Sensory Reconstruction of the Fossil Lorisid Mioeuoticus: Systematic and Evolutionary Implications

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

The manuscript “Sensory Reconstruction of the Fossil Lorisid Mioeuoticus: Systematic and Evolutionary Implications” is devoted to a detailed craniometric analysis of a series of CT scans of one lorisid specimen made by a different group of researchers. This was supplemented by detailed comparison with their already scanned and published crania of related species. Overall, this manuscript looks highly professional, satisfactorily structured, and written in perfect English. I was able to detect only a few number of minor bugs, and, therefore, acceptance for publication in “Animals” is stronly recommended.

1.      “The main aim of this project is to deduce the sensory capacities” – deduction of any kind cannot be the main aim of any serious project, it should have broader implications for science or certain perspectives for practical use or education.

2.      “shares a turbinal morphology with lemuroids, which likely denotes the primitive status of Mioeuoticus within Lorisidae. Thus, this taxon may be a stem member” – this is a typical way of hypothesizing and frequently leads to errors since the evolutionary changes in the long run may be not necessarily single but repeated. Therefore, authors should state that this explanation is just the most parsimonious one. Also, olfaction is usually rapidly evolving and the olfactory receptor genes’ diversity is a matter of remarkable jumps due to both natural selection and genetic drift. In extant species it is possible to analyze underlying genetics and compare different adaptations, so it would be nice to discuss the possibility that any apparent insufficiency for keen smell may be compensated at cellular or molecular levels

3.      “disturbs microscopic hairs that convert” – this is a simplified description, in fact hair cells have their own frequencies.

4.      “size of the semicircular canals give strong evidence of the visual acuity,” – relationship between vision and semicircular canals is not clear.

5.      Authors are not sure  – “or a cathemeral lifestyle” – perhaps a reference is needed to an article where a clear difference between closely related species – one nocturnal and another cathemeral – should be included so that there would be a better understanding of the matter. Indeed, Fig. 11 does not show a clear difference even for diurnal Strepsirrhini. Perhaps, it should be stated explicitly that that even nocturnal animals may be called cathemeral until careful behaviorial studies (impossible for extinct ones). Please clarify for unprofessional audience in Conclusion and perhaps in Abstract.

6.      “the absence of ET/et-IV, 564 which are present in” please make this sentence clearer, it may be ambiguous when reading fast…

7.      “[7] previously measured the curvature radii in this specimen” in a sentence constructed like this it would be nice write “Someone et al [7]”

8.      Order of figure numbers mentioned in the text is haphazard (5B after 1)

9.      Fig. 9.2 is mentioned but lacking

10.   Figure 11 – A and B missing

 

 

Author Response

1. “The main aim of this project is to deduce the sensory capacities” – deduction of any kind cannot be the main aim of any serious project, it should have broader implications for science or certain perspectives for practical use or education.

The term ‘deduce’ has been replaced with ‘reconstruct’.

2. “shares a turbinal morphology with lemuroids, which likely denotes the primitive status of Mioeuoticus within Lorisidae. Thus, this taxon may be a stem member” – this is a typical way of hypothesizing and frequently leads to errors since the evolutionary changes in the long run may be not necessarily single but repeated. Therefore, authors should state that this explanation is just the most parsimonious one. Also, olfaction is usually rapidly evolving and the olfactory receptor genes’ diversity is a matter of remarkable jumps due to both natural selection and genetic drift. In extant species it is possible to analyze underlying genetics and compare different adaptations, so it would be nice to discuss the possibility that any apparent insufficiency for keen smell may be compensated at cellular or molecular levels

We have deleted the sentence, ‘Thus, this taxon may be a stem member’. Our position is better explained in the following sentence: ‘Our data are consistent with Mioeuoticus being a member of the family Lorisidae, as it shares morphological features in the olfactory system, orbital structure, and inner ear anatomy with modern representatives’. We do not consider Mioeuoticus as a stem member because of the organisation of the turbinals, we state only that this animal’s characteristics are consistent with this idea.

3. “disturbs microscopic hairs that convert” – this is a simplified description, in fact hair cells have their own frequencies.

This sentence has been rephrased and restructured, and now reads as ‘As sound waves enter the inner ear, the fluid in the utricle, sacculus, and cochlear receptor organs vibrate. The hairs in the cochlea have different lengths and vibrate at numerous sound frequencies. Stimulating these microscopic hairs generate electrical impulses and sends them to the brain for interpretation and behavioural response [7,50]’.

4. “size of the semicircular canals give strong evidence of the visual acuity,” – relationship between vision and semicircular canals is not clear.

The term ‘visual acuity’ has been deleted and the sentence now reads, ‘The orientation, relative position, and size of the semicircular canals give strong evidence of the locomotor behaviour, and shape concerning phylogenetic affinities of fossil primates [51-57]’.         

5. Authors are not sure  – “or a cathemeral lifestyle” – perhaps a reference is needed to an article where a clear difference between closely related species – one nocturnal and another cathemeral – should be included so that there would be a better understanding of the matter. Indeed, Fig. 11 does not show a clear difference even for diurnal Strepsirrhini. Perhaps, it should be stated explicitly that that even nocturnal animals may be called cathemeral until careful behaviorial studies (impossible for extinct ones). Please clarify for unprofessional audience in Conclusion and perhaps in Abstract.

We have added a sentence to the text of the conclusion for clarification, which reads: ‘Because the entire radiation of modern lorisids, as well as its sister group (Galagidae), are nocturnal, the most parsimonious explanation for the activity pattern of M. shipmani is that this animal belonged to an entirely nocturnal radiation of lorisoids’.

6. “the absence of ET/et-IV, 564 which are present in” please make this sentence clearer, it may be ambiguous when reading fast…

This sentence has been rephrased for clarity, and now reads ‘The most disparate characteristic in Mioeuoticus would be the absence of ET/et-IV, a feature which is present in…..’

7. “[7] previously measured the curvature radii in this specimen” in a sentence constructed like this it would be nice write “Someone et al [7]”

This sentence has been rephrased to include the author's name as recommended, and now reads ‘Walker et al. [7] previously measured the curvature radii in this specimen’.

8. Order of figure numbers mentioned in the text is haphazard (5B after 1)

The figure numbers of the figures used directly within this paper are cited and referenced in the correct numerical order from Figure 1 to 11. However, we also reference figures not directly included in this manuscript, derived from referenced publications including ‘Kay & Kirk ^[17]: Figure 5B’. This figure number corresponds with the figure number in the original publication by Kay & Kirk (2000) (full reference below).

Kay, R.F. and Kirk, E.C. Osteological evidence for the evolution of activity pattern and visual acuity in primates. American Journal of Physical Anthropology: The Official Publication of the American Association of Physical Anthropologists, 2000, 113(2), pp.235-262.

 

This referencing follows formatting guidelines, but for extra clarity, we have changed the capitalised ‘F’ to lowercase and abbreviated the term to ‘fig.’ for any cited figure that is not used directly in this manuscript. However, we delegate the final decision about how to format this to the journal.

9. 9.2 is mentioned but lacking

Figure 9.2 is referenced throughout the text as being published in

[41] Lundeen, I.K.  Making scents of olfactory sensitivity in lorises and pottos. Behaviour, Ecology and Evolutionary Biology of Lorises and Pottos. Cambridge University Press, Cambridge, 2020, pp.97-112.

 

We cite this example from within the text, ‘([41]: Figure 9.2, C& D)’, and the associated reference is available in the reference list. IThis referencing follows formatting guidelines. See also our response to Comment 8 by Reviewer 1, as it is the same issue.

10. Figure 11 – A and B missing

The letters A and B have been added to the figure as shown in the attached form copy

Author Response File: Author Response.docx

Reviewer 2 Report

Comments and Suggestions for Authors

 

The manuscript visualizes, measures, and interprets skull structures of a fossil primate for inference of sensory capabilities and evolutionary/phylogenetic evidence.  The manuscript is well written, detailed, well-referenced, and the conclusions generally follow logically from data and analyses presented.  I do wonder whether the text could be cut back in some of the ‘description’ sections of the manuscript where the text is very detailed and extensive.  Perhaps some of this description could be moved to online files and the description summarized in a more efficient manner for the main paper text along with the nice figure representations of the various bones/anatomy/shapes?  The authors might also consider the following in editing/revising/improving their nice manuscript:

1)   line 19.  It is not clear what ‘specimen’ is being referred to here, as it has not been noted in the abstract whether there are one or more specimens of Mioeuoticus that have been collected, and a particular specimen (KNM-RU 2052) is noted only later in the abstract.

2)   Line 34.  Change ‘specious’ to ‘speciose’?

3)   Line 44. Say here that the fossils discovered ‘double the temporal range of crown lorisoids’, but what was the original temporal range (that was doubled) based on if not the fossils?  Maybe clarify a bit?

4)   Line 72.  The abbreviation ‘OFQ’ does not seem to be defined until later on line 159?

5)   Line 77.  Where say, ‘OFQ gives a direct indication as to the degree of visual acuity in a primate’, it seems more correct to say, ‘OFQ represents a solid proxy for the degree of visual acuity in a primate’ or some other wording instead of ‘direct indication’, since the inference is pretty indirect?

6)   Line 92.  The authors say that odorant molecules ‘interpret’ smell, but it is more accurate to say these molecules help to ‘detect’ odorants and then smell in ‘interpreted’ more by the brain, which is the way the authors explain this in the next sentence?

7)   Line 114.  Can fluid ‘undulate’, or is there a better word choice here?

8)   Line 172.  It is maybe too strong to say that this is an ‘accurate estimation’?  It is more of a rough estimate maybe, or the authors’ definition of ‘accurate’ in this context should be given. 

9)   Line 177.  I am not familiar with the latest literature on the validity of the various measures and proxies that the authors’ use in this section, so I am trusting that their judgment in using these measures/equations/proxies rather than alternatives.

10)                   Line 255.  Maybe explain briefly why breakage, fragmentation, or distortion of the fossil relative to its state in life results generally in underestimation of measurements and not overestimation?

11)                   Figure 9.  Here and in other places in the text, the authors seem to generally use correlations between characters that do not account for phylogenetic relatedness of different species?  It might be best for the authors to explicitly state which of their calculations throughout the paper are centered on inferences based on phylogenetically-corrected correlations vs. straight correlations.

 

Author Response

• line 19.  It is not clear what ‘specimen’ is being referred to here, as it has not been noted in the abstract whether there are one or more specimens of Mioeuoticusthat have been collected, and a particular specimen (KNM-RU 2052) is noted only later in the abstract.

Line 19 – The sentence has been rephrased to ‘of Mioeuoticus shipmani specimen (KNM-RU 2052)…’ for clarification. Further down, the specimen reference of ‘(KNM-RU 2052)’ is deleted.

2)   Line 34.  Change ‘specious’ to ‘speciose’?

Line 34 – ‘specious’ has been changed to ‘speciose’.

• Line 44. Say here that the fossils discovered ‘double the temporal range of crown lorisoids’, but what was the original temporal range (that was doubled) based on if not the fossils?  Maybe clarify a bit?

We have deleted the statement that the fossils discovered ‘double the temporal range of crown lorisoids’ as we consider that this point was not significant and created confusion.

4)   Line 72.  The abbreviation ‘OFQ’ does not seem to be defined until later on line 159?

Line 72 – The abbreviation of ‘OFQ’ is now defined as ‘Optic Foramen Quotient (OFQ) in the first instance on this line and is reduced solely to the abbreviation of ‘OFQ’ on line 159.

5)   Line 77.  Where say, ‘OFQ gives a direct indication as to the degree of visual acuity in a primate’, it seems more correct to say, ‘OFQ represents a solid proxy for the degree of visual acuity in a primate’ or some other wording instead of ‘direct indication’, since the inference is pretty indirect?

Line 77 – This sentence has been rephrased as recommended and now reads: ‘OFQ gives a solid proxy for the degree of visual acuity in a primate….’

6)   Line 92.  The authors say that odorant molecules ‘interpret’ smell, but it is more accurate to say these molecules help to ‘detect’ odorants and then smell in ‘interpreted’ more by the brain, which is the way the authors explain this in the next sentence?

Line 92 – The sentence has been rephrased to ‘molecules that detect odorants that the brain interprets as smell’ as we agree this is more accurate.

7)   Line 114.  Can fluid ‘undulate’, or is there a better word choice here?

Line 114 - The word ‘undulates’ has been replaced with ‘vibrate’.

8)   Line 172.  It is maybe too strong to say that this is an ‘accurate estimation’?  It is more of a rough estimate maybe, or the authors’ definition of ‘accurate’ in this context should be given. 

Line 172 - The word ‘accurate’ has been removed, and so the line now reads simply as ‘substitute and estimation…’

9)   Line 177.  I am not familiar with the latest literature on the validity of the various measures and proxies that the authors’ use in this section, so I am trusting that their judgment in using these measures/equations/proxies rather than alternatives.

The reviewer's concern about this particular issue is further discussed in lines 682-689, where we mention that more recent studies have assessed the validity of the metric by Kirk & Kay, and even though we acknowledge the shortcomings of this method, it is still the most reliable.

10)  Line 255.  Maybe explain briefly why breakage, fragmentation, or distortion of the fossil relative to its state in life results generally in underestimation of measurements and not overestimation?

We have extended our explanation of fragmentation and underestimation of surface area further, which now reads, ‘These data are likely an underestimation as fragmentation of the turbinals reduces their overall surface area to less than that of the original total turbinal structure and turbinal surface area present in the living Mioeuoticus nasal cavities…..’

11)  Figure 9.  Here and in other places in the text, the authors seem to generally use correlations between characters that do not account for phylogenetic relatedness of different species?  It might be best for the authors to explicitly state which of their calculations throughout the paper are centered on inferences based on phylogenetically-corrected correlations vs. straight correlations.

Line 171: Re-doing the Kirk & Kay (2000) analysis using phylogenetic generalised least squares regressions is beyond the scope of our study. We have used the same regression lines calculated by Kirk & Kay (2000) and subsequent publications studying primate visual acuity, which allows us to compare our data with all previous results for analysis.

 

Author Response File: Author Response.docx