the food deception strategy is multidirectional, and reproductive output can vary considerably both spatially and temporally within the context of this strategy.

          Abstract

          We observed that a wide range of variations in Dactylorhiza morphological traits, floral display, and flowering phenology in an environmental context affects Dactylorhiza's reproductive success. In contrast, a higher number of flowers per inflorescence and higher inflorescences in relation to individual height always decreased female success. The low number of co‐flowering rewarding plants in populations could shape the Dactylorhiza fruits set as magnets and competitor plants. The lack of synchronized flowering between Dactylorhiza and rewarding plants limits reproduction. This demonstrates that the food deception strategy is multidirectional, and reproductive output can vary considerably spatially and temporally within the context of this strategy.

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            Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification

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              Mechanisms and evolution of deceptive pollination in orchids.

              The orchid family is renowned for its enormous diversity of pollination mechanisms and unusually high occurrence of non-rewarding flowers compared to other plant families. The mechanisms of deception in orchids include generalized food deception, food-deceptive floral mimicry, brood-site imitation, shelter imitation, pseudoantagonism, rendezvous attraction and sexual deception. Generalized food deception is the most common mechanism (reported in 38 genera) followed by sexual deception (18 genera). Floral deception in orchids has been intensively studied since Darwin, but the evolution of non-rewarding flowers still presents a major puzzle for evolutionary biology. The two principal hypotheses as to how deception could increase fitness in plants are (i) reallocation of resources associated with reward production to flowering and seed production, and (ii) higher levels of cross-pollination due to pollinators visiting fewer flowers on non-rewarding plants, resulting in more outcrossed progeny and more efficient pollen export. Biologists have also tried to explain why deception is overrepresented in the orchid family. These explanations include: (i) efficient removal and deposition of pollinaria from orchid flowers in a single pollinator visit, thus obviating the need for rewards to entice multiple visits from pollinators; (ii) efficient transport of orchid pollen, thus requiring less reward-induced pollinator constancy; (iii) low-density populations in many orchids, thus limiting the learning of associations of floral phenotypes and rewards by pollinators; (iv) packaging of pollen in pollinaria with limited carry-over from flower to flower, thus increasing the risks of geitonogamous self-pollination when pollinators visit many flowers on rewarding plants. All of these general and orchid-specific hypotheses are difficult to reconcile with the well-established pattern for rewardlessness to result in low pollinator visitation rates and consequently low levels of fruit production. Arguments that deception evolves because rewards are costly are particularly problematic in that small amounts of nectar are unlikely to have a significant effect on the energy budget of orchids, and because reproduction in orchids is often severely pollen-, rather than resource-limited. Several recent experimental studies have shown that deception promotes cross-pollination, but it remains unknown whether actual outcrossing rates are generally higher in deceptive orchids. Our review of the literature shows that there is currently no evidence that deceptive orchids carry higher levels of genetic load (an indirect measure of outcrossing rate) than their rewarding counterparts. Cross-pollination does, however, result in dramatic increases in seed quality in almost all orchids and has the potential to increase pollen export (by reducing pollen discounting). We suggest that floral deception is particularly beneficial, because of its promotion of outcrossing, when pollinators are abundant, but that when pollinators are consistently rare, selection may favour a nectar reward or a shift to autopollination. Given that nectar-rewardlessness is likely to have been the ancestral condition in orchids and yet is evolutionarily labile, more attention will need to be given to explanations as to why deception constitutes an 'evolutionarily stable strategy'.
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                Author and article information

                Contributors
                adabot@uwb.edu.pl
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                18 April 2024
                April 2024
                : 14
                : 4 ( doiID: 10.1002/ece3.v14.4 )
                : e11233
                Affiliations
                [ 1 ] Faculty of Biology University of Bialystok Białystok Poland
                [ 2 ] Faculty of Computer Science University of Bialystok Białystok Poland
                [ 3 ] Faculty of Science University of South Bohemia České Budějovice Czech Republic
                [ 4 ] Biology Centre, Institute of Entomology Czech Academy of Sciences České Budějovice Czech Republic
                Author notes
                [*] [* ] Correspondence

                Ada Wróblewska, Faculty of Biology, University of Bialystok, Ciołkowskiego 1J Street, Białystok 15‐245, Poland.

                Email: adabot@ 123456uwb.edu.pl

                Author information
                https://orcid.org/0000-0002-1260-4595
                Article
                ECE311233 ECE-2023-10-01812.R2
                10.1002/ece3.11233
                11026981
                38646005
                44aef9d4-b331-4b54-8189-0714b1c4ed8d
                © 2024 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 05 March 2024
                : 17 October 2023
                : 20 March 2024
                Page count
                Figures: 3, Tables: 2, Pages: 12, Words: 7600
                Funding
                Funded by: National Science Center of Poland
                Award ID: 2013/09/B/NZ8/03350
                Categories
                Evolutionary Ecology
                Research Article
                Research Articles
                Custom metadata
                2.0
                April 2024
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.4.0 mode:remove_FC converted:19.04.2024

                Evolutionary Biology
                co‐flowering rewarding plants,dactylorhiza,food‐deception,fruit set,magnet species,orchids,pollinaria removal,remote hypothesis

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