PONE-D-24-30961Cryptic coral community composition across environmental gradientsPLOS ONE

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Reviewers' comments:

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Comments to the Author

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Reviewer #1: Yes

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: General comments

Evaluating how population and community structure is influenced by environmental conditions is key to understanding the influence of environmental change on ecosystems and implementing effective restoration/conservation efforts. This study explores the genetic structure of coral communities around St. Croix and how that genetic structure relates to a spatiotemporal variation in environmental conditions. The authors find variable genetic structuring across coral taxa with certain environmental conditions of key influence on coral community structure over space and time.

Generally, I found this manuscript to be well-written, well-structured and easy to read. Moreover, the quantitative design appears to be well constructed and performed. However, I feel that the manuscript would benefit from greater detail on portions of the analysis and environmental data structure (expanded on below). My technical understanding of these genetic methods is limited and thus I cannot provide meaningful technical review of this section.

Although the study is designed to be a more exploratory assessment, an important consideration here is the lack of specific hypotheses that are set out to be tested. While this isn’t necessarily a make-or-break issue, it is important for how the study is framed. The authors suggest that the broader implication of this work is around conservation and restoration actions—understanding where corals perform well and poorly can inform where corals are out planted. However, I find the interpretation of results provided here to be a bit of a stretch in a restoration context. Simply put, it is difficult to assess whether corals perform better or worse in a particular area without causal-type experimentation and hypothesis testing, indeed the authors indicate that such examination is a logical next step. This association-type analysis evaluates how spatial variation in genetic structure of corals is associated with long-term trends in environmental conditions, but it doesn’t say how these variables actually affect corals or their genetic structure. Given that consideration, reframing portions of the introduction and discussion to be focused on how environmental conditions can contribute to genetic heterogeneity might be a better framing than trying to make the leap regarding restoration efficacy.

Specific comments

Introduction

L53-55: “ecologically cohesive communities”. What is an ecologically cohesive community? Does this imply some type of facilitation by heterospecifics? This is not defined here or in the referenced literature. The potential facilitation effect may not be entirely relevant to this study.

L60: The authors note species and genera. Better to note these as coral “taxa” not species.

L64: The referenced literature, Grupstra et al. (2024 in NEE), reviews the potential drivers of genetic divergence among cryptic corals. I wouldn’t necessarily call this divergence for unknown reasons as the authors purport in this line. Rather it appears that there are many supported hypotheses for why provided by Grupstra et al. and by the authors in the following sentence. This context is a critical component of this study given that the authors do not generate specific hypotheses regarding why certain environmental attributes influence genetic structure. Perhaps a more useful approach would be to evaluate the hypotheses, pre or post-hoc, generated by Grupstra et al. within the study system, species.

L77-79: I appreciate the broadening of this topic to relevant examples in temperate ecosystems. However, I would suggest focusing this section on the abiotic factors that influence marine communities exclusively. Perhaps the broader strokes would be more useful earlier in the introduction.

L89-91: “highlighting the intricate relationship between genetic variation and environmental challenges in coral ecosystems.” Can the authors be more specific regarding environmental challenges? Are they referring to climate change?

L93-104: This paragraph seems like it should be in the methods section. The authors note potential mechanistic drivers of these patterns in the previous paragraph. Perhaps this space could be used to introduce specific hypotheses that the authors are testing?

Methods

L153-155: This passage would benefit from additional detail regarding sampling design. What was the size distribution per species of colonies sampled? Are these similarly sized colonies? What is the sample size per species per site?

L222-223: Can the authors expand on the structure and processing of environmental data? Mainly, what was the temporal resolution of environmental data used and subsequently summarized? Perhaps this information can be added to Supplementary Table 1. Moreover, interpretation of the environmental heterogeneity across sites and years would benefit from an additional supplementary figure illustrating spatiotemporal variation in each environmental variable.

L227: Kriging interpolation appears to be an appropriate way to interpolate environmental conditions for the location of colonies sampled. However, evaluating interpolation performance is contingent on the location of monitoring sites relative to colony locations. Where were the environmental monitoring sites? How far apart were they? Can the authors provide a supplementary figure of the variograms generated from kriging interpolation?

L235-236: The authors note that the “optimal number of genetic linkages was visually determined” (L206). Was a similar method performed for the environmental data (i.e., ecoregions and environmental data)? For ecoregions, what was the visual criteria for ecoregion grouping? Was there consideration of the height of each site similarity?

L260: It appears that two gradient forest models were employed here: one that assessed the influence of the 40 environmental predictors and another that assessed the effect of depth and the four ecoregions. Is this interpretation correct? This section would benefit for an explicit statement regarding the model structure[s].

Results

Table 1: What were the sample sizes per species per location? Are the sample sizes adequate to characterize genetic variation within and between locations? Additionally, in Fig. 4, there is some indication that genetic diversity appears to increase with sample size (panel b., M. cavernosa) although these patterns may not be as evident for the other 5 taxa. It is possible that the diversity of genetic linkages revealed may be an artifact of sampling design, although it is challenging to assess this without explicit reporting of sampling size per site per species. Do sample sizes reflect the relative abundance of each taxa at each site?

L338: The authors refer to Fig. 1d here. Should this be Fig. 2c? Its difficult to tell.

L334: The amount of variation in coral community structure explained by environmental conditions in the two separate models appears to be relatively small (12.5 and 18.9%), with cross validation values quite low for environmental predictors? Could this be a result of overfit models (i.e., too many environmental predictors)? Can the authors provide detail as to whether hierarchal cluster models and subsequently gradient forest models were assessed with fewer environmental variables? A more parsimonious environmental cluster model could contribute to increased gradient forest model performance. It might be beneficial to provide an explanation of why the variance explained was relatively low (e.g., low sample size).

L346: The authors refer to depth being the strongest predictor of community composition. However, Fig. 5a shows Ecoregion to be the most important, followed by depth. Do they mean Fig. 5b?

Figure 4: Add figure legend for bubble size corresponding to sample size.

Figure 5: Remove titles from panels A and B and provide x-axis labels.

Discussion

L376: The authors note that community composition is partially shaped by environmental conditions, mainly ecoregions and depth. Indeed, there is a high degree of variation in coral community structure that isn’t explained by models. While the authors expand on other potential drivers of these dynamics (e.g., cyclones temperature anomalies etc.), it is important to note that the temporal resolution of environmental conditions is not matched to the instantaneous measure of genetic structure. In other words, the authors assess how the environmental legacy of sites over ~12 years contributes to “current” community genetic structure. This approach makes many assumptions about what the coral community ‘looked like’ over this 12-year period. An acknowledgement and brief discussion of this assumption is probably needed here.

Reviewer #2: This is a nice study and a well-written paper. Strengths are that the distribution of cryptic coral lineages were studied in many (six) sympatric species from many (12) sites. One potential weakness might be that the number of individuals sampled per species was perhaps a bit low in some species (n = 21, 25 spread across 8 sites) so potential that some composition-environment patterns might not be fully characterized (but this is hard to know).

The manuscript is presented well, and it was easy to read. The data analyses all seem robust to me. I think the result will be useful to those working at St. Croix as well as to the bolster the evidence that cryptic species of corals are becoming the rule rather than the exception.

The overall result is consistent with previous studies that many morphologically-defined species contain evolutionarily distinct genetic lineages, that these lineages commonly co-occur but differ in relative abundance across depths and locations that differ in environmental variables. This study finds a correlation with yearly pH variation.

My only main comments are:

1) Because the association between community composition and environmental variables is still a correlation (and this is acknowledged e.g., 459), the discussion could perhaps be strengthened by considering alternative explanations for the current composition-distribution pattern that can be made without invoking environmental variables, like dispersal patterns / limitation or that they are just a signature of past disturbance history.

2) Genetic lineages within species were identified by visual examination only (of the hierarchical clustering tree and PCoA). The clustering analyses included samples from prior studies, which increases the confidence in the visual determination of lineages. However, the evidence for how the current samples cluster with previous samples is hard to find. It might be good to show which tips in Figure 3 are the “reference” samples from previous studies, and make a better connection to the nomenclature of each lineage (if a consistent one even exists for these species?), so readers can trace what lineages are showing up where.

Minor:

Line 224: Could you mention here what the frequency of recording are, and what the mean, maximum, etc refer to (mean per day, per month? How many measurements comprised each mean?). This is just to get a better idea of how well the environmental variables are characterized.

Line 227: Again, could you mention the spatial resolution of the sampling (how many sites?). Just trying to understand the robustness of the spatial interpolations. If a site where coral is sampled is far from the nearest site where environmental variables were measured, how good are the environmental estimates?

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Reviewer #1: No

Reviewer #2: No

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PONE-D-24-30961R1Cryptic coral community composition across environmental gradientsPLOS ONE

Dear Dr. Black,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Jan 19 2025 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

• A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
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• An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

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We look forward to receiving your revised manuscript.

Kind regards,

Vitor Hugo Rodrigues Paiva, Ph.D.

Academic Editor

PLOS ONE

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Reviewers' comments:

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Comments to the Author

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Reviewer #1: (No Response)

Reviewer #2: (No Response)

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Evaluating how population and community structure is influenced by environmental conditions is key to understanding the influence of environmental change on ecosystems and implementing effective restoration/conservation efforts. This study explores the genetic structure of coral communities around St. Croix and how that genetic structure relates to a spatiotemporal variation in environmental conditions. The authors find variable genetic structuring across coral taxa with certain environmental conditions of key influence on coral community structure over space and time.

This is my second review of this manuscript. The authors have made useful modifications and additions to all sections of the manuscript that assist in bolstering their approach. The revised version of this manuscript is much improved. Although the hypothesis outlined in the introduction is relatively broad, I feel that the updated context of the approach assists in the interpretation of the results. I have a few lingering comments that should be addressed and may benefit the manuscript further.

L89-100: In the previous version of the manuscript I noted that this paragraph would be best if placed in the methods section. Although the revised introduction adequately addresses my other comments I still feel that a description if the specific gradient forest methods here is out of place. Although these methods are certainly key to the analytical structure of the assessment, noting them in the introduction feels abrupt, especially after the paragraph noting the hypothesis examined but before the description of study area. Given that the gradient forest methods aren’t the key focus of this study, rather environmental drivers of cryptic coral composition, the introduction would benefit from a reduced focus on the particular methods.

Supplementary Figures: These appear to be out of order in the main text. Although this will probably be addressed in copy-editing, it may be best to rearrange them at this stage.

Semivariograms and kriging approach:

I appreciate the authors providing these supplementary figures—they greatly enhance the interpretation of the spatial interpolation of environmental conditions. Although, it is unclear what the numbers next to each point represent. Also, shouldn’t the points be pairwise comparisons of environmental stations? If so, shouldn’t there be many more points for each plot which may improve model fit.

As the authors note, the fit of these models is quite variable: some perform better than others. Based on even the good fits, I am somewhat concerned about the spatial scale of interpolation. For example, the fit for DO_max isn’t very good over the distance of ~0.03 (what are the units here?). For other variables (e.g., monthly range in Nitrogen), the fit line doesn’t appear to fit the [negative] trend at all. Given these fits, I am concerned that the environmental patterns over space may not be adequately represented by the models described. In general, some of the fits appear to either (1) obscure the spatial variability inherent to some variables or (2) don't appropriately capture trends.

Reviewer #2: 1) Overall I thought the revised text was fairly superficial, but it more or less addresses the point. For example, the phrase “stepped clines driving tension zone formation and assortative mating” is quite jargony and “other factors, such as ocean currents influencing larval dispersal” is quite vague. The statement that “the ability of currents to sustain high dispersal and connectivity” (L462) seems at odds with all the research showing that larvae (including corals) disperse much less than expected from ocean currents. For example: Prata et al 2024 Some reef-building corals only disperse metres per generation. Proc. R. Soc. B 291: 20231988. https://doi.org/10.1098/rspb.2023.1988

2) Thanks for the info. I noted that no changes were made to the manuscript here. The point of my comment was just to make some edits that could help the reader (not just the reviewer). I think at least a statement in the manuscript that summarizes these connections would help the reader.

“Generally, environmental variables were monitored across all coastlines of St. Croix, and very close to coral sampling sites. The only exception is that E. coli was not monitored near Cane Bay on the north shore.” So this would be good to mention this is the manuscript.

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Reviewer #1: No

Reviewer #2: No

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Cryptic coral community composition across environmental gradients

PONE-D-24-30961R2

Dear Dr. Black,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Vitor Hugo Rodrigues Paiva, Ph.D.

Academic Editor

PLOS ONE

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