PONE-D-22-06171Predation history has no effect on lateralized behavior in Brachyrhaphis rhabdophoraPLOS ONE

Dear Dr. Callaway,

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Reviewer #1: No

Reviewer #2: Partly

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

Reviewer #1: No

Reviewer #2: Yes

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Reviewer #1: No

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: This paper set out to determine the impact of predation pressure on laterality in a poeciliid in Costa Rica. Unfortunately, with just 2 rivers examined (1 high and 1 low predation pressure) it can not examine the hypothesis as stated. The data about the response to the various stimuli may be useful but it is difficult to know how (if) they should be combined owing to the variation in populations from which they were drawn. The authors also make several statements attempting to enhance the apparent novelty of this study, but seem to ignore the literally 100s of papers that have addressed this topic previously. Data analysis is limited.

Specific comments.

L35-36: Rephrase this. There must be 100 papers on laterality in fishes. You also contradict this statement L152 as the opener to the Discussion.

L46: Odd that till now there is no mention of the work on Brachyrphaphis episcopi. A sister species where a number of papers have examined high and low predation effects on laterality.

L61: Im not so sure about these hypotheses. If predation drives the evolution and or development of laterality then shouldn’t the high predation population be highly lateralised irrespective of the stimuli. Otherwise you are suggesting domain specific laterality which would be rather unusual. Also these 2 hypotheses are clearly not independent of one another. What we are expecting is a population by stimuli interaction of some sort.

L64: I would delete the last line. This is the introduction not the results section.

L75: with just one population from each of high and low predation the authors can not generalise about the potential impact of predation pressure on laterality. There are presumably any number of environmental variables that differ between these two streams that could result in variation in laterality (or not).

L118: did a male have to make a certain number of choices to be included in the data set? Eg more than 10?

119: its important to describe the lighting above the tank and discrepancies in shadow can induce false positives.

L139: Im not sure why there was no attempt to use a 2 way-anova to examine laterality scores. Nor is there any mention of absolute laterality which tends to be a good predictor of the strength of laterality irrespective of direction.

Fig 1? My version doesn’t seem to have a map.

Fig 3. Why 2 SE ?

L161-167: This explanation does not make sense. Clearly populations within a species vary with respect to predation regime, so to suggest that a sister species ought to show the same pattern due to a common ancestor is irrational. Moreover, Bisazza and colleagues have conducted multiple comparisons across species and found that schooling tendency predicted laterality not phylogeny.

L168: also not true. There are multiple papers examining the costs and benefits of laterality in poeciliids as well as in vertebrates more generally, including multiple reviews.

L178: There is most certainly a publication bias. I have three students working on laterality in 5 species and is not reliably showing up in any of them.

Reviewer #2: Glad to read this paper that aimed at investigating behavioural lateralisation in a poeciliid fish depending on predation history. Although well written and organized my opinion is that there are some flawless in the current form of the paper. First of all it is not clear to me how many trials were recorded in order to compute the index of laterality for each subject during the 20min of observation, whether or not they have discarded subjects that does not spontaneously turn or if they tend make "proper turn" toward one or the other end of the apparatus. I was also wondering about the possibility to test for possible behavioural asymmetries using a viewing situation in which the subject is required to make closer inspection to the stimuli. Finally why do not include females?

In the discussion section (line 167) the authors claim that there are "too few tests of laterality....", not sure what they are arguing here but actually theres a quite large literature on how to assess lateralization in poeciliid fish.

In general the result section appear to be pretty much concise.

Minor comments:

reference 31: Giorgio V. should be Vallortigara G

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PONE-D-22-06171R1Predation history has no effect on lateralized behavior in Brachyrhaphis rhabdophoraPLOS ONE

Dear Dr. Callaway,

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.

The manuscript has improved a great deal. The reviewers suggest you check on a handfull of things and clarify certain points. Most important of those are the following.

1. Figure 3 shows that there is a very large variation in the data, and we must consider the causes of this variation. Follow rev 3 and explore this further with graphs and statistics.
2. Rev 1 is still uncomfortable with the one population from high and one from low predation environments (n = 1). These populations undoubtedly differ in any number of ways which may influence laterality. Adjust interpretation accordingly.
3. Several issues on methodology and statistics have to be clarified. including
    
   1. how long males recovered before being tested again?
   2. Are there variation by pop and treatment – analyze with a mixed model with individual ID as the random variable, pop and treatment as independent variables and LI as the dependent?
   3. How was the variation around means? Where any of the individuals lateralised in their response to various cues? Eg. Where strongly lateralised fish consistently strongly lateralised?
4. Provide the raw data as csv file, with better annotation of columns and summaries.

Please submit your revised manuscript by Oct 22 2022 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.

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Academic Editor

PLOS ONE

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Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments (if provided):

The manuscript has improved a great deal. The reviewers suggest you check on a handfull of things and clarify certain points. Most important of those are the following.

1. Figure 3 shows that there is a very large variation in the data, and we must consider the causes of this variation. Follow rev 3 and explore this further with graphs and statistics.

2. Rev 1 is still uncomfortable with the one population from high and one from low predation environments (n = 1). These populations undoubtedly differ in any number of ways which may influence laterality. Adjust interpretation accordingly.

3. Several issues on methodology and statistics have to be clarified. including

a. how long males recovered before being tested again?

b. Are there variation by pop and treatment – analyze with a mixed model with individual ID as the random variable, pop and treatment as independent variables and LI as the dependent?

c. How was the variation around means? Where any of the individuals lateralised in their response to various cues? Eg. Where strongly lateralised fish consistently strongly lateralised?

4. Provide the raw data as csv file, with better annotation of columns and summaries.

[Note: HTML markup is below. Please do not edit.]

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Comments to the Author

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Reviewer #1: (No Response)

Reviewer #3: All comments have been addressed

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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: Partly

Reviewer #3: Partly

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

Reviewer #1: No

Reviewer #3: Yes

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Reviewer #1: Yes

Reviewer #3: Yes

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Reviewer #3: 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: PONE-D-22-06171R1

Predation history has no effect on lateralized behavior in Brachyrhaphis rhabdophora

Callaway

This paper has certainly improved and I thank the authors for taking on and addressing previous concerns. I confess, even given previous work on this system, I’m still uncomfortable with n = 1.

Having done many of these projects myself, I recognize how much work goes into it, and I want to be sure the authors have really explored their data as best they can. With this in mind I’ve offered some alternative analyses that they might consider.

The methods still require a bit more detail so folks could replicate them.

Specific comments:

L65 I still don’t feel comfortable with the one population from high and one from low predation environments. These populations undoubtedly differ in any number of ways which may influence laterality. However, given the historical context (Johnson and Belk 2001) it is reasonably likely that the variation may due to predation. I would be far happier to see multiple pops tested.

L126: Its also not clear how long males recovered before being tested again. (inter-trial period). Also state here that you did not set a min number of turns for the males to qualify and perhaps make a statement about how many runs the fish did make.

L144: Im still a bit confused by the statistics. I can appreciate that the current method tells us if the estimates of LI overlap with 0, but I still think its worth-while exploring if they differ with pop and treatment as this speaks directly to your hypotheses. In this case, would it not be better to include a mixed model with individual ID as the random variable, pop and treatment as independent variables and LI as the dependent?

L157: I would be interested to know if any of the individuals were lateralised in their response to various cues. What does the distribution look like? Where strongly lateralised fish consistently strongly lateralised? Previous papers, for instance, have examined the proportion of the population tested that scored at 70% L or R (lateralised). I just get the feeling you could do more with this data and individual details get lost in population averages.

L203: of course there are other explanations, including low sample sizes or inappropriate experimental design, which are less interesting but nonetheless significant concerns.

Reviewer #3: The paper “Predation history has no effect on lateralized behavior in Brachyrhaphis

rhabdophora”

The paper of Callaway and coll. investigate the effect of predation history on eye preference in the livebearing fish Brachyrhaphis rhabdophora by detour test. The authors reported no evidence for behavioral lateralization at all in response to any stimuli (predator, mate, novel, control), regardless of predation population or predation-free population.

This paper is written clearly and the unique behavioral experiment has been conducted. Appropriate corrections have already been noted by the reviewers. I feel that this manuscript provides a novel contribution to the field. Interesting concept and idea but there is a lot of variation in the behavioral data and no explanation for this. Also, I point out that there are problems with the experimental design.

Please make a couple of improvements as follows:

Introduction

P4, line48-53: It is necessary to explain in detail how much mortality in the fish differs between environments with and without predators.

Methods

P7, line127-129: Insufficient information about the experimental procedure: in what order were the four stimuli presented? Were the stimuli random order? The interval of the experiment was short (10 minutes), and it is suspected that the subjects may become accustomed to the experimental test and feel tired.

Result

Figure 3 shows that there is a very large variation in the data, and we must consider the causes of this variation. This is because this result is directly related to the conclusion that there is no laterality in the livebearing fish. One possibility is that a detour test of 20 minutes may be too long for observation. Even at the beginning and end of the experiment, the laterality tendency eye may change (Cantalupo et al. Neuropsychologia 1995, Sovrano et al. Physiology and Behavior 2001, Bisazza et al. Behavioural Brain Research 2002). If LI is calculated for only the first 5 or 10 minutes, will the results change? Longer experiment time introduces the effect of habituation and learning, which makes the interpretation of results more difficult.

The number of trials per individual is not specified in the results. It is unfortunate that this has not been corrected in the text, even though this was pointed out by reviewer 2.

Discussion

P9, line167-171: It is necessary to specify what type of left-right behavior is exhibited by the three closely related species of this species. Whether there is a unifying trend or not would allow us to consider the need to question the phylogenetic background.

P10, line181-183: "non-lateralized individuals tend to choose higher-quality shoals than lateralized individuals"

What is meant by “higher-quality shoals” and how is it costly needs to be explained.

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Reviewer #1: Yes: Prof. Culum Brown

Reviewer #3: No

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Predation history has no effect on lateralized behavior in Brachyrhaphis rhabdophora

PONE-D-22-06171R2

Dear Dr. Callaway,

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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