Of Necks, Trunks and Tails: Axial Skeletal Diversity among Vertebrates

Round 1

Reviewer 1 Report

Dear Dr Mallo,

I find your paper very interesting. I have only few minor suggestions to you.

1. Please add formal (latin) names when you mention any species, like the long tailed grass lizard (line 364, and others species - swann, giraffe etc.) - do you mean Takydromus sexlineatus?

2. Figures #1 and #2 are not mentioned in the text. 

3. In this paper you focus mostly on the Hox genes and somites. I think the paper could be improved if you discuss also the allometric patterns of vertebrae elongation and differentation. You shortly address this with classic Giraffe neck (increase of vertebrae size) and give only single sentence on the "differential growth of the skeletal elemens" (lines 142-144). I think it should be more detailed covered here. 

Also - the neck of the swann as the example of increase of vertebrae number. In the figure 1 legend you wrote that "in birds, neck size is directly related to the number of cervical vertebare, illustrated here with the cervical region of a swann (...)" - Right, however please notice, that that the neck vertebrae of swann are also elongated comapred to "short-necked" birds, thus it is possible that both process of neck elongation act simultanously. 

4. What about intraspecific variation in vertebrae size and number? This is common in lizards and snakes both as intersexual differences (i.e. male snakes usually have more caudal vertebrae, whereas females more trunk vertebrae) and within sexes. The interspecific variation in development is rather understudied and I think it is worth to discuss this here. Especially, it provides link between macrovelutionary patterns and microevolutionary process. 

Btw. What about turtles? Their vertebrae column is very peculiar (it forms part of the carapax). I understand that it may be to detailed to review here, however should be at least shortly mentioned. 

5. Please add the concluding paragraph. At this moment I feel the paper ends rapidly. 

6. Please italize the formal species names in the references. 

Author Response

Reviewer comment #1: Please add formal (latin) names when you mention any species. like the long tailed grass lizard - do you mean Takydromus sexlineatus?

Reply: I added the latin names in all relevant places and I indeed meant Takydromus sexlineatus when referring to the long tailed grass lizard.

Reviewer comment #2: Figures #1 and #2 are not mentioned in the text. 

Reply: Thank you for pointing this out, somehow I had missed it. Now they are mentioned in the text.

Reviewer comment #3: you discuss also the allometric patterns of vertebrae elongation and differentiation. And "the neck vertebrae of swann are also elongated compared to "short-necked" birds, thus it is possible that both process of neck elongation act simultaneously"

Reply: I have introduced a short discussion about this for both mammals (lines 123-128) and for birds (lines 211-215)

Reviewer comment #4: What about intraspecific variation in vertebrae size and number?

Reply: I have now introduced a small comment about this important issue (lines 321-324).

Reviewer comment #4-1: What about turtles? Their vertebrae column is very peculiar (it forms part of the carapax). I understand that it may be to detailed to review here, however should be at least shortly mentioned. 

Reply: I have now changed a bit the sentence describing the carapace to include the vertebrae (line 367, 368).

Reviewer comment #5: Please add the concluding paragraph.

Reply: Now I have included such paragraph as "concluding remarks".

Reviewer comment #6. Please italize the formal species names in the references. 

Reply: Done

Reviewer 2 Report

This is an important review presenting what is known about the developmental basis for the diversity in the vertebrate axial skeleton. To my knowledge no recent review on this topic exists and it is my expectation that the paper will be frequently cited. As a general comment I would have that the review is very focused on tetrapods and that some diversity as present in the fish skeleton is not covered. Anatomies that spring to mind are epicentrals (formerly “dorsal ribs”), occipital ribs, or the Weberian apparatus. I do not consider it to be required that these elements are discussed considering the already very extensive scope of the article, however it might be appropriate to include a brief note that some diversity in non-tetrapods is not covered. Then I do have just some minor comments.

Line 43: It is stated that the number of occipital somites in frogs has been reduced to 3. It has always been my understanding that there is evidence that the ancestral anamniote number of occipital somites is 3 which likely has been extended to 5 in amniotes. Evidence for this could come for the presence of 3 occipital somites in fish and amphibians. This is amongst others discussed in Woltering et al. BMC Dev Biol 2018 from which I copied the relevant references below. Maybe the author can double check this information and update the details included on occipital somites.

Morin-Kensicki EM, Melancon E, Eisen JS. Segmental relationship between somites and vertebral column in zebrafish. Development. 2002;129(16):3851–60.

Piekarski N, Olsson L. Muscular derivatives of the cranialmost somites revealed by long-term fate mapping in the Mexican axolotl (Ambystoma mexicanum). Evol Dev. 2007;9(6):566–78.

Piekarski N, Olsson L. Resegmentation in the Mexican axolotl, Ambystoma mexicanum. J Morphol. 2014;275(2):141–52.

Patterson C, Johnson GD. The Intermuscular bones and ligaments of teleosten fishes, vol. 559. Washington, D.C.: Smithsonian institution pres; 1995.

Line 272 – Sentence with missing word perhaps “ The possibilities for direct…”

Line 277 – Segment (not plural)

Line 382-389 – The section about the homocercal tail fin contains incorrect information. In fish three types of caudal fins are generally distinguished: heterocercal, homocercal and diphycercal. Only the diphycercal type of fin, as for instance present in lungfish, coelacanth or eels, is truly symmetric with lobes arising from dorsal and ventral sides of the axis. The heterocercal tail as found in sharks indeed is outwardly asymmetric containing only a strongly developed ventral lobe. However, the homocercal tail fin in teleost fishes is in fact a modified type heterocercal fin that is outwardly symmetric, but in the organization of the endoskeleton and embryonal origins of the fin precursors preserves all characters of the ancestral heterocercal type with a very strongly upturned spine that ends in the “urostyle”. A good description of teleost caudal fin morphology including references is present in Woltering et al. BMC Dev Biol 2018. A further good description of caudal fin types is present in:

Metscher B, Ahlberg P: Origin of the teleost tail: phylogenetic frameworks for developmental studies. In: Major events in early vertebrate evolution. Edited by P.E. A. London: CRC press; 2001. pp. 333–49.

Another good resource into caudal fins is:

Moriyama, Takeda, Evolution and development of the homocercal caudal fin in teleosts.Development, growth and differentiation, 2013

Please note that this latter article has been retracted because of plagiarism as I understand, so perhaps it is better not cited, it remains however valid as a literature resource.

Author Response

Reviewer comment :... it might be appropriate to include a brief note that some diversity in non-tetrapods is not covered"

Reply: I have now introduced a sentence to point this out in the concluding remarks (lines 496-499)

Reviewer comment: It is stated that the number of occipital somites in frogs has been reduced to 3.  It has always been my understanding that there is evidence that the ancestral anamniote number of occipital somites is 3 which likely has been extended to 5 in amniotes.

Reply: I actually did not mean that the ancestral condition was 5 occipital somites and that the 3 occipital somites in frogs resulted from a reduction during evolution but just state a different count of occipital somites in amniotes and anamniotes. I modified the sentence (lines 40, 41) to avoid confusion.

Reviewer comment: The section about the homocercal tail fin contains incorrect information.

Reply: I thank the reviewer for pointing this out. I have now modified the section to include the correct information (lines 396-405).