The response of interacting species to biotic seasonal cues
Sex makes them sleepy: host reproductive status induces diapause in a parasitoid population experiencing harsh winters
Recommendation: posted 21 May 2019, validated 22 May 2019
Mennerat, A. and Frago, E. (2019) The response of interacting species to biotic seasonal cues . Peer Community in Ecology, 100022. 10.24072/pci.ecology.100022
In temperate regions, food abundance and quality vary greatly throughout the year, and the ability of organisms to synchronise their phenology to these changes is a key determinant of their reproductive success. Successful synchronisation requires that cues are perceived prior to change, leaving time for physiological adjustments.
But what are the cues used to anticipate seasonal changes? Abiotic factors like temperature and photoperiod are known for their driving role in the phenology of a wide range of plant an animal species [1,2] . Arguably though, biotic cues directly linked to upcoming changes in food abundance could be as important as abiotic factors, but the response of organisms to these cues remains relatively unexplored.
Biotic cues may be particularly important for higher trophic levels because of their tight interaction with the hosts or preys they depend on. In this study Tougeron and colleagues  address this topic using interacting insects, namely herbivorous aphids and the parasitic wasps (or parasitoids) that feed on them. The key finding of the study by Tougeron et al.  is that the host morph in which parasitic wasp larvae develop is a major driver of diapause induction. More importantly, the aphid morph that triggers diapause in the wasp is the one that will lay overwintering eggs in autumn at the onset of harsh winter conditions. Its neatly designed experimental setup also provides evidence that this response may vary across populations as host-dependent diapause induction was only observed in a wasp population that originated from a cold area. As the authors suggests, this may be caused by local adaptation to environmental conditions because, relative to warmer regions, missing the time window to enter diapause in colder regions may have more dramatic consequences. The study also shows that different aphid morphs differ greatly in their chemical composition, and points to particular types of metabolites like sugars and polyols as specific cues for diapause induction.
This study provides a nice example of the complexity of biological interactions, and of the importance of phenological synchrony between parasites and their hosts. The authors provide evidence that phenological synchrony is likely to be achieved via chemical cues derived from the host. A similar approach was used to demonstrate that the herbivorous beetle Leptinotarsa decemlineata uses plant chemical cues to enter diapause . Beetles fed on plants exposed to pre-wintering conditions entered diapause in higher proportions than those fed on control plants grown at normal conditions. As done by Tougeron et al. , in  the authors associated diapause induction to changes in the composition of metabolites in the plant. In both studies, however, the missing piece is to unveil the particular chemical involved, an answer that may be provided by future experiments.
Latitudinal clines in diapause induction have been described in a number of insect species . Correlative studies, in which the phenology of different trophic levels has been monitored, suggest that these clines may in part be governed by lower trophic levels. For example, Phillimore et al.  explored the relative contribution of temperature and of host plant phenology on adult flight periods of the butterfly Anthocharis cardamines. Tougeron et al. , by using aphids and their associated parasitoids, take the field further by moving from observational studies to experiments. Besides, aphids are not only a tractable host-parasite system in the laboratory, they are important agricultural pests. Improving our basic knowledge of their ecological interactions may ultimately contribute to improving pest control techniques. The study by Tougeron et al.  exemplifies the multiple benefits that can be gained from addressing fundamental questions in species that are also directly relevant to society.
 Tauber, M. J., Tauber, C. A., and Masaki, S. (1986). Seasonal Adaptations of Insects. Oxford, New York: Oxford University Press.
 Bradshaw, W. E., and Holzapfel, C. M. (2007). Evolution of Animal Photoperiodism. Annual Review of Ecology, Evolution, and Systematics, 38(1), 1–25. doi: 10.1146/annurev.ecolsys.37.091305.110115
 Tougeron, K., Brodeur, J., Baaren, J. van, Renault, D., and Lann, C. L. (2019b). Sex makes them sleepy: host reproductive status induces diapause in a parasitoid population experiencing harsh winters. bioRxiv, 371385, ver. 6 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/371385
 Izzo, V. M., Armstrong, J., Hawthorne, D., and Chen, Y. (2014). Time of the season: the effect of host photoperiodism on diapause induction in an insect herbivore, Leptinotarsa decemlineata. Ecological Entomology, 39(1), 75–82. doi: 10.1111/een.12066
 Hut Roelof A., Paolucci Silvia, Dor Roi, Kyriacou Charalambos P., and Daan Serge. (2013). Latitudinal clines: an evolutionary view on biological rhythms. Proceedings of the Royal Society B: Biological Sciences, 280(1765), 20130433. doi: 10.1098/rspb.2013.0433
 Phillimore, A. B., Stålhandske, S., Smithers, R. J., and Bernard, R. (2012). Dissecting the Contributions of Plasticity and Local Adaptation to the Phenology of a Butterfly and Its Host Plants. The American Naturalist, 180(5), 655–670. doi: 10.1086/667893
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://doi.org/10.1101/371385
Version of the preprint: 3
Author's Reply, 25 Apr 2019
Decision by Adele Mennerat and Enric Frago, posted 23 Apr 2019
Dear K. Tougeron and co-authors,
We have now read your revised manuscript, as well as your answer to reviewers. Congratulations for all the work done addressing the reviewers' suggestions and questions, and for a neat and thorough experimental study. We are willing to recommend your preprint, but before we do this, could you please consider the following suggestions for edits and upload a new version of your preprint?
Thanks in advance,
Adele Mennerat & Enric Frago.
L46: trait expression (remove hyphen)
L59: across time -> over time
L74: contributes to maintain -> contributes to maintaining
L75: reproductive cycle (remove hyphen)
L91: detangled -> disentangled
L124: the mild winter area (add "the")
L125: diapause-inducing cues (add hyphen)
L126: and to the relative occurrence
L127: respective area of origin -> respective areas of origin
L134: origins -> origin
L135: , which (comma before which)
L142: half of the grandparent was -> either "half of the grandparent generation" or "half of the grandparents"
L143: , it is thus likely... -> . It is thus likely... (break sentence in two)
L144: fava bean -> fava beans
L166: allows to measuring -> allows to measure
L272: summed up among -> summed up within
L297: in some female's brood -> in some broods
L325: lines may be confounded -> lines may be overlapping?
L363: one species needs to synchronize its life cycle -> species need to synchronize their life cycle
L380: within each female's offspring -> across broods of individual females (?)
L381: in a lower extent -> to a lower extent
L382: the response of diapause inducing cues -> the response to diapause-inducing cues
L423: comma before which
L430: the importance of each cue at inducing diapause -> importance for diapause induction (?)
L432: parasitoid's response -> the response of parasitoids
L481: glycerol, a cryoprotective compound (add comma)
Evaluation round #1
DOI or URL of the preprint: 10.1101/371385
Version of the preprint: 1
Author's Reply, 11 Apr 2019
Decision by Adele Mennerat and Enric Frago, posted 22 Oct 2018
We have now received two reviews for your preprint, and would like to apologize for the long delay. It was very difficult to get reviewers during the summer. Based on the reviews and our own reading, we find this preprint mostly interesting and well written. The study is carefully designed, and its main asset lies in the fact that several factors are tested simultaneously (harsh/mild climate at the site of origin, host morph, and seasonal abiotic conditions).
As you will see however, the reviewers raise a number of points that, if addressed, can further improve the quality of your manuscript. We would therefore like you to revise your manuscript.
As suggested by one of the reviewers, we believe that you don't have real replicates in terms of populations originating from harsh/mild winters as a single population from each condition was used. As suggested by reviewer 2 this issue is not likely to invalidate your findings, but this has to be carefully discussed in your manuscript.
We would like to raise your attention on many other comments made by reviewer 2, we find them really useful, particularly those concerning the genetic variation in plasticity in diapause induction and the potential inference of reaction norms in the insects studied. Adding this aspect(s) to your study would further increase both its quality and relevance.
We also think that the title and abstract should more explicitly state that diapause levels vary mainly between harsh and mild winter areas, and that diapause induction in oviparous hosts is observed in the harsh winter area only. This would not make your abstract any weaker; on the contrary, the two findings make more sense when taken together. The abstract and some parts of the introduction sections are a bit too technical, we believe that writing some parts of the manuscript using less field-specific jargon would help your manuscript to be read by non-experts on the field.
Please also state the sample sizes more explicitly and report your statistical results in a summary table (including also some information on the random effects). You will see that the reviewers’ opinions differ on Figure 3. We would suggest you to keep the PCA plots (both detailed and per metabolite category), but to move the contributions of variables to Supplementary materials, as this would allow you to increase the legend size and readability. Could you also specify somewhere in your manuscript - or supplementary material - whether the patterns found in each of the two repeated experiments were consistent with each other?
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