Time to Eat Your Vegetables: The Role of Circadian Clocks in Insect Herbivory

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

This review focuses on the role of circadian clocks in the relationship between insect herbivory and its host plants. The topic has significant ecological and agricultural value. It systematically summarizes the mechanisms of circadian clocks in insects and plants, their temporal regulatory relationships in herbivory interactions, and potential applications. Overall, the literature coverage is comprehensive, and the rational of most parts is clear. However, the structure, content and writing still could be improved:

 

For the structure:

1. The logical connection between the subsections in chapter 5 should be modified: the transition between evolutionary aspects and specific system cases is abrupt, with no clear logical link between the two parts; cases are presented without classification, making it difficult for readers to quickly grasp core patterns.
2. The section of 6.2, the impacts of climate change on interaction between insects and plants is inadequately integrated with the temporal regulatory mechanisms described in previous chapters, failing to highlight the role of "circadian rhythms" in responding to climate change, the link should be strengthened.
3. The abstract mentions the content "how circadian rhythms influence when insects feed", but the main text provides insufficient explanation on the molecular regulatory mechanisms of insect feeding rhythms, but only briefly mentioned in Chapter 4, with no clear connection to core components of the insect circadian clock. This part of content should be optimized. 

 

For the content

1. There is no explanation about the molecular link between the output pathways of the insect circadian clock and herbivory-related behaviors. This content should be added.
2. Many abbreviations (e.g., HIPV, GSL, PER) are used throughout the text. Although an abbreviation list is provided at the end, no clear definition is given when each abbreviation first appears. Some terms (e.g., "chronoculture", "chronotoxicity") lack popular explanations, so not easy to understand for readers outside the specialized field.

 

For writing

1. Some paragraphs contain redundant information. For example, the rhythmic accumulation of JA is mentioned in both Chapter 3 and Chapter 5, should be integrated.
2. Some long sentences have complex structures, such as line 67-69: "Clock-controlled rhythms in both insects and plants contribute to the ecological dynamics of herbivory, through the temporal alignment of insect behaviors and plant physiological processes". The sentence is too long and complicated to be understand, should be split to improve readability.

 

Overall, this a very interesting review, the manuscript is suitable for publication in Insects after revision.

Author Response

Comment 1: "This review focuses on the role of circadian clocks in the relationship between insect herbivory and its host plants. The topic has significant ecological and agricultural value. It systematically summarizes the mechanisms of circadian clocks in insects and plants, their temporal regulatory relationships in herbivory interactions, and potential applications. Overall, the literature coverage is comprehensive, and the rational of most parts is clear." "Overall, this a very interesting review, the manuscript is suitable for publication in Insects after revision."

Response 1: We thank the reviewer for this assessment.

Comment 2: "The logical connection between the subsections in chapter 5 should be modified: the transition between evolutionary aspects and specific system cases is abrupt, with no clear logical link between the two parts; cases are presented without classification, making it difficult for readers to quickly grasp core patterns."

Response 2:  We have updated Chapter 5 including a revised introductory paragraph and we have added a column to Table 1 to provide clear classification of the examples.

Comment 3: "The section of 6.2, the impacts of climate change on interaction between insects and plants is inadequately integrated with the temporal regulatory mechanisms described in previous chapters, failing to highlight the role of "circadian rhythms" in responding to climate change, the link should be strengthened."

Response 3: We have made this more clear by revising the third paragraph of this section to more explicitly address this issue. That being said, we do want to limit expansion of the review beyond its intended scope. There is, for example, quite a bit of literature on the molecular basis of circadian control of flowering in plants. However, we prefer to direct the reader to other sources for more information.

Comment 4: "The abstract mentions the content "how circadian rhythms influence when insects feed", but the main text provides insufficient explanation on the molecular regulatory mechanisms of insect feeding rhythms, but only briefly mentioned in Chapter 4, with no clear connection to core components of the insect circadian clock. This part of content should be optimized."

Response 4: It is important to point to the section on clock output in insects (section 2.2.3) in this context, which provides much of what the reviewer is looking for. It does not make sense to replicate this information again in Chapter 4 as we agree with the reviewer's recommendation to limit redundancy.

Comment 5: "There is no explanation about the molecular link between the output pathways of the insect circadian clock and herbivory-related behaviors. This content should be added."

Response 5: Again section 2.2.3 is relevant in this context. Of course, as we point out, more work is to be done to verify whether findings in model insects such as Drosophila melanogaster are applicable to the most relevant insect herbivores.

Comment 6: "Many abbreviations (e.g., HIPV, GSL, PER) are used throughout the text. Although an abbreviation list is provided at the end, no clear definition is given when each abbreviation first appears. Some terms (e.g., "chronoculture", "chronotoxicity") lack popular explanations, so not easy to understand for readers outside the specialized field."

Response 6: We have examined all instances where abbreviations are introduced and made sure that we provide not only a fully written out version of the term, but also explain the concept involved.

Comment 7: "Some paragraphs contain redundant information. For example, the rhythmic accumulation of JA is mentioned in both Chapter 3 and Chapter 5, should be integrated."

Response 7: This issue was addressed. We have kept cross-references within the review to a minimum.

Comment 8: "Some long sentences have complex structures, such as line 67-69: "Clock-controlled rhythms in both insects and plants contribute to the ecological dynamics of herbivory, through the temporal alignment of insect behaviors and plant physiological processes". The sentence is too long and complicated to be understand, should be split to improve readability."

Response 8: We have revised these lines and examined the rest of our manuscript for similar issues.

 

 

Reviewer 2 Report

Comments and Suggestions for Authors

This is an exceedingly important paper because it represents a unique, much-needed synthesis. The material in each section is, by and large, well-known to the relatively small number of specialists in that area, but hardly anyone is versatile  enough to be comfortably informed in multiple sections. I expected to learn a great deal by reading this MS, and I did, and so far I have already tracked down and read a dozen references from it and will read quite a few more.

Allow me to elaborate on both why I consider this paper so important and why it is important  to ME. I work on butterfly ecology and life-history evolution. Those of us who work on insect life cycles generally have a fairly superficial understanding of photoperiod and temperature as regulatory environmental factors. For species with facultative seasonal diapause, most workers are at least dimly aware  that these two factors interact, e.g. in general warmer temperatures require shorter photophases/longer scotophases to induce or permit diapause. We are aware of this as a phenomenon but almost never understand the interaction in depth, and there are very few studies in which the interaction has been characterized quantitatively, leading to testable models that have been tested. I have been trying for years to convince the "Monarch butterfly establishment" that this is a very strong canidate to explain both the decline of the species toward possible endangerment AND the conspicuous alterations in its seasonal biology, including the sudden emergence of winter breeding and the decline of both seasonal migration and roosting, both of which historically have been associated with adult reproductive diapause which is photopriod/T driven but the details of which have not been elaborated. In California the increase of T, especially night T, in the winter roosting areas is well-documented. Yet the "establishment" continues to neglect photoperiodic/T mismatch, instead pushing host plant introductions or availability or the associated issue of infectious parasites as putative but to me much less persuasive explanations.  This paper, when published, gives me exactly the bludgeon I need to make them stand up and take notice. The only reason I haven't done so myself is that I am semi-retired, 80 years old, and frankly not up to the exigencies of such an effort. But the authors of this paper deserve many thanks for throwing a conspicuous spotlight on an effect of climate change that may be profoundly important but has suffered because very few researchers possess the breadth to achieve the kind of synthesis provided here.

Author Response

Comment: This is an exceedingly important paper because it represents a unique, much-needed synthesis. The material in each section is, by and large, well-known to the relatively small number of specialists in that area, but hardly anyone is versatile  enough to be comfortably informed in multiple sections. I expected to learn a great deal by reading this MS, and I did, and so far I have already tracked down and read a dozen references from it and will read quite a few more.

Response: We thank the reviewer for the kind words.