Ephemeral signatures of phylosymbiosis in dermal microbiomes within the requiem shark family (Carcharhinidae)
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The elasmobranch dermal microbiome may be important for buffering effects of environmental stress on host health and population viability via functional metabolic interactions. Dermal microbiomes among elasmobranch orders co-vary with host phylogeny (phylosymbiosis), indicating functional co-evolution with their hosts at deep phylogenetic splits. However, the extent of phylosymbiosis and potential for functional co-evolution within particularly species-rich elasmobranch families is unknown. Here we re-analyse Illumina amplicon sequence data from the 16S rRNA gene from eight Carcharhinid shark species (plus one Ginglymostomatid outgroup) across six independent studies and explicitly examine the extent of phylosymbiosis in dermal microbiomes within this family. We found extensive divergence in OTU abundance and functional metabolic capacity between studies, driven by disparity in OTU sharing and probably reflecting geographical and seasonal factors. Total microbiome structure was incongruent with shark phylogeny, providing no evidence for phylosymbiosis when considering all species and OTUs. However, using bootstrapping and subsampling methods, we identified several subsets of OTUs where Bray-Curtis dissimilarity supported perfect topological congruence with shark phylogeny or strong associations with phylogenetic distances, but not both. Partial Mantel tests identified ten candidate OTUs that supported a moderately strong signal of phylosymbiosis across all shark species and included the immunostimulant skin symbiont genera Lactiplantibacillus and Alcaligenes. Overall, this provides provisional evidence for phylosymbiosis in a minority fraction of the elasmobranch dermal microbiome within the Carcharhinidae family and will necessitate coordinated large-scale studies to establish generality of these findings.
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Thank you for revising the manuscript. I am satisfied with the changes you made and I am pleased to tell you that your article has now been accepted for publication in Access Microbiology.
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The reviewers have highlighted minor concerns with the work presented. Please ensure that you address their comments.
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Comments to Author
This manuscript addresses whether phylosymbiosis can be detected in the dermal microbiomes of requiem sharks using publicly available 16S rRNA data. The study is carefully conducted, methodologically transparent, and conservatively interpreted. The main conclusion—that whole-microbiome phylosymbiosis is not supported within Carcharhinidae, with only weak and inconsistent signals in limited OTU subsets—is reasonable and supported by the analyses. Minor clarification would improve the manuscript. specifically, the authors should more clearly define what is meant by "ephemeral phylosymbiosis," maintain a cautious interpretation of candidate taxa, briefly address the implications of discordance between topology- and distance-based approaches, and reemphasise the dominant influence of environmental and …
Comments to Author
This manuscript addresses whether phylosymbiosis can be detected in the dermal microbiomes of requiem sharks using publicly available 16S rRNA data. The study is carefully conducted, methodologically transparent, and conservatively interpreted. The main conclusion—that whole-microbiome phylosymbiosis is not supported within Carcharhinidae, with only weak and inconsistent signals in limited OTU subsets—is reasonable and supported by the analyses. Minor clarification would improve the manuscript. specifically, the authors should more clearly define what is meant by "ephemeral phylosymbiosis," maintain a cautious interpretation of candidate taxa, briefly address the implications of discordance between topology- and distance-based approaches, and reemphasise the dominant influence of environmental and methodological heterogeneity. Overall, this is a solid contribution that would benefit from minor textual clarification only.
Please confirm that no generative AI tools or large language models have been used to generate this peer review report or to assist with any part of the peer review process.
I confirm no generative AI tools were used in preparation of this review.
Please rate the manuscript for methodological rigour
Very good
Please rate the quality of the presentation and structure of the manuscript
Very good
To what extent are the conclusions supported by the data?
Strongly support
Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?
No
Is there a potential financial or other conflict of interest between yourself and the author(s)?
No
If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?
Yes
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Comments to Author
The main concerns are variability and limited sample size, which should be acknowledged as the key limitations. The 17 samples from nine different species across six studies differ in primer regions and sampling settings. Even with Mantel conditioning applied, study effects can still overshadow the results. While analyzing the core samples is helpful, the authors should make clear that these findings are mainly exploratory and not a conclusive test of phylosymbiosis, unless supported by additional validation. In addition to these considerations, merging OTUs at the genus level is a significant step that warrants further justification and additional sensitivity checks. While I think I understand your reasoning, for example, due to variations in variable regions across studies, I believe consolidating …
Comments to Author
The main concerns are variability and limited sample size, which should be acknowledged as the key limitations. The 17 samples from nine different species across six studies differ in primer regions and sampling settings. Even with Mantel conditioning applied, study effects can still overshadow the results. While analyzing the core samples is helpful, the authors should make clear that these findings are mainly exploratory and not a conclusive test of phylosymbiosis, unless supported by additional validation. In addition to these considerations, merging OTUs at the genus level is a significant step that warrants further justification and additional sensitivity checks. While I think I understand your reasoning, for example, due to variations in variable regions across studies, I believe consolidating ASVs into genus categories across different primers can potentially obscure meaningful biological signals and introduce classification errors. Misassignments can lead to artificial similarities between samples or mask actual differences. At the very least, it would be wise to do a sensitivity analysis to verify if the primary conclusions remain valid at the family or order level. Additionally, the authors need to clarify what proportion of reads or features were labelled as "genus-unclassified" and how these were managed.
Please rate the manuscript for methodological rigour
Satisfactory
Please rate the quality of the presentation and structure of the manuscript
Good
To what extent are the conclusions supported by the data?
Partially support
Do you have any concerns of possible image manipulation, plagiarism or any other unethical practices?
No
Is there a potential financial or other conflict of interest between yourself and the author(s)?
No
If this manuscript involves human and/or animal work, have the subjects been treated in an ethical manner and the authors complied with the appropriate guidelines?
Yes
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