Evolutionary and ecological perspectives on the wheat phenotype

Technologies, from molecular genetics to precision agriculture, are outpacing theory, which is becoming a bottleneck for crop improvement. Here, we outline theoretical insights on the wheat phenotype from the perspective of three evolutionary and ecologically important relations—mother–offspring, plant–insect and plant–plant. The correlation between yield and grain number has been misinterpreted as cause-and-effect; an evolutionary perspective shows a striking similarity between crop and fishes. Both respond to environmental variation through offspring number; seed and egg size are conserved. The offspring of annual plants and semelparous fishes, lacking parental care, are subject to mother–offspring conflict and stabilizing selection. Labile reserve carbohydrates do not fit the current model of wheat yield; they can stabilize grain size, but involve trade-offs with root growth and grain number, and are at best neutral for yield. Shifting the focus from the carbon balance to an ecological role, we suggest that labile carbohydrates may disrupt aphid osmoregulation, and thus contribute to wheat agronomic adaptation. The tight association between high yield and low competitive ability justifies the view of crop yield as a population attribute whereby the behaviour of the plant becomes subordinated within that of the population, with implications for genotyping, phenotyping and plant breeding.


Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. No
It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Do you have any ethical concerns with this paper? No
Comments to the Author This paper purports to offer provide theoretical insights into the results of artificial selection from evolutionary and ecological biology, but these insights are not all firmly established. I shall concentrate on two: mother-offspring conflict, and trade-offs between root growth and grain number.
The evidence supposed to bear on mother-offspring conflict is in Fig. 2, which shows that wheat and salmon do not adjust offspring size when availability of resources varies. But this is not what mother-offspring conflict is about. Mother-offspring conflict is seen in evolutionary biology as occurring when genes are selected in offspring to obtain more resources from the mother than independent genes in the mother are selected to provide. The genes in the mother and in the offspring are considered as occurring at different loci, and expressed at different phenotypic ages. See Burt and Trivers: Genes in Conflict. It is not clear that the paper has anything to do with mother-offspring conflict.
In considering trade-offs between root growth and grain number, Section 3 of the paper shows that wheat plants allocate resources to reserves (WSC) as well as reproduction, so the allocation to reproduction is not fixed. The allocation to reserves increased in a five-decade selection experiment (Fig. 3d,e), and osmotic potential decreased as a correlated response (Fig. 3f). Section 4 shows that the high allocation to reserves may defend against aphids. While I see this may be interesting, it is does not seem unexpected to me.
Quality of the paper: Is the overall quality of the paper suitable? Excellent

Is the length of the paper justified? Yes
Should the paper be seen by a specialist statistical reviewer? No Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. No It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Do you have any ethical concerns with this paper? No
Comments to the Author A Darwinian view of the wheat phenotype; Victor Sadras; Proc Royal Soc A refreshing view on phenotyping with some valuable new insights. Please see comments below LINES 102-103 resources are difficult to estimate but crop growth rate in the critical period of grain set is a sound approximation [48,50] THIS IS A BIG ASSUMPTION AND IT SHOULD BE BETTER JUSTIFIED, DON'T EXPECT READERS NECESSARILY TO REFER BACK THE REVIEWS CITED.
108-114 EGR-GN is the efficiency of conversion of growth rate per unit grain size into grain number Crops with more resources allocated to reserve will have lower efficiency to produce grain Likewise, EGR-GN is expected to decline with increasing allocation of resources to root. How, therefore, selection for yield and agronomic adaptation has favoured traits -amount and concentration of labile reserve carbohydrates -that are at best neutral for yield…correlates with yet unrecognized, agronomically important traits.

THE LARGE GENETIC VARIATION EXPRESSED FOR RESERVES AMONG ELITE LINES -AT LEAST IN SPRING WHEAT-DOES SUGGEST TRADE-OFFS WITH OTHER PROCESSES, ROOTS BEING PERHAPS JUST ONE OF MANY.
156-159 This is illustrated in figure 4a, showing the relative growth rate of pea aphid (Acyrthosiphon pisum) was impaired by reduced feeding, reflecting the importance of sucrose as a phagostimulant at low dietary sucrose concentrations, and by osmoregulation failure at high concentrations DID YOU MEAN TO SAY "IMPAIRED BY REDUCED FEEDING" ? It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Do you have any ethical concerns with this paper? No
Comments to the Author This manuscript presents some innovative hypotheses, and the basic point: that agricultural research needs more theoretical developments if modern technologies and data are to be applied in useful ways, is certainly correct. I do see some minor issues, which I urge the author to consider.
The fact that plants produce a distribution of seed (here grain) sizes, and they vary the number of seeds produced in response to their conditions was documented by Harper in the 1970's and described in detail in his book on plant population biology -it is far from new. However, many agronomists will point out that this idea can be taken too far. Pruning experiments on beans (by G.E. Blackman if I remember correctly) over 50 years ago, showed that when all meristems were removed after flowering started so the plant could not grow more, plants did produce larger seeds when supplied with more resources. This is the "exception that proves the rule" that plants will do everything possible to respond with seed number rather than seed size. A more relevant example here is that, if a wheat field is fertilized early in the season, the plants will be larger and produce more grains, but if fertilization occurs after flowering when plants can no longer produce new flowering tillers, grains will be larger and have higher N content, which is important for yield quality.
I found the hypothesis that the high levels of WSC in in what plants is an evolved response to aphids intriguing, but not convincing. Have aphids been evolutionarily more important than other insect pests, especially chewing insects for which high levels of WSC would probably be a disadvantage? This hypothesis also suggests that much higher yield could be obtained if aphids are controlled and the level of WSC were used to increase yield. One would think that such behaviour would have appeared through breeding for high yield under high resource high pesticide applications -which represents much of the wheat breeding over the past 60 years. If there is a trade-off between WSC and root growth, it is not clear why there is no trade-off with yield. In any case, this is not a criticism of the manuscript. Agricultural research needs new ideas and hypotheses. Even if this hypothesis does not stand up to critical analyses, it can still be considered a useful contribution, because it will inspire alternative hypotheses.
Finally: What's in a title? For better or for worse, a title is important, and the current title is misleading. "Darwinian" is a now popular word in some agricultural research circles, and it has been promoted by Denison. But group selection, the basis of Dension's work and section 5 of the current manuscript, is actually anti-Darwinian. The same is true for earlier parts of the paper, in which population-level characteristics are considered drivers of yield production. For Darwin, evolution is driven by individuals and their offspring, although it is the population that evolves. Thus, while I have no objection to quoting Darwin throughout the paper, the title does not represent "truth in advertising". I would suggest something like "An evolutionary view..." or "An evolutionary-ecological view..." What is Darwinian here is the change in emphasis from the plant and its abiotic environment (which Harper called "Wallacian") to the plant and its biotic environment (which he called Darwinian). This change in emphasis is long overdue, especially in crop physiology. Some minor comments: l. 46 "abiotic factors" would be a better term than "the elements" and "respond to" would be less adaptationist than "accommodate" (also in Fig. 1 legend) l. 54 remove "this is universal" -it is not. Some horticultural crops have been selected to not overproduce flowers. I'm sure there are also exceptions in wild plants. Such universality is not common in the plant kingdom.
l. 92-94 The emphasis on resources is totally appropriate, but conditions, as well as resources, can limit growth.
ll. 95-98 -"The first assumption is that plants are able to account for past, current and future environmental conditions by combining memory mechanisms including epigenetics, proximate environmental cues such as direct sensing of water and nutrient availability in soil, and cues such as photoperiod that allow for future conditions..." This is extremely adaptationist and expects more of crop plants than is reasonable. Plants are not omnipotent, as this sentence implies. Constraints are as important as abilities in agriculture.

06-Jul-2021
Dear Dr Sadras: Your manuscript has now been peer reviewed and the reviewers' comments (not including confidential comments to the Editor) are included at the end of this email for your reference. As you will see, the reviewers have raised some concerns with your manuscript -for one of these (referee 1) the points are sufficiently serious to merit a recommendation of rejection but referees 2 and 3 consider that their points could be addressed in a revision. My view is that the necessary changes are potentially achievable without this being a totally new manuscript, so I would like to give you the chance to revise your manuscript. And I do agree with referee 3 about the title.
We do not allow multiple rounds of revision so we urge you to make every effort to fully address all of the comments at this stage. If deemed necessary by the Associate Editor, your manuscript will be sent back to one or more of the original reviewers for assessment. If the original reviewers are not available we may invite new reviewers. Please note that we cannot guarantee eventual acceptance of your manuscript at this stage.
To submit your revision please log into http://mc.manuscriptcentral.com/prsb and enter your Author Centre, where you will find your manuscript title listed under "Manuscripts with Decisions." Under "Actions", click on "Create a Revision". Your manuscript number has been appended to denote a revision.
When submitting your revision please upload a file under "Response to Referees" in the "File Upload" section. This should document, point by point, how you have responded to the reviewers' and Editors' comments, and the adjustments you have made to the manuscript. We require a copy of the manuscript with revisions made since the previous version marked as 'tracked changes' to be included in the 'response to referees' document.
Your main manuscript should be submitted as a text file (doc, txt, rtf or tex), not a PDF. Your figures should be submitted as separate files and not included within the main manuscript file.
When revising your manuscript you should also ensure that it adheres to our editorial policies (https://royalsociety.org/journals/ethics-policies/). You should pay particular attention to the following: Research ethics: If your study contains research on humans please ensure that you detail in the methods section whether you obtained ethical approval from your local research ethics committee and gained informed consent to participate from each of the participants.
Use of animals and field studies: If your study uses animals please include details in the methods section of any approval and licences given to carry out the study and include full details of how animal welfare standards were ensured. Field studies should be conducted in accordance with local legislation; please include details of the appropriate permission and licences that you obtained to carry out the field work.
Data accessibility and data citation: It is a condition of publication that you make available the data and research materials supporting the results in the article (https://royalsociety.org/journals/authors/authorguidelines/#data). Datasets should be deposited in an appropriate publicly available repository and details of the associated accession number, link or DOI to the datasets must be included in the Data Accessibility section of the article (https://royalsociety.org/journals/ethicspolicies/data-sharing-mining/). Reference(s) to datasets should also be included in the reference list of the article with DOIs (where available).
In order to ensure effective and robust dissemination and appropriate credit to authors the dataset(s) used should also be fully cited and listed in the references.
If you wish to submit your data to Dryad (http://datadryad.org/) and have not already done so you can submit your data via this link http://datadryad.org/submit?journalID=RSPB&manu=(Document not available), which will take you to your unique entry in the Dryad repository.
If you have already submitted your data to dryad you can make any necessary revisions to your dataset by following the above link.
For more information please see our open data policy http://royalsocietypublishing.org/datasharing.
Electronic supplementary material: All supplementary materials accompanying an accepted article will be treated as in their final form. They will be published alongside the paper on the journal website and posted on the online figshare repository. Files on figshare will be made available approximately one week before the accompanying article so that the supplementary material can be attributed a unique DOI. Please try to submit all supplementary material as a single file.
Online supplementary material will also carry the title and description provided during submission, so please ensure these are accurate and informative. Note that the Royal Society will not edit or typeset supplementary material and it will be hosted as provided. Please ensure that the supplementary material includes the paper details (authors, title, journal name, article DOI). Your article DOI will be 10.1098/rspb.[paper ID in form xxxx.xxxx e.g. 10.1098/rspb.2016.0049].
Please submit a copy of your revised paper within three weeks. If we do not hear from you within this time your manuscript will be rejected. If you are unable to meet this deadline please let us know as soon as possible, as we may be able to grant a short extension.
Thank you for submitting your manuscript to Proceedings B; we look forward to receiving your revision. If you have any questions at all, please do not hesitate to get in touch.

Best wishes, Innes Cuthill
Prof. Innes Cuthill Reviews Editor mailto: proceedingsb@royalsociety.org Reviewer(s)' Comments to Author: Referee: 1 Comments to the Author(s) This paper purports to offer provide theoretical insights into the results of artificial selection from evolutionary and ecological biology, but these insights are not all firmly established. I shall concentrate on two: mother-offspring conflict, and trade-offs between root growth and grain number.
The evidence supposed to bear on mother-offspring conflict is in Fig. 2, which shows that wheat and salmon do not adjust offspring size when availability of resources varies. But this is not what mother-offspring conflict is about. Mother-offspring conflict is seen in evolutionary biology as occurring when genes are selected in offspring to obtain more resources from the mother than independent genes in the mother are selected to provide. The genes in the mother and in the offspring are considered as occurring at different loci, and expressed at different phenotypic ages. See Burt and Trivers: Genes in Conflict. It is not clear that the paper has anything to do with mother-offspring conflict.
In considering trade-offs between root growth and grain number, Section 3 of the paper shows that wheat plants allocate resources to reserves (WSC) as well as reproduction, so the allocation to reproduction is not fixed. The allocation to reserves increased in a five-decade selection experiment (Fig. 3d,e), and osmotic potential decreased as a correlated response (Fig. 3f). Section 4 shows that the high allocation to reserves may defend against aphids. While I see this may be interesting, it is does not seem unexpected to me.
Referee: 2 Comments to the Author(s) A Darwinian view of the wheat phenotype; Victor Sadras; Proc Royal Soc A refreshing view on phenotyping with some valuable new insights. Please see comments below LINES 102-103 resources are difficult to estimate but crop growth rate in the critical period of grain set is a sound approximation [48,50] THIS IS A BIG ASSUMPTION AND IT SHOULD BE BETTER JUSTIFIED, DON'T EXPECT READERS NECESSARILY TO REFER BACK THE REVIEWS CITED.
108-114 EGR-GN is the efficiency of conversion of growth rate per unit grain size into grain number Crops with more resources allocated to reserve will have lower efficiency to produce grain Likewise, EGR-GN is expected to decline with increasing allocation of resources to root.  Comments to the Author(s) This manuscript presents some innovative hypotheses, and the basic point: that agricultural research needs more theoretical developments if modern technologies and data are to be applied in useful ways, is certainly correct. I do see some minor issues, which I urge the author to consider.
The fact that plants produce a distribution of seed (here grain) sizes, and they vary the number of seeds produced in response to their conditions was documented by Harper in the 1970's and described in detail in his book on plant population biology -it is far from new. However, many agronomists will point out that this idea can be taken too far. Pruning experiments on beans (by G.E. Blackman if I remember correctly) over 50 years ago, showed that when all meristems were removed after flowering started so the plant could not grow more, plants did produce larger seeds when supplied with more resources. This is the "exception that proves the rule" that plants will do everything possible to respond with seed number rather than seed size. A more relevant example here is that, if a wheat field is fertilized early in the season, the plants will be larger and produce more grains, but if fertilization occurs after flowering when plants can no longer produce new flowering tillers, grains will be larger and have higher N content, which is important for yield quality.
I found the hypothesis that the high levels of WSC in in what plants is an evolved response to aphids intriguing, but not convincing. Have aphids been evolutionarily more important than other insect pests, especially chewing insects for which high levels of WSC would probably be a disadvantage? This hypothesis also suggests that much higher yield could be obtained if aphids are controlled and the level of WSC were used to increase yield. One would think that such behaviour would have appeared through breeding for high yield under high resource high pesticide applications -which represents much of the wheat breeding over the past 60 years. If there is a trade-off between WSC and root growth, it is not clear why there is no trade-off with yield. In any case, this is not a criticism of the manuscript. Agricultural research needs new ideas and hypotheses. Even if this hypothesis does not stand up to critical analyses, it can still be considered a useful contribution, because it will inspire alternative hypotheses.
Finally: What's in a title? For better or for worse, a title is important, and the current title is misleading. "Darwinian" is a now popular word in some agricultural research circles, and it has been promoted by Denison. But group selection, the basis of Dension's work and section 5 of the current manuscript, is actually anti-Darwinian. The same is true for earlier parts of the paper, in which population-level characteristics are considered drivers of yield production. For Darwin, evolution is driven by individuals and their offspring, although it is the population that evolves. Thus, while I have no objection to quoting Darwin throughout the paper, the title does not represent "truth in advertising". I would suggest something like "An evolutionary view..." or "An evolutionary-ecological view..." What is Darwinian here is the change in emphasis from the plant and its abiotic environment (which Harper called "Wallacian") to the plant and its biotic environment (which he called Darwinian). This change in emphasis is long overdue, especially in crop physiology. Some minor comments: l. 46 "abiotic factors" would be a better term than "the elements" and "respond to" would be less adaptationist than "accommodate" (also in Fig. 1 legend) l. 54 remove "this is universal" -it is not. Some horticultural crops have been selected to not overproduce flowers. I'm sure there are also exceptions in wild plants. Such universality is not common in the plant kingdom.
l. 92-94 The emphasis on resources is totally appropriate, but conditions, as well as resources, can limit growth.
ll. 95-98 -"The first assumption is that plants are able to account for past, current and future environmental conditions by combining memory mechanisms including epigenetics, proximate environmental cues such as direct sensing of water and nutrient availability in soil, and cues such as photoperiod that allow for future conditions..." This is extremely adaptationist and expects more of crop plants than is reasonable. Plants are not omnipotent, as this sentence implies. Constraints are as important as abilities in agriculture.

Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. No
It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Do you have any ethical concerns with this paper? No
Comments to the Author All good now, except I suggest the response to the comment below be to make it explicit that even enzymes shaped by natural selection may need to be modified -or genetic variation tappedto fits the unique crop canopy environment. That was at best ambiguous in the original statement. Decision letter (RSPB-2021-1259.R1)

11-Aug-2021
Dear Dr Sadras I am pleased to inform you that your manuscript RSPB-2021-1259.R1 entitled "Evolutionary and ecological perspectives on the wheat phenotype" has been accepted for publication in Proceedings B.
The referee is happy with your revisions and has recommended publication, but also suggests a further minor revision to your manuscript. Therefore, I invite you to respond to the comments and revise your manuscript. Because the schedule for publication is very tight, it is a condition of publication that you submit the revised version of your manuscript within 7 days. If you do not think you will be able to meet this date please let us know.
To revise your manuscript, log into https://mc.manuscriptcentral.com/prsb and enter your Author Centre, where you will find your manuscript title listed under "Manuscripts with Decisions." Under "Actions," click on "Create a Revision." Your manuscript number has been appended to denote a revision. You will be unable to make your revisions on the originally submitted version of the manuscript. Instead, revise your manuscript and upload a new version through your Author Centre.
When submitting your revised manuscript, you will be able to respond to the comments made by the referee(s) and upload a file "Response to Referees". You can use this to document any changes you make to the original manuscript. We require a copy of the manuscript with revisions made since the previous version marked as 'tracked changes' to be included in the 'response to referees' document.
Before uploading your revised files please make sure that you have: 1) A text file of the manuscript (doc, txt, rtf or tex), including the references, tables (including captions) and figure captions. Please remove any tracked changes from the text before submission. PDF files are not an accepted format for the "Main Document".
2) A separate electronic file of each figure (tiff, EPS or print-quality PDF preferred). The format should be produced directly from original creation package, or original software format. PowerPoint files are not accepted.
3) Electronic supplementary material: this should be contained in a separate file and where possible, all ESM should be combined into a single file. All supplementary materials accompanying an accepted article will be treated as in their final form. They will be published alongside the paper on the journal website and posted on the online figshare repository. Files on figshare will be made available approximately one week before the accompanying article so that the supplementary material can be attributed a unique DOI.
Online supplementary material will also carry the title and description provided during submission, so please ensure these are accurate and informative. Note that the Royal Society will not edit or typeset supplementary material and it will be hosted as provided. Please ensure that the supplementary material includes the paper details (authors, title, journal name, article DOI). Your article DOI will be 10.1098/rspb.[paper ID in form xxxx.xxxx e.g. 10.1098/rspb.2016.0049]. 4) A media summary: a short non-technical summary (up to 100 words) of the key findings/importance of your manuscript.

5) Data accessibility section and data citation
It is a condition of publication that data supporting your paper are made available either in the electronic supplementary material or through an appropriate repository (https://royalsociety.org/journals/authors/author-guidelines/#data).
In order to ensure effective and robust dissemination and appropriate credit to authors the dataset(s) used should be fully cited. To ensure archived data are available to readers, authors should include a 'data accessibility' section immediately after the acknowledgements section. This should list the database and accession number for all data from the article that has been made publicly available, for instance: • DNA sequences: Genbank accessions F234391-F234402 • Phylogenetic data: TreeBASE accession number S9123 • Final DNA sequence assembly uploaded as online supplemental material • Climate data and MaxEnt input files: Dryad doi:10.5521/dryad.12311 NB. From April 1 2013, peer reviewed articles based on research funded wholly or partly by RCUK must include, if applicable, a statement on how the underlying research materials -such as data, samples or models -can be accessed. This statement should be included in the data accessibility section.
If you wish to submit your data to Dryad (http://datadryad.org/) and have not already done so you can submit your data via this link http://datadryad.org/submit?journalID=RSPB&manu=(Document not available) which will take you to your unique entry in the Dryad repository. If you have already submitted your data to dryad you can make any necessary revisions to your dataset by following the above link. Please see https://royalsociety.org/journals/ethics-policies/data-sharing-mining/ for more details.
6) For more information on our Licence to Publish, Open Access, Cover images and Media summaries, please visit https://royalsociety.org/journals/authors/author-guidelines/.
Once again, thank you for submitting your manuscript to Proceedings B and I look forward to receiving your revision. If you have any questions at all, please do not hesitate to get in touch.

Best wishes, Innes Cuthill
Prof. Innes Cuthill Reviews Editor, Proceedings B mailto: proceedingsb@royalsociety.org Reviewer(s)' Comments to Author: Referee: 2 Comments to the Author(s) All good now, except I suggest the response to the comment below be to make it explicit that even enzymes shaped by natural selection may need to be modified -or genetic variation tappedto fits the unique crop canopy environment. That was at best ambiguous in the original statement. Decision letter (RSPB-2021-1259.R2)

12-Aug-2021
Dear Dr Sadras I am pleased to inform you that your manuscript entitled "Evolutionary and ecological perspectives on the wheat phenotype" has been accepted for publication in Proceedings B.
You can expect to receive a proof of your article from our Production office in due course, please check your spam filter if you do not receive it. PLEASE NOTE: you will be given the exact page length of your paper which may be different from the estimation from Editorial and you may be asked to reduce your paper if it goes over the 10 page limit.
If you are likely to be away from e-mail contact during this period, let us know. Due to rapid publication and an extremely tight schedule, if comments are not received, we may publish the paper as it stands.
If you have any queries regarding the production of your final article or the publication date please contact procb_proofs@royalsociety.org Your article has been estimated as being 10 pages long. Our Production Office will be able to confirm the exact length at proof stage.
Data Accessibility section Please remember to make any data sets live prior to publication, and update any links as needed when you receive a proof to check. It is good practice to also add data sets to your reference list. The open access fee is £1,700 per article (plus VAT for authors within the EU). If you wish to opt for open access then please let us know as soon as possible.
Paper charges An e-mail request for payment of any related charges will be sent out shortly. The preferred payment method is by credit card; however, other payment options are available.
Electronic supplementary material: All supplementary materials accompanying an accepted article will be treated as in their final form. They will be published alongside the paper on the journal website and posted on the online figshare repository. Files on figshare will be made available approximately one week before the accompanying article so that the supplementary material can be attributed a unique DOI.
You are allowed to post any version of your manuscript on a personal website, repository or preprint server. However, the work remains under media embargo and you should not discuss it with the press until the date of publication. Please visit https://royalsociety.org/journals/ethicspolicies/media-embargo for more information.
Thank you for your fine contribution. On behalf of the Editors of the Proceedings B, we look forward to your continued contributions to the Journal.

Prof. Innes Cuthill Reviews Editor
Thanks for your editorial input, reports of three reviewers, and the opportunity to submit a revised version of my article.
I have addressed all comments as explained in the question-answer section below. The title has been changed as proposed. Key words were updated to account for the change in title. The most important change relates to Reviewer 1 comment on mother-offspring conflict. The original ms relied excessively on references. To correct this, the revised ms (i) spells out the mother-offspring conflict and (ii) includes a new Fig. 2b. The revised version is 3100 words including abstract.
Below please also find the revised ms with track changes. Sincerely,

Victor Sadras
Appendix A Referee: 1 Comments to the Author(s) This paper purports to offer provide theoretical insights into the results of artificial selection from evolutionary and ecological biology, but these insights are not all firmly established. I shall concentrate on two: mother-offspring conflict, and trade-offs between root growth and grain number.
The evidence supposed to bear on mother-offspring conflict is in Fig. 2, which shows that wheat and salmon do not adjust offspring size when availability of resources varies. But this is not what mother-offspring conflict is about. Mother-offspring conflict is seen in evolutionary biology as occurring when genes are selected in offspring to obtain more resources from the mother than independent genes in the mother are selected to provide. The genes in the mother and in the offspring are considered as occurring at different loci, and expressed at different phenotypic ages. See Burt and Trivers: Genes in Conflict. It is not clear that the paper has anything to do with mother-offspring conflict. Agree with this comment; Fig. 2 and associated text do not show mother-offspring conflict. The original ms relied excessively on references. To correct this, the revised ms (i) spells out the mother-offspring conflict with supporting references, and (ii) includes new Fig. 2b.
In considering trade-offs between root growth and grain number, Section 3 of the paper shows that wheat plants allocate resources to reserves (WSC) as well as reproduction, so the allocation to reproduction is not fixed. The allocation to reserves increased in a five-decade selection experiment (Fig. 3d,e), and osmotic potential decreased as a correlated response (Fig. 3f). Section 4 shows that the high allocation to reserves may defend against aphids. While I see this may be interesting, it is does not seem unexpected to me. Thanks for comment and good summary. Here the point is that the dominant view in plant breeding has been that reserves buffer grain size, and therefore efforts have been allocated to incorporate WSC in breeding programs -crosses were done, populations screened, and QTL identified. Del Pozo in Chile and Ovenden in Australia are examples of massive investments of money and time along these lines (del Pozo et al., 2016;Ovenden et al., 2017). The rationale in Ovenden et al reads: "The potential to increase the genetic capacity for water-soluble carbohydrate (WSC) accumulation is an opportunity to improve the drought tolerance capability of rainfed wheat varieties..." These large investments have failed because the model of the phenotype was incomplete: trade-offs (with grain number and root biomass) and osmotic effects were completely overlooked. This is a primary motivation of this article as stated in introduction and conclusion. The relationship between seed number and growth rate has been verified in wheat, pulses, soybean, maize, sunflower. The graph below is typical. Please also see Fig. 3a supporting the strong correlation growth rategrain number.
108-114 EGR-GN is the efficiency of conversion of growth rate per unit grain size into grain number Crops with more resources allocated to reserve will have lower efficiency to produce grain Likewise, EGR-GN is expected to decline with increasing allocation of resources to root.

156-159
This is illustrated in figure 4a, showing the relative growth rate of pea aphid (Acyrthosiphon pisum) was impaired by reduced feeding, reflecting the importance of sucrose as a phagostimulant at low dietary sucrose concentrations, and by osmoregulation failure at high concentrations DID YOU MEAN TO SAY "IMPAIRED BY REDUCED FEEDING" ? Original ms was correct, no changes.

173-177
Empirical evidence linking labile reserve carbohydrates and aphid tolerance is just emerging, but the view of an ecological role of labile carbohydrates opens a new dimension to the established, narrow focus on plant carbon balance and source-sink relations. AGREED, THIS GIVES NEW BREADTH TO THE TERM "ECO-PHYSIOLOGICAL TRAITS". OK, no change in response to this comment.

222-225
First, plant breeding is unlikely to improve traits shaped by natural selection over evolutionary time scales, such as the efficiency of photosynthetic enzymes [78,87] Comments to the Author(s) This manuscript presents some innovative hypotheses, and the basic point: that agricultural research needs more theoretical developments if modern technologies and data are to be applied in useful ways, is certainly correct. I do see some minor issues, which I urge the author to consider.
The fact that plants produce a distribution of seed (here grain) sizes, and they vary the number of seeds produced in response to their conditions was documented by Harper in the 1970's and described in detail in his book on plant population biology -it is far from new. However, many agronomists will point out that this idea can be taken too far. Pruning experiments on beans (by G.E. Blackman if I remember correctly) over 50 years ago, showed that when all meristems were removed after flowering started so the plant could not grow more, plants did produce larger seeds when supplied with more resources. This is the "exception that proves the rule" that plants will do everything possible to respond with seed number rather than seed size. A more relevant example here is that, if a wheat field is fertilized early in the season, the plants will be larger and produce more grains, but if fertilization occurs after flowering when plants can no longer produce new flowering tillers, grains will be larger and have higher N content, which is important for yield quality. OK. I completely agree the number-size trade-off is not new. The point of discussion is the interpretation of the correlation yield-grain number, and the shift from misconstructed cause-and-effect to a broader view informed by evolutionary perspective. This was expanded in the revised ms.
I found the hypothesis that the high levels of WSC in in what plants is an evolved response to aphids intriguing, but not convincing. Have aphids been evolutionarily more important than other insect pests, especially chewing insects for which high levels of WSC would probably be a disadvantage? This hypothesis also suggests that much higher yield could be obtained if aphids are controlled and the level of WSC were used to increase yield. One would think that such behaviour would have appeared through breeding for high yield under high resource high pesticide applications -which represents much of the wheat breeding over the past 60 years. If there is a trade-off between WSC and root growth, it is not clear why there is no tradeoff with yield. In any case, this is not a criticism of the manuscript. Agricultural research needs new ideas and hypotheses. Even if this hypothesis does not stand up to critical analyses, it can still be considered a useful contribution, because it will inspire alternative hypotheses. The reviewer captured well the spirit of this section. I accept the link aphids-WSC is far from proved, and this is explicit in the paper where it reads: "Empirical evidence linking labile reserve carbohydrates and aphid tolerance is just emerging, but the view of an ecological role of labile carbohydrates opens a new dimension to the established, narrow focus on plant carbon balance and source-sink relations." The point is the need for new ideas. We cannot discard the role of other herbivores as pointed out by the reviewer, but the case for aphids is supported by: (a) aphids and the viruses they carry are the major pests of wheat and a focus of breeding programs worldwide and (b) intricate mechanisms for osmoregulation in aphids.
Finally: What's in a title? For better or for worse, a title is important, and the current title is misleading. "Darwinian" is a now popular word in some agricultural research circles, and it has been promoted by Denison. But group selection, the basis of Dension's work and section 5 of the current manuscript, is actually anti-Darwinian. The same is true for earlier parts of the paper, in which populationlevel characteristics are considered drivers of yield production. For Darwin, evolution is driven by individuals and their offspring, although it is the population that evolves. Thus, while I have no objection to quoting Darwin throughout the paper, the title does not represent "truth in advertising". I would suggest something like "An evolutionary view..." or "An evolutionary-ecological view..." What is Darwinian here is the change in emphasis from the plant and its abiotic environment (which Harper called "Wallacian") to the plant and its biotic environment (which he called Darwinian). This change in emphasis is long overdue, especially in crop physiology.
ACCEPTED. The title was changed as suggested to "Evolutionary and ecological perspectives on the wheat phenotype" Some minor comments: l. 46 "abiotic factors" would be a better term than "the elements" and "respond to" would be less adaptationist than "accommodate" (also in Fig. 1 legend). OK changed as proposed.
l. 54 remove "this is universal" -it is not. Some horticultural crops have been selected to not overproduce flowers. I'm sure there are also exceptions in wild plants. Such universality is not common in the plant kingdom. OK, deleted. l. 59 "...we observe that annual..." OK, changed as indicated.
l. 92-94 The emphasis on resources is totally appropriate, but conditions, as well as resources, can limit growth. Agree. Here we assume that the plant has R resources (e.g. total C), which result from Comments to the Author(s) All good now, except I suggest the response to the comment below be to make it explicit that even enzymes shaped by natural selection may need to be modified -or genetic variation tapped-to fits the unique crop canopy environment. That was at best ambiguous in the original statement.
222-225 First, plant breeding is unlikely to improve traits shaped by natural selection over evolutionary time scales, such as the efficiency of photosynthetic enzymes [78,87], but unrealised opportunities may exist for the selection of traits that increase crop yield at the expense of plant fitness [78,88,89 In response to this observation, the revised ms expanded the paragraph in lines 216-225 to make explicit that even enzymes shaped by natural selection may need to be modified -or genetic variation tapped-to fit the current crop environment.