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GIMENEZ-BENAVIDES LuisORCID_LOGO

  • Biodiversity and Conservation, Universidad Rey Juan Carlos, Móstoles, Spain
  • Evolutionary Ecology, Species interactions

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pollination, plant reproduction,

Review:  1

18 Dec 2024
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Investigating the effects of diurnal and nocturnal pollinators on male and female reproductive success and on floral trait selection in Silene dioica

More in less: almost everything you wanted to know about sex in flowers is in a single experiment with a single plant species

Recommended by and based on reviews by Luis Gimenez-Benavides, Andrea Cocucci, Giovanni Scopece and 1 anonymous reviewer

Most flowering plants (almost 90% of species) are pollinated by animals (Ollerton et al. 2011). In fact, many plants are completely dependent on pollinator visits for reproductive success, due to the complete inability of selfing if they are self-incompatible or have strong gender differentiation, as in dioecious plants. Others have diminished reproductive output in the absence of pollinators, even being self-compatible, if their flowers present strong herkogamy or dichogamy, making autonomous selfing more difficult. Ultimately, all animal-pollinated plant species rely on pollinators for outcrossing. Depending on the genetic structure of plant populations and the movement patterns of these animals, outcrossing patterns will shape the population genetic variation, which will determine its adaptive fate. Thus, understanding the mechanisms governing the pollination interaction is crucial for unraveling the uncertainties of a huge proportion of biodiversity on Earth. Being mutualistic by definition, the animal side of this interaction is less understood, despite most pollinator groups being likely dependent on it for their persistence and perhaps diversity (Ollerton 2017). The role of pollinators in plant diversification has generated much literature and controversy ever since Darwin and his “abominable mystery” about angiosperm diversification (Friedman 2009). However, the other way around, that of plant`s effect on pollinator diversification, is more debatable. A remarkable example of this effect is the possible case of co-speciation mediated by nursery (brood site) pollination, which also includes antagonistic insect herbivory (Wiens et al. 2015), as in some Silene species and their moth pollinators and herbivores (Hembry and Althoff 2016).
 
A properly functional pollination interaction relies on efficient pollinators being attracted to flowers (by visual and olfactory stimuli), rewarded or deceived by them (in feeding, nesting, basking, mating, etc. sites), fit the flower shape and contact the sex organs to enhance both male and female plant fitness. Whereas flower rewards, visually attractive stimuli, and flower architecture and shape greatly dominate pollination studies; there are much fewer studies of olfactory attractive stimuli through flower volatile organic compounds (VOC), due to inherent methodological difficulties (Raguso 2008). Most of the studies dealing with flower volatiles are correlative by nature, whereas manipulative experimental approaches are far less common. 
 
Albeit still plant-centered, the manuscript by Barbot et al. (2024) on Silene dioica and its varied pollinator arrays has great merit in including many of the issues mentioned above to solve long-standing questions in plant reproduction. It elegantly fills a gap with well-designed and performed experiments in a particular pollination mode, nursery pollination, which is now considered more frequent and diverse than formerly thought (Nunes et al. 2018, Haran et al. 2023, Suetsugu 2023). The authors demonstrate that Silene dioica has a truly mixed pollination system, including not only generalist diurnal pollinators as it was formerly considered but also nocturnal pollinators of similar proven efficiency. Although the specialized nursery pollination system of Silene-Hadena is widely reported and described in the literature (Kephart et al. 2006; Prieto-Benítez et al. 2017), it was not formerly considered important for Silene dioica, based on its floral syndrome. However, the experiments designed by Barbot et al. (2024) explore in detail the mechanisms of attraction of nocturnal pollinators and their consequences for plant reproductive success, fully confirming the proper functioning of nursery pollination in this plant species. All these prospects are robustly performed through classical sound phenotypic selection analyses and manipulative experiments, together with other approaches less frequent due to technical difficulties but critical when testing authors’ hypotheses. In particular, male fitness estimates using suitable microsatellite markers are especially appropriate in this dioecious species, although they are also very useful in hermaphroditic species when different pollinators and flower variants are interacting (Kulbaba and Worley 2013, Simón-Porcar et al. 2015). Finally, the manipulation of flower fragrance (in fact, of a single VOC) has proved also critical to getting insight into its effect on night pollinators and their joint role as ovipositors and thus predators. All these questions are addressed with a fully crossed experimental design that allows unveiling interactions between experimental factors, a challenge in experimental biology, especially under natural conditions. 
 
In evolutionary biology, most experiments are carried out in laboratories, where factors under scrutiny are carefully controlled and hence their effects are easy to reproduce. The cost of this approach is that the variables of interest are oversimplified and difficult to extrapolate to real ecological conditions. In evolutionary ecology, experiments under field conditions greatly solve this shortcoming, but the cost arises in the difficulties of dealing with several interacting and uncontrolled factors. The study by Barbot et al. (2024) nicely addresses real-world questions in a specialized pollination plus herbivory interaction. The results are robust and pave the road for further overarching pursuits, as mentioned by the reviewers. Thus, it would be interesting to assess actual, absolute values of pollen dispersal distance in natural populations, the selection exerted through the complete reproductive period of male and female plants, provided that they are different, or the effect of using more natural flower bouquets, in the next steps. However, as it stands, this outstanding study will be of high interest to scholars on any of the many topics dealt with there, but also to students willing to start research in the fascinating field of experimental pollination biology, given the wide array of questions addressed and the modern methodological approaches provided.
 
Acknowledgments

The authors of this recommendation benefitted from grants provided by grants PID2021-122715NB-I00 and TED2021-131037B-I00 funded by MCIN/AEI/ 10.13039/501100011033 and by the “European Union NextGeneration EU/PRTR”, and by MSCA-IF-2019-89789.
 
References

Barbot, E., Dufaÿ, M., Godé, C., & De Cauwer, I. (2024). Exploring the effect of scent emission and exposition to diurnal versus nocturnal pollinators on selection patterns on floral traits. Zenodo. https://doi.org/10.5281/zenodo.11490231

Friedman, W. E. (2009). The meaning of Darwin's “abominable mystery”. American Journal of Botany, 96(1), 5-21. https://doi.org/10.3732/ajb.0800150

Haran, J., Kergoat, G. J., & de Medeiros, B. A. (2023). Most diverse, most neglected: weevils (Coleoptera: Curculionoidea) are ubiquitous specialized brood-site pollinators of tropical flora. Peer Community Journal, 3. https://doi.org/10.24072/pcjournal.279 

Hembry, D.H. and Althoff, D.M. (2016), Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity. American Journal of Botany, 103: 1783-1792. https://doi.org/10.3732/ajb.1600056

Kephart, S., Reynolds, R. J., Rutter, M. T., Fenster, C. B., & Dudash, M. R. (2006). Pollination and seed predation by moths on Silene and allied Caryophyllaceae: evaluating a model system to study the evolution of mutualisms. New Phytologist, 169(4), 667-680. https://doi.org/10.1111/j.1469-8137.2005.01619.x

Kulbaba, M. W., & Worley, A. C. (2013). Selection on Polemonium brandegeei (Polemoniaceae) flowers under hummingbird pollination: in opposition, parallel, or independent of selection by hawkmoths?. Evolution, 67(8), 2194-2206. https://doi.org/10.1111/evo.12102

Nunes, C. E. P., Maruyama, P. K., Azevedo-Silva, M., & Sazima, M. (2018). Parasitoids turn herbivores into mutualists in a nursery system involving active pollination. Current Biology, 28(6), 980-986. https://doi.org/10.1016/j.cub.2018.02.013

Ollerton, J. (2017). Pollinator diversity: distribution, ecological function, and conservation. Annual review of ecology, evolution, and systematics, 48(1), 353-376. https://doi.org/10.1146/annurev-ecolsys-110316-022919

Ollerton, J., Winfree, R., & Tarrant, S. (2011). How many flowering plants are pollinated by animals?. Oikos, 120(3), 321-326. https://doi.org/10.1111/j.1600-0706.2010.18644.x

Prieto-Benitez, S., Yela, J. L., & Gimenez-Benavides, L. (2017). Ten years of progress in the study of Hadena-Caryophyllaceae nursery pollination. A review in light of new Mediterranean data. Flora, 232, 63-72. https://doi.org/10.1016/j.flora.2017.02.004

Raguso, R. A. (2008). Wake up and smell the roses: the ecology and evolution of floral scent. Annual review of ecology, evolution, and systematics, 39(1), 549-569. https://doi.org/10.1146/annurev.ecolsys.38.091206.095601

Simón-Porcar, V. I., Meagher, T. R., & Arroyo, J. (2015). Disassortative mating prevails in style-dimorphic Narcissus papyraceus despite low reciprocity and compatibility of morphs. Evolution, 69(9), 2276-2288. https://doi.org/10.1111/evo.12731

Suetsugu, K. (2023). A novel nursery pollination system between a mycoheterotrophic orchid and mushroom-feeding flies. Ecology, 104(11), e4152. https://doi.org/10.1002/ecy.4152

Wiens, J. J., Lapoint, R. T., & Whiteman, N. K. (2015). Herbivory increases diversification across insect clades. Nature communications, 6(1), 8370. https://doi.org/10.1038/ncomms9370 

avatar

GIMENEZ-BENAVIDES LuisORCID_LOGO

  • Biodiversity and Conservation, Universidad Rey Juan Carlos, Móstoles, Spain
  • Evolutionary Ecology, Species interactions

Recommendations:  0

Review:  1

Areas of expertise
pollination, plant reproduction,