Spreading the risk of reproductive failure when the environment is unpredictable and ephemeral
Bimodal breeding phenology in the Parsley Frog Pelodytes punctatus as a bet-hedging strategy in an unpredictable environment despite strong priority effects
Recommendation: posted 20 August 2022, validated 15 September 2022
Many species breed in environments that are unpredictable, for instance in terms of the availability of resources needed to raise the offspring. Organisms might respond to such spatial and temporal unpredictability by adopting plastic responses to adjust their reproductive investment according to perceived cues of environmental quality. Some species such as the amphibians might also face the problem of ephemeral habitats, when the ponds where they breed have a chance of drying up before metamorphosis has occurred. In this case, maximizing long-term fitness might involve a strategy of spreading the risk, even though the reproductive success of a single reproductive bout might be lower. Understanding how animals (and plants) get adapted to stochastic environments is particularly crucial in the current context of rapid environmental changes.
In this article, Jourdan-Pineau et al. report the results of field surveys of the Parsley Frog (Pelodytes punctatus) in Southern France. This frog has peculiar breeding phenology with females breeding in autumn and spring. The authors provide quite an extensive amount of information on the reproductive success of eggs laid in each season and the possible ecological factors accounting for differences between seasons. Although the presence of interspecific competitors and predators does not seem to account for pond-specific reproductive success, the survival of tadpoles hatching from eggs laid in spring is severely impaired when tadpoles from the autumn cohort have managed to survive. This intraspecific competition takes the form of a “priority” effect where tadpoles from the autumn cohort outcompete the smaller larvae from the spring cohort. Given this strong priority effect, one might tentatively predict that females laying in spring should avoid ponds with tadpoles from the autumn cohort. Surprisingly, however, the authors did not find any evidence for such avoidance, which might indicate strong constraints on the availability of ponds where females might possibly lay.
Assuming that each female can indeed lay both in autumn and spring, how is this bimodal phenology maintained? Would not be worthier to allocate all the eggs to the autumn (or the spring) laying season? Eggs laid in autumn and spring have to face different environmental hazards, reducing their hatching success and the probability to produce metamorphs (for instance, tadpoles hatching from eggs laid in autumn have to overwinter which might be a particularly risky phase).
Jourdan-Pineau and coworkers addressed this question by adapting a bet-hedging model that was initially developed to investigate the strategy of allocation into seed dormancy of annual plants (Cohen 1966) to the case of the bimodal phenology of the Parsley Frog. By feeding the model with the parameter values obtained from the field surveys, they found that the two breeding strategies (laying in autumn and in spring) can coexist as long as the probability of breeding success in the autumn cohort is between 20% and 80% (the range of values allowing the coexistence of a bimodal phenology shrinking a little bit when considering that frogs can reproduce 5 times during their lifespan instead of three times).
This paper provides a very nice illustration of the importance of combining approaches (here field monitoring to gather data that can be used to feed models) to understand the evolution of peculiar breeding strategies. Although future work should attempt to gather individual-based data (in addition to population data), this work shows that spreading the risk can be an adaptive strategy in environments characterized by strong stochastic variation.
Cohen D (1966) Optimizing reproduction in a randomly varying environment. Journal of Theoretical Biology, 12, 119–129. https://doi.org/10.1016/0022-5193(66)90188-3
Jourdan-Pineau H., Crochet P.-A., David P. (2022) Bimodal breeding phenology in the Parsley Frog Pelodytes punctatus as a bet-hedging strategy in an unpredictable environment despite strong priority effects. bioRxiv, 2022.02.24.481784, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.02.24.481784
Gabriele Sorci (2022) Spreading the risk of reproductive failure when the environment is unpredictable and ephemeral. Peer Community in Evolutionary Biology, 100147. https://doi.org/10.24072/pci.evolbiol.100147
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 #2
DOI or URL of the preprint: https://www.biorxiv.org/content/10.1101/2022.02.24.481784v2
Version of the preprint: 2
Author's Reply, 12 Aug 2022
Decision by Gabriele Sorci, posted 29 Jul 2022
We could only get one review from the referees who read the first version of the manuscript. As you can see, the referee is very happy with the revision but there are still some typos and minor corrections that have been done. I'll be very pleased to recommend this preprint once these minor corrections are done.
Reviewed by Thomas Haaland, 23 Jun 2022
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2022.02.24.481784
Version of the preprint: 1
Author's Reply, 21 Jun 2022
Decision by Gabriele Sorci, posted 17 Mar 2022
Both referees agreed that this is an intersting work. However, they also suggested that some revision is needed in order to improve the clarity of the manuscript. In particular, they thought that more details should be provided on the rationale underlying the definition and use of the reproductive indeces, the structure of the statistical models, the meaning of selection gradient in this context, etc. They also did a terrific job in spotting the typos and mispelling. I am looking forward to seeing the revised version of this nice piece of work.