PONE-D-20-09231

Geolocator tagging links distributions in the non-breeding season to population genetic structure in a sentinel North Pacific seabird

PLOS ONE

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Additional Editor Comments (if provided):

Please pay close attention to and address concerns raised by both reviewers. Both make legit points. Major concerns that need to be addressed are:

1) General issues regarding IBD, e.g. whether appropriate or not across the entire range, and needing to be introduced and conceptually developed within the Introduction.

2) Correlation vs. causation.

3) Clarity regarding breeding vs. non-breeding/winter areas, timing of such, etc... e.g. as identified by Reviewer 2. To the extent that genetic structure is a consequence of gene flow, which of course is tied directly to mating, there needs to be better description of these colonies and where/when breeding takes place versus where/when they are relative to this when not breeding. Like Reviewer 2, I was confused. The reader is provided insufficient information to understand the situation.

In addition to the other issues the two reviewers identified, below is a list of minor problems I found.

Throughout, replace the apostrophe in F'ST with a straight apostrophe (e.g. using insert symbol in Word).

Figure 2a & 2b. Double check the ordering/naming of the colonies. To the extent, n is larger for MAT than TEU, these two, at least, apparently switched order between a & b. I also wondered about DE & PR. Be 100% sure that all names are associated with the correct genetic info in the STRUCTURE diagram.

Also, Figure 2a & 2b. Both should look identical structurally given they are essentially part of the same figure: 2a currently has more space and an additional solid black line on the left. The region names and brackets also need to better match the associated breeding colonies. Currently, TOD looks to be part of Alaska, especially in 2b. The brackets and region names in general appear to be less carefully aligned/applied in 2b versus 2a. There's also no reason the bracket for Japan should extend well beyond the colony info. Making things exact is easy using PowerPoint by inserting figures, then adding text/brackets and aligning using grid lines. Seems to me 2a and b could have easily been pre-assembled into a single jpeg.

Seems to me given their geographic location and their genetic similarity, SGG and TRI should be ordered together in all STRUCTURE figures/diagrams.

In general, bracket lines on all STRUCTURE figures should line up with the vertical bracket lines in the STRUCTURE diagram.

Figure 4. Relevance of colors and legend. Change label for Protection to PR.

Figure 6. Correlation coefficients are generally designated using 'r' not 'p'. Until I read the text, I thought the figure included p-values of non significance. For clarity, replace 'p' with 'r'.

Line 393 and 394. Replace Table 4 with Table 3.

Line 419. Replace 'Moore, Cleland' with 'Moore and Cleland'

Line 420. Identify which cluster

Line 436-440. Given that you're dealing with Q>60% throughout, use it once only... or at most twice. E.g. The eastern Pacific colonies split into two clusters at Q>60%. Cluster one included... etc. Cluster two included... In cluster one, delete 'Protection'. In both cases, precede the last colony in the list by 'and'. Why were SEF and MID singled out given all member of cluster 1 and cluster 2 were associated with the respective clusters at Q>60%?

Line 447. Delete Protection. The text says 60%. Which is it 50 or 60%?

Line 448. Delete 'and' before Protection. Replace '&' with 'and' before Ano Nuevo. The text says 60%. Which is it 50 or 60%?

Line 520. Figure 6b says -0.21. Which is it?

Lines 641-643. Given the amount of spread, i.e. low correlation, and fact the correlation was only significant at 0.05, I think this is a bit overstated.

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Reviewers' comments:

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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

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Reviewer #1: This paper contributes to our understanding of the factors promoting population differentiation in seabirds and other species. I really enjoyed reading this paper. It's written very well and and it is clear and easy to follow. The science is sound and the methods are appropriate to test the hypotheses presented in the introduction. The conclusions are supported by the data and are well presented and discussed in a comparative framework as well. I have only very minor edits to suggest.

371-372: negative FST values are an artifact of some programs and should be replaced by zeros.

389-390: A significant Mantel’s test indicates correlation between genetic and physical distance but this doesn’t translate necessarily into isolation by distance. The fact that you get a significant Mantel’s test when you include populations from both sides of the Pacific but not when you analyze eastern Pacific colonies alone (lines 516-518) indicate that in the former the pattern is driven by strong pop structure between eastern and western Pacific colonies rather than by IBD. See Meirmans, P.G. 2012. The trouble with isolation by distance. Molecular Ecology 21: 2839-2846.

516-518: I would say that all results from Mantel’s should be presented together but testing for IBD between eastern and western Pacific colonies may be inappropriate (see above).

547-548: See comments above. This is structure between two differentiated groups rather than IBD.

Line 682: Analysis of highly differentiated loci in thick-billed murres (Tigano et al. 2017) has revealed a similar pattern, although not quantitively. The three Atlantic colonies that were more genetically similar at these outlier loci were also the colonies showing the highest overlap in wintering distributions. However, this pattern could have also been explained by colonization history following the retreat of the Pleistocene ice sheets or selection during the non-breeding time.

Figure 1. Please show all colonies included in the study and highlight those that have also GLS data

Figure 2-4 Structure plot image quality is low and pop labels are hard to read. Make sure that images are high quality.

Fig. 4 What do colors represent? Add legend.

Fig. 6 Add p-values on graphs and/or figure caption.

Reviewer #2: This paper makes an important contribution to our understanding of population structure, distribution, and space use of the Rhinoceros Auklet. The study is particularly valuable because it aggregates data from breeding colonies across nearly the entire distribution of the species, which will be critical baseline information for management and conservation of the species. The data are robust and well analyzed. Overall this is a well researched and well written paper!

My only real issue with the paper is that the abstract, intro, and discussion use language that makes it appear the authors found a causal relationship when they only tested a correlation. The study is framed as a test of the hypothesis that segregation in the wintering distributions drives genetic differentiation among breeding colonies. However, the paper does not test a causal mechanisms by which nonbreeding segregation would drive genetic differentiation, and as a paper the authors cite (Rayner et al 2011) points out, “Spatial segregation during the non-breeding season appears to provide an intrinsic barrier to gene flow among seabird populations that otherwise occupy nearby or overlapping regions during breeding, but how this is achieved remains unclear.” What the study does do is test if there is a correlation between genetic differentiation and degree of difference in space use during the nonbreeding season. I think the language can easily be revised to clarify that this distinction by removing words like “promotes” and “drives” that imply causation and replacing them with words like “correlates with” that make it clear what the authors are testing.

The authors only set up one hypothesis test in the intro (winter segregation is correlated with genetic structure), but they test an additional hypothesis in the paper (distance between breeding colonies is correlated with genetic structure). I assume the authors test this to evaluate if average dispersal difference accounts for genetic structure, assuming all populations have equal mean dispersal differences (which is not a given). Since the authors present results of both tests and use them to say that overwintering overlap better accounts for genetic difference than mean isolating distance, both hypothesis tests should be set up in the intro. The authors also discuss two additional hypotheses in the discussion: genetic structure correlates with egg lay date or morphological differences like body size or mass (potentially indicating differences in foraging niche). These are also testable hypotheses, and it appears the authors have the data to test them instead of just discussing them. I think this could potentially strengthen the paper, though it’s not essential.

A limitation of the study is that the authors did not consider temporal segregation, only spatial segregation. Because of that, it is unclear to what degree these breeding colonies are potentially in contact during the nonbreeding season. The geolocator study cited from Japan (Takahashi et al. 2015) did find that space use varied with month, so I’m curious why the authors did not consider or account for that. I think the authors should address this in the discussion at a minimum.

Authors use inconsistent terminology for geolocators. I found the following terms used in the ms: geolocator, geologger, logger, and GLS device. Bird carrying geolocators were also referred to as loggered and geologgered. Best to pick one and use it consistently to avoid confusion.

325: When do the colonies initiate and end breeding? How does that relate to the “winter” dates selected?

365, comma missing

631-633: I found this sentence confusing. I recommend “in which the population showed the unusual behavior of remaining in close proximity to a breeding colony year-round and foraging…”

640-643: change word from “promotes” as you don’t have evidence of a mechanistic relationship.

658: not “driven,” correlated with. Again, no causation has been shown.

669-670: These are alternative hypotheses that are testable.

Table 4: I think there’s an error in Middleton, which shows more track files recovered than geolocators recovered.

Fig 1: As this is the only full study area map, the Western Pacific sites should be included and differentiated with a different color or icon.

Fig 4: Unclear what the colors represent. Please include a color legend. It would be logical for colors to be grouped by the five regions identified in figures 2 and 3, but there are more than five colors presented here. Please clarify.

Figure 5: The resolution of the file attached for figure 5 is low, so it’s hard to figure out what the gray lines are. The caption says they represent the geolocator tracks, but the look like dashed, horizontal lines, whereas geolocator tracks are typically presented as a single connected line. The gray lines here look more like shading, but it’s unclear how that shading was generated. Does this incorporate some metric of uncertainty around each point in the track or aggregate all tracks in some way? Please clarify.

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Reviewer #1: Yes: Anna Tigano

Reviewer #2: No

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Geolocator tagging links distributions in the non-breeding season to population genetic structure in a sentinel North Pacific seabird

PONE-D-20-09231R1

Dear Dr. Hipfner,

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PLOS ONE

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Reviewers' comments: