Interactions between breeding system and ploidy affect niche breadth in Solanum

Understanding the factors driving ecological and evolutionary interactions of economically important plant species is important for agricultural sustainability. The geography of crop wild relatives, including wild potatoes (Solanum section Petota), have received attention; however, such information has not been analysed in combination with phylogenetic histories, genomic composition and reproductive systems to identify potential species for use in breeding for abiotic stress tolerance. We used a combination of ordinary least-squares (OLS) and phylogenetic generalized least-squares (PGLM) analyses to identify the discrete climate classes that make up the climate niche that wild potato species inhabit in the context of breeding system and ploidy. Self-incompatible diploid or self-compatible polyploid species significantly increase the number of discrete climate classes within a climate niche inhabited. This result was sustained when correcting for phylogenetic non-independence in the linear model. Our results support the idea that specific breeding system and ploidy combinations increase niche breadth through the decoupling of geographical range and niche diversity, and therefore, these species may be of particular interest for crop adaptation to a changing climate.

1) Unfortunately, it is totally unclear how the data were acquired, especially how the breeding system information and ploidy has been assigned. Do the authors simply fully rely on the previously published works cited in Methods? Even if so it would be worth explaining how the data have been acquired in the original works and potentially critically review their approach. Or did the authors curated the data anyhow, re-assigning the group or updating with potential novel data?. Specifically: -How the ploidy was assigned to a each species? What is the basic chromosome number for Solanum and which 2n= value is thus assigned to be a diploid and tetraploid? In how many cases more chromosome counts have been recorded per species and in what proportion of such cases intraspecific ploidy variation has been observed (e.g. diploid and tetraploid chromosome counts in one species)? How ploidy-variable species were then handled (excluded / assigned to both classess?)? Are there higher polyploids than tetraploids in the analysis? -How was self-compatibility assessed and does this trait also vary within some species (it can do, e.g. in Arabidopsis lyrata). If so, how such variable species have been handled? Is there anything known about the outcrossing levels of the SC species (i.e. real manifestation of the breeding system shift in natural populations)?
2) The absolute correlation of ploidy and breeding system (polyploids are always self-compatible asexuals, and this combination of breeding systems is not present in a diploid, l. 108-110) makes impossible to decouple the effect of ploidy and breeding system. This is the nature and it is worth studying, yet under the current natural setup it is impossible to distill the role of ploidy in niche evolution (contrary e.g. to the statements on l. 196). Re-focusing the main aim towards breeding system (taking ploidy into account as a potential side-effect), or the study and/or focusing on different model system may help to address this issue. In the former case, however, I am not sure about the novelty of the study as relatively a lot of work has been done on the relationships between breeding systems and distributions.
Minors: What is "unknown breeding system asexually propagating diploid"? Is it asexual or unknown?
Even putting polyploidy apart, it is also unclear to which extent the expansion of the "self compatible asexual polyploid" category is due o selfing and asexuality. This shall be also taken into account in the Discussion (e.g 208-219)

Decision letter (RSOS-211090.R0)
We hope you are keeping well at this difficult and unusual time. We continue to value your support of the journal in these challenging circumstances. If Royal Society Open Science can assist you at all, please don't hesitate to let us know at the email address below.

Dear Dr Kantar
The Editors assigned to your paper RSOS-211090 "Interactions between breeding system and ploidy affect niche breadth in Solanum" have made a decision based on their reading of the paper and any comments received from reviewers.
Regrettably, in view of the reports received, the manuscript has been rejected in its current form. However, a new manuscript may be submitted which takes into consideration these comments.
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Please resubmit your revised manuscript and required files (see below) no later than 21-Apr-2022. Note: the ScholarOne system will 'lock' if resubmission is attempted on or after this deadline. If you do not think you will be able to meet this deadline, please contact the editorial office immediately.
Please note article processing charges apply to papers accepted for publication in Royal Society Open Science (https://royalsocietypublishing.org/rsos/charges). Charges will also apply to papers transferred to the journal from other Royal Society Publishing journals, as well as papers submitted as part of our collaboration with the Royal Society of Chemistry (https://royalsocietypublishing.org/rsos/chemistry). Fee waivers are available but must be requested when you submit your manuscript (https://royalsocietypublishing.org/rsos/waivers). We've now had two reviews on your manuscript. Both reviewers raise very different but pertinent issues: one disputes that a) the definition of a climatic niche is adequate and b) that climate zones are not categorical entities, and therefore the manuscript does not adequately represent an analysis of niche breadth. This seems more than a semantic discussion on the term 'niche'.
The second reviewer highlights that ploidy and mating system co-vary to a large extent, as a result of which a decoupling between ploidy and mating system is not possible (line 109: all polyploids are self-compatible asexuals).
As for myself, I had a hard time understanding some concepts. How is a an asexual species selfcompatible? If it's asexual, self-incompatibility is irrelevant, no? If on the other hand it depends on pollination, it's not asexually propagating. This conundrum shows that much clearer definitions of what is understood by the different mating systems are required in the text, as we are not speaking the same language here.
Next, you talk about polyploid versus diploid species, yet you also consider "species" having both asexual polyploids, and sexual diploids. To what extent is this sensitive to "advances in taxonomic insight?" When asexuality and polyploidy are involved, the boundaries of species are often arbitrary and a matter of convention, rather than representing clear biological or evolutionary units. Hence, are all 'species' equivalent? What may be considered a single species with a large variation in ploidy and mating systems, may already have been split into various distinct species in another taxon. To what extent is this analysis sensitive to such taxonomic idiosyncracies? One may even argue to what extent it is useful to consider evolutionary distinct entities together (polyploid vs diploid, sexual vs asexual), even though they are considered as part of the same taxonomic man-made box. Do the polyploids in a 'species' containing both diploid and polyploid lineages have a larger niche breadth than the polyploids in a 'species' containing only polyploids? And is this niche diversity dependent on the sample size (was a same number of lineages considered for each group?). Each asexual lineage could have its own narrow niche (and the combination of all lineages may show a broad niche). Alternatively, asexual polyploid lineages may indeed have broad niches. This is a classical question in the evolutionary biology and ecology of asexuality.
Overall, there are a few fundamental issues that need to be resolved and clarified before this work can be considered any further. I am sorry to disappoint you with this decision, but hope it will help you improve a revised manuscript.

Sincerely, Joachim Mergeay
Reviewer comments to Author: Reviewer: 1 Comments to the Author(s) The paper by Fumia and co-workers is a good attempt to characterize niche attributes through climate classes and search for signals of phylogenetic interactions with breeding systems and ploidy in species from Solanum. Overall the paper is well-written, the problem, data collection and results are clearly presented and the discussion is nicely addressed (but see minor comments below).
The only major problem I see is in the methods, and the rationale used to estimate or assess niche diversity. The authors use discrete climate classes as a proxy of niche breadth (lines 101-104) and take these as discrete niches (see following example in line 105) in the estimation of niche breadth (lines 168-171) and niche diversity (lines 158-163). Those are climate subclasses, not discrete niches. As the authors probably know, the niche of a species represents a collection of biotic and abiotic variables (and the ranges within them) in which the species is found in nature. It can be considered as an ecological space in which the species can survive. Therefore, there is no such as "fifteen discrete niches" (line 105) of a species. One could perhaps subdivide the niche of a species in groups representing traits to extract more information, for example, for alternative cytotypes within a species. But even in such cases the niche of the species is one. Moreover, climate classes are arbitrary classifications which do not reflect niche differences and cannot be used as a proxy to a species´ climatic niche. For example, even within a tropical wet forest there are different niches based on macro-ecology and the species under consideration. Instead, climate classes are habitat or ecosystem classification of a species. These implies that, even when conclusions are not wrong, the use of terms related to niche attributes is conceptually wrong or misleading (see e.g., the statement on niche divergence in lines 187-189, or the one about breeding systems and evolution of climatic niche diversity in lines 228-232) Minor comments As a minor comment, it is not completely clear why the authors consider the compatibility system when evaluating taxa propagating asexually (lines 107-110). Additionally, since breeding system in asexually propagating diploids is unknown, it makes sense to remove the (self-) compatibility system from the comparison to the asexually propagating polyploids. I would also be careful about making statements using breeding system (i.e., self-incompatible vs. self-compatible) as discrete classes. The truth is that there are greys in these classes and many species show intermediate levels of pollen-pistil compatibility or variation in the activity of SSI and GSI systems (e.g., unilateral vs. bilateral cross-incompatibility in Solanum species).
lines 166-167: a diploid species does not possess polyploids, the species have diploid and polyploid cytotypes, and populations cannot "show polyploidization". lines 184-187: this sound weird. How the "plants with increased development of wild areas can lead to changes in habitat and climate"? line 201: "diploidy" or "the self-incompatible diploid state has" lines 210-211: this is wrong. The breakdown of self-incompatibility is caused by an increase in ploidy, not the other way. At least this is what is known for plants. Many polyploids still conserve self-incompatibility systems. lines 220-227: this is highly speculative, and I found no need to write such statement in the current study. First, no measure of genetic diversity was estimated nor considered here. Second, Solanum species show a complex interaction of genomes during endosperm development (EBN) which render unfruitful many interspecific crosses. Even in the case the observed variability in species´ habitat occurrences presented here is associated to genetic diversity parameters, there is no possible way of concluding this can be transferred to cultivated Solanum varieties.
Reviewer: 2 Comments to the Author(s) The study addresses very relevant topic on how polyploidy and breeding system **interacts** in order to affect niche breadth of a genus. The question is certainly very interesting, however I am not sure how well-suited the presented model group is given (i) absolute correlation between ploidy and breeding system (polyploids exhibit only one breeding system, self-compatible asexual, which is not present in a diploid state) and lack of own data, specifically sampled to fill in particular gaps in the sampling (e.g. shortage of the plastome data, causing PGLS analysis relying only on 27 out of 72 focal species). A re-analysis using modern statistical methods may certainly also bring novel results, the question is, however, if the dataset is suitable for addressing this question. Please see the following remarks. 1) Unfortunately, it is totally unclear how the data were acquired, especially how the breeding system information and ploidy has been assigned. Do the authors simply fully rely on the previously published works cited in Methods? Even if so it would be worth explaining how the data have been acquired in the original works and potentially critically review their approach. Or did the authors curated the data anyhow, re-assigning the group or updating with potential novel data?. Specifically: -How the ploidy was assigned to a each species? What is the basic chromosome number for Solanum and which 2n= value is thus assigned to be a diploid and tetraploid? In how many cases more chromosome counts have been recorded per species and in what proportion of such cases intraspecific ploidy variation has been observed (e.g. diploid and tetraploid chromosome counts in one species)? How ploidy-variable species were then handled (excluded / assigned to both classess?)? Are there higher polyploids than tetraploids in the analysis? -How was self-compatibility assessed and does this trait also vary within some species (it can do, e.g. in Arabidopsis lyrata). If so, how such variable species have been handled? Is there anything known about the outcrossing levels of the SC species (i.e. real manifestation of the breeding system shift in natural populations)?
2) The absolute correlation of ploidy and breeding system (polyploids are always self-compatible asexuals, and this combination of breeding systems is not present in a diploid, l. 108-110) makes impossible to decouple the effect of ploidy and breeding system. This is the nature and it is worth studying, yet under the current natural setup it is impossible to distill the role of ploidy in niche evolution (contrary e.g. to the statements on l. 196). Re-focusing the main aim towards breeding system (taking ploidy into account as a potential side-effect), or the study and/or focusing on different model system may help to address this issue. In the former case, however, I am not sure about the novelty of the study as relatively a lot of work has been done on the relationships between breeding systems and distributions.

Minors:
What is "unknown breeding system asexually propagating diploid"? Is it asexual or unknown?
Even putting polyploidy apart, it is also unclear to which extent the expansion of the "self compatible asexual polyploid" category is due o selfing and asexuality. This shall be also taken into account in the Discussion (e.g 208-219) ===PREPARING YOUR MANUSCRIPT=== Your revised paper should include the changes requested by the referees and Editors of your manuscript. You should provide two versions of this manuscript and both versions must be provided in an editable format: one version identifying all the changes that have been made (for instance, in coloured highlight, in bold text, or tracked changes); a 'clean' version of the new manuscript that incorporates the changes made, but does not highlight them. This version will be used for typesetting if your manuscript is accepted.
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Author's Response to Decision Letter for (RSOS-211090.R0)
See Appendix A.
We hope you are keeping well at this difficult and unusual time. We continue to value your support of the journal in these challenging circumstances. If Royal Society Open Science can assist you at all, please don't hesitate to let us know at the email address below.

Dear Dr Kantar
On behalf of the Editors, we are pleased to inform you that your Manuscript RSOS-211862 "Interactions between breeding system and ploidy affect niche breadth in Solanum" has been accepted for publication in Royal Society Open Science subject to minor revision in accordance with the referees' reports. Please find the referees' comments along with any feedback from the Editors below my signature.
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Please submit your revised manuscript and required files (see below) no later than 7 days from today's (ie 03-Dec-2021) date. Note: the ScholarOne system will 'lock' if submission of the revision is attempted 7 or more days after the deadline. If you do not think you will be able to meet this deadline please contact the editorial office immediately.
Please note article processing charges apply to papers accepted for publication in Royal Society Open Science (https://royalsocietypublishing.org/rsos/charges). Charges will also apply to papers transferred to the journal from other Royal Society Publishing journals, as well as papers submitted as part of our collaboration with the Royal Society of Chemistry (https://royalsocietypublishing.org/rsos/chemistry). Fee waivers are available but must be requested when you submit your revision (https://royalsocietypublishing.org/rsos/waivers).
Thank you for submitting your manuscript to Royal Society Open Science and we look forward to receiving your revision. If you have any questions at all, please do not hesitate to get in touch. Dear authors, I went through the revised manuscript, and added a few extra notes as comments in the pdf. Overall, I understand that you categorize climate into distinct categories (classes) for analytical reasons, but these are still no real physical entities with clear boundaries. This still needs to be highlighted more clearly at the onset of the methods ( § data collection).
Ensure that figures are intelligible (also supplementary). This typically means increasing font sizes, increasing line widths, and adapt color schemes in R to something a bit more color-blind friendly, or at least with more contrast between adjacent colors. There were so many different hues of green, blue, reddish, pink in some supplemental figures that they became hard to understand (suppl figs 1 and 3 in particular). Also, please explain abbreviations in supplemental figures too.
Sincerely, Joachim Mergeay Associate editor ===PREPARING YOUR MANUSCRIPT=== Your revised paper should include the changes requested by the referees and Editors of your manuscript.
You should provide two versions of this manuscript and both versions must be provided in an editable format: one version should clearly identify all the changes that have been made (for instance, in coloured highlight, in bold text, or tracked changes); a 'clean' version of the new manuscript that incorporates the changes made, but does not highlight them. This version will be used for typesetting.
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If you have been asked to revise the written English in your submission as a condition of publication, you must do so, and you are expected to provide evidence that you have received language editing support. The journal would prefer that you use a professional language editing service and provide a certificate of editing, but a signed letter from a colleague who is a proficient user of English is acceptable. Note the journal has arranged a number of discounts for authors using professional language editing services (https://royalsociety.org/journals/authors/benefits/language-editing/).

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Author's Response to Decision Letter for (RSOS-211862.R0) We hope you are keeping well at this difficult and unusual time. We continue to value your support of the journal in these challenging circumstances. If Royal Society Open Science can assist you at all, please don't hesitate to let us know at the email address below.
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