Water primerose (Ludwigia grandiflora subsp. hexapetala) auto- and allogamy: an ecological perspective
Late-acting self-incompatible system, preferential allogamy and delayed selfing in the heterostylous invasive populations of Ludwigia grandiflora subsp. hexapetala
Recommendation: posted 28 March 2022, validated 05 April 2022
Vernay, A. (2022) Water primerose (Ludwigia grandiflora subsp. hexapetala) auto- and allogamy: an ecological perspective. Peer Community in Ecology, 100095. https://doi.org/10.24072/pci.ecology.100095
Invasive plant species are widely studied by the ecologist community, especially in wetlands. Indeed, alien plants are considered one of the major threats to wetland biodiversity (Reid et al., 2019). Ludwigia grandiflora subsp. hexapetala (Hook. & Arn.) G.L.Nesom & Kartesz, 2000 (Lgh) is one of them and has received particular attention for a long time (Hieda et al., 2020; Thouvenot, Haury, & Thiebaut, 2013). The ecology of this invasive species and its effect on its biotic and abiotic environment has been studied in previous works. Different processes were demonstrated to explain their invasibility such as allelopathic interference (Dandelot et al., 2008), resource competition (Gérard et al., 2014), and high phenotypic plasticity (Thouvenot, Haury, & Thiébaut, 2013), to cite a few of them. However, although vegetative reproduction is a well-known invasive process for alien plants like Lgh (Glover et al., 2015), the sexual reproduction of this species is still unclear and may help to understand the Lgh population dynamics.
Portillo Lemus et al. (2021) showed that two floral morphs of Lgh co-exist in natura, involving self-compatibility for short-styled phenotype and self-incompatibility for long-styled phenotype processes. This new article (Portillo Lemus et al., 2022) goes further and details the underlying mechanisms of the sexual reproduction of the two floral morphs.
Complementing their previous study, the authors have described a late self-incompatible process associated with the long-styled morph, which authorized a small proportion of autogamy. Although this represents a small fraction of the L-morph reproduction, it may have a considerable impact on the L-morph population dynamics. Indeed, authors report that “floral morphs are mostly found in allopatric monomorphic populations (i.e., exclusively S-morph or exclusively L-morph populations)” with a large proportion of L-morph populations compared to S-morph populations in the field. It may seem counterintuitive as L-morph mainly relies on cross-fecundation.
Results show that L-morph autogamy mainly occurs in the fall, late in the reproduction season. Therefore, the reproduction may be ensured if no exogenous pollen reaches the stigma of L-morph individuals. It partly explains the large proportion of L-morph populations in the field.
Beyond the description of late-acting self-incompatibility, which makes the Onagraceae a third family of Myrtales with this reproductive adaptation, the study raises several ecological questions linked to the results presented in the article. First, it seems that even if autogamy is possible, Lgh would favour allogamy, even in S-morph, through the faster development of pollen tubes from other individuals. This may confer an adaptative and evolutive advantage for the Lgh, increasing its invasive potential. The article shows this faster pollen tube development in S-morph but does not test the evolutive consequences. It is an interesting perspective for future research. It would also be interesting to describe cellular processes which recognize and then influence the speed of the pollen tube. Second, the importance of sexual reproduction vs vegetative reproduction would also provide information on the benefits of sexual dimorphism within populations. For instance, how fruit production increases the dispersal potential of Lgh would help to understand Lgh population dynamics and to propose adapted management practices (Delbart et al., 2013; Meisler, 2009).
To conclude, the study proposes a morphological, reproductive and physiological description of the Lgh sexual reproduction process. However, underlying ecological questions are well included in the article and the ecophysiological results enlighten some questions about the role of sexual reproduction in the invasiveness of Lgh. I advise the reader to pay attention to the reviewers’ comments; the debates were very constructive and, thanks to the great collaboration with the authorship, lead to an interesting paper about Lgh reproduction and with promising perspectives in ecology and invasion ecology.
Dandelot S, Robles C, Pech N, Cazaubon A, Verlaque R (2008) Allelopathic potential of two invasive alien Ludwigia spp. Aquatic Botany, 88, 311–316. https://doi.org/10.1016/j.aquabot.2007.12.004
Delbart E, Mahy G, Monty A (2013) Efficacité des méthodes de lutte contre le développement de cinq espèces de plantes invasives amphibies : Crassula helmsii, Hydrocotyle ranunculoides, Ludwigia grandiflora, Ludwigia peploides et Myriophyllum aquaticum (synthèse bibliographique). BASE, 17, 87–102. https://popups.uliege.be/1780-4507/index.php?id=9586
Gérard J, Brion N, Triest L (2014) Effect of water column phosphorus reduction on competitive outcome and traits of Ludwigia grandiflora and L. peploides, invasive species in Europe. Aquatic Invasions, 9, 157–166. https://doi.org/10.3391/ai.2014.9.2.04
Glover R, Drenovsky RE, Futrell CJ, Grewell BJ (2015) Clonal integration in Ludwigia hexapetala under different light regimes. Aquatic Botany, 122, 40–46. https://doi.org/10.1016/j.aquabot.2015.01.004
Hieda S, Kaneko Y, Nakagawa M, Noma N (2020) Ludwigia grandiflora (Michx.) Greuter & Burdet subsp. hexapetala (Hook. & Arn.) G. L. Nesom & Kartesz, an Invasive Aquatic Plant in Lake Biwa, the Largest Lake in Japan. Acta Phytotaxonomica et Geobotanica, 71, 65–71. https://doi.org/10.18942/apg.201911
Meisler J (2009) Controlling Ludwigia hexaplata in Northern California. Wetland Science and Practice, 26, 15–19. https://doi.org/10.1672/055.026.0404
Portillo Lemus LO, Harang M, Bozec M, Haury J, Stoeckel S, Barloy D (2022) Late-acting self-incompatible system, preferential allogamy and delayed selfing in the heteromorphic invasive populations of Ludwigia grandiflora subsp. hexapetala. bioRxiv, 2021.07.15.452457, ver. 4 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.1101/2021.07.15.452457
Portillo Lemus LO, Bozec M, Harang M, Coudreuse J, Haury J, Stoeckel S, Barloy D (2021) Self-incompatibility limits sexual reproduction rather than environmental conditions in an invasive water primrose. Plant-Environment Interactions, 2, 74–86. https://doi.org/10.1002/pei3.10042
Reid AJ, Carlson AK, Creed IF, Eliason EJ, Gell PA, Johnson PTJ, Kidd KA, MacCormack TJ, Olden JD, Ormerod SJ, Smol JP, Taylor WW, Tockner K, Vermaire JC, Dudgeon D, Cooke SJ (2019) Emerging threats and persistent conservation challenges for freshwater biodiversity. Biological Reviews, 94, 849–873. https://doi.org/10.1111/brv.12480
Thouvenot L, Haury J, Thiebaut G (2013) A success story: water primroses, aquatic plant pests. Aquatic Conservation: Marine and Freshwater Ecosystems, 23, 790–803. https://doi.org/10.1002/aqc.2387
Thouvenot L, Haury J, Thiébaut G (2013) Seasonal plasticity of Ludwigia grandiflora under light and water depth gradients: An outdoor mesocosm experiment. Flora - Morphology, Distribution, Functional Ecology of Plants, 208, 430–437. https://doi.org/10.1016/j.flora.2013.07.004
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
Evaluation round #3
DOI or URL of the preprint: https://doi.org/10.1101/2021.07.15.452457
Version of the preprint: 3
Author's Reply, 14 Mar 2022
Decision by Antoine Vernay, posted 07 Mar 2022
This second round of your manuscript is now completed. The reviewer made a great job on this new version and encouraged you to improve it with small changes. Please consider the minor revisions asked by the reviewer. I think we are now close to the final version of your manuscript. If you have any questions, please contact me.
Best regards,Download recommender's annotations
Reviewed by Emiliano Mora-Carrera, 04 Mar 2022
Evaluation round #2
DOI or URL of the preprint: 10.1101/2021.07.15.452457
Version of the preprint: 2
Author's Reply, 04 Feb 2022
Decision by Antoine Vernay, posted 29 Nov 2021
I carefully read your rebuttal letter about my first decision and I may make a decision "in hurry", as you suggested, therefore I asked the two previous reviewers to read again your reply. One reviewer declined the invitation to review your manuscript so I asked a third new one to do it. They now completed their reviews.
After reading their different comments, I think that the manuscript deserves some major changes again, especially because we need to read the entire manuscript (and not only your rebuttal letter) with your edits relative to the first round of review, and now to the second. My main concern is about the use of "heterostyly" which can be misleading as a reviewer wrote. However, reviewers made several constructive comments to improve the manuscript.
In your next version, please reply to all comments from all reviewers. You wrote your disagreements with some comments but consider reformulate when your argumentation seemed to not convince everybody. Reviewers most often, suggest some ways to reply to their comments. I can ensure you that the reviewers and I, have spent considerable time on your manuscript and we debate a lot about it. We felt that all the comments were appropriate and deserve improvements in the text. You mentioned that semantic can be easily changed, which is certainly true, but that will change the message of your paper, therefore I thought it was not trivial change.
I hope you will accept to edit your manuscript accordingly. I will then make a new decision about it.
Best regardsDownload recommender's annotations
Reviewed by anonymous reviewer 1, 27 Nov 2021
Reviewed by Juan Arroyo, 18 Nov 2021
Reviewed by Emiliano Mora-Carrera, 23 Nov 2021
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2021.07.15.452457
Version of the preprint: 1
Author's Reply, 25 Oct 2021
Decision by Antoine Vernay, posted 22 Sep 2021
Dear Dominique and colleagues,
First of all, I would like to apologize for this late decision, summer vacations slowed the reviewing process. Two referees were assigned to your manuscript, and in my opinion, read and commented on your paper very carefully.
Unfortunately, I have decided to not consider your manuscript for recommendation by PCI Ecology for two main reasons:
- As mentioned by referees, I agree that if reproduction is a key aspect of the invasion process, your experiment was not designed to fully address this question and did not bring clear evidence of the role of Ludwigia heterostyly in its invasive abilities. Your paper may more fit in a biology or physiology journal.
- the Ludwigia heterostyly is not consensual in the botanist community. The Onagraceae family does not even have any heterostyly species for some authors. I agree with the referees that this fundamental aspect of your study is not clearly demonstrated. Referees also highlighted several (maybe too many) inaccuracies in your introduction in the different comparisons with others studies you made among the manuscript.
Referees wrote several other concerns, suggestions, and advice to improve the paper but I think the manuscript needs too many modifications and reconsideration to be recommended even with major revisions.
I attach to this email the reviews of the two referees and I hope it can help you to improve your paper. Thanks for submitting your manuscript to PCI Ecology and I hope that, despite this rejection, you will consider PCI Ecology again for future submissions.
NB from the managing board of PCI Ecology: a procedure of appeal started the 25th of October 2021Download recommender's annotations