Taxonomic Status of Nanotyrannus lancensis (Dinosauria: Tyrannosauroidea)—A Distinct Taxon of Small-Bodied Tyrannosaur

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

Longrich and Saitta report their conclusions about the taxonomic status of Nanotyrannus lancensis based on comprehensive analyses of multiple lines of evidence. In general, the data presented are solid, the analyses are convincing, the illustrations are informative, and the manuscript is well written, and I thus recommend the acceptance of this manuscript for publication in Fossils. Meanwhile I also have some suggestions for the authors, which might be helpful to improving the quality of this manuscript.

One issue is related to which specimens are really referable to Nanotyrannus. This is important because different lines of evidence used in this study are derived from different specimens. Without solid evidence supporting the referral of the relevant specimens to Nanotyrannus, it would be hard to convince the readers. I suggest the authors to expand the section on why the supposed Nanotyrannus specimens are really Nanotyrannus. One way is to add a phylogenetic analysis with all the supposed Nanotyrannus specimens treated as separate OTUs, and to see whether these fossils form a monophyletic group.

The authors use cluster analysis (strictly speaking, the method used by the authors is kind of overall-similarity-based phylogenetic method) to infer the taxonomic status of the supposed Nanotyrannus. Because the specimens used in the analysis belong to two classes of huge size difference, they are expected to form two discrete clusters. I am not saying that the method used here is not valid, but the result could be derived from factors other than taxonomy. One way to further test the conclusion is to run similar analysis on other tyrannosaur species that are represented by multiple specimens similar in size distribution to the ones used in this study. If the latter analysis produces multiple clusters or even no discrete clusters, it will provide strong support to the claim by the authors.

 There are issues pertaining to phrasing and/or format. For example, the authors use “primitive” and “derived” to describe the systematic position of some species in the text, but such usages have been abandoned for good reasons. I thus suggest the authors to replace “primitive” with “early-diverging” and replace “derived” with “late-diverging” (or other proper words) in those taxonomy-related phrasing throughout the text. One other minor issue related to phrasing is about the usage of holotype or type specimen. Only species have holotype, but there are phrasings such as “Stygivenator holotype”, “Nanotyrannus holotype”, and “the type of Nanotyrannus”. Please revise all sentences pertaining to this.  Also please italize all generic and species names in both text and figures (including the figures showing the cladgrams). Another case pertaining to phrasing is in clustering analysis section (and also in some places in the text). The authors use “intermediate morphologies” to refer to intermediate forms or intermediate morphotypes throughout the text, and this should be corrected.

 Other minor points:

Line 44: add a comma between “motion [11]” and “feeding”

 Lines 165-166: “in Tyrannosaurus”: here the authors might mean “in tyrannosaurids”

 Line 166: delete “t” before “closely appressed”

 Line 237: the authors might mean “< 2000 kg”

 Line 742: replace “Horizontal line” with “Vertical line”

Author Response

Longrich and Saitta report their conclusions about the taxonomic status of Nanotyrannus lancensis based on comprehensive analyses of multiple lines of evidence. In general, the data presented are solid, the analyses are convincing, the illustrations are informative, and the manuscript is well written, and I thus recommend the acceptance of this manuscript for publication in Fossils. Meanwhile I also have some suggestions for the authors, which might be helpful to improving the quality of this manuscript.

We thank the author for a constructive review.

One issue is related to which specimens are really referable to Nanotyrannus. This is important because different lines of evidence used in this study are derived from different specimens. Without solid evidence supporting the referral of the relevant specimens to Nanotyrannus, it would be hard to convince the readers. I suggest the authors to expand the section on why the supposed Nanotyrannus specimens are really Nanotyrannus. One way is to add a phylogenetic analysis with all the supposed Nanotyrannus specimens treated as separate OTUs, and to see whether these fossils form a monophyletic group.

 

We agree that this is an important issue, and that in our efforts to separate Nanotyrannus from Tyrannosaurus, we’ve probably spent too little time on trying to understand what unites the nanotyrannosaurs (Nanotyrannosaurini?) in the earlier drafts.

            We’d argue that first of all, given that the animals are occurring at the same place and time, they’re probably related at the clade level if not congeneric/conspecific. It’s unlikely that several unrelated lineages of basal Tyrannosauroidea go up to the K-Pg boundary- although we concede it’s not absolutely impossible- especially given their overall resemblance. As we discuss there could be more than one species.

            Most of the resemblances uniting these things are plesiomorphies, however. Almost all of the 150-something characters separating the animal from Tyrannosaurus are found in animals such as Alioramus or other basal tyrannosaurs.

            However, going back through the character list, a few character emerge as potential autapomorphies. These include

(i) the upturned premaxilla,

(ii) the procumbent premaxillary teeth (although arguably a single character),

(iii) possibly the unserrated premaxillary teeth (assuming this is derived)

(iv) the pneumatic foramen in the quadratojugal.

            A specimen-level phylogenetic analysis would be the ideal way to demonstrate that these animals form a clade but this is already a very long paper, so it might be best left to a future paper. However just based on the characters visible in our matrix, it seems quite clear these animals will tend to cluster together (we could do this analysis but it would be, as they say, like a drunk using a lamppost- for support, rather than illumination).

The authors use cluster analysis (strictly speaking, the method used by the authors is kind of overall-similarity-based phylogenetic method) to infer the taxonomic status of the supposed Nanotyrannus. Because the specimens used in the analysis belong to two classes of huge size difference, they are expected to form two discrete clusters. I am not saying that the method used here is not valid, but the result could be derived from factors other than taxonomy. One way to further test the conclusion is to run similar analysis on other tyrannosaur species that are represented by multiple specimens similar in size distribution to the ones used in this study. If the latter analysis produces multiple clusters or even no discrete clusters, it will provide strong support to the claim by the authors.

There’s a fair amount of variation between the smallest T. rex specimens and the largest, and between the smallest Nanotyrannus and the largest, and the larger Nanotyrannus like Jane approach the smaller T. rex in size. Given that, we’d expect the variation to be more continuous in nature.

            This idea- of a major gap between these morphologies- is a function of the data not our interpretation, and the observation isn’t ours: Carr (2020) notes the extreme difference that occurs between the largest Nanotyrannus and the smallest Tyrannosaurus. The difference is so extreme Carr is forced to invoke a sort of metamorphosis similar to that seen in fish to account for it.

There are issues pertaining to phrasing and/or format. For example, the authors use “primitive” and “derived” to describe the systematic position of some species in the text, but such usages have been abandoned for good reasons. I thus suggest the authors to replace “primitive” with “early-diverging” and replace “derived” with “late-diverging” (or other proper words) in those taxonomy-related phrasing throughout the text.

In some cases we’d agree with this argument. It’s probably incorrect to call centrosaurines “primitive” relative to chasmosaurines (or vice versa) since they are both specialized in different ways from the ancestral condition, beetles primitive relative to butterflies, or grasses primitive relative to composites. However in many cases some branches of the tree evolve more slowly so it is probably accurate to refer to their members as “primitive”.

In this particular case Nanotyrannus is almost entirely distinguished by the absence of derived features that characterized Tyrannosaurus— it shows the primitive or ancestral morphology in almost 150 characters, which is why it’s a somewhat frustrating exercise to come up with derived characters pulling the Nanotyrannus specimens together.

One other minor issue related to phrasing is about the usage of holotype or type specimen. Only species have holotype, but there are phrasings such as “Stygivenator holotype”, “Nanotyrannus holotype”, and “the type of Nanotyrannus”. Please revise all sentences pertaining to this.

Fixed

 Also please italize all generic and species names in both text and figures (including the figures showing the cladgrams). Another case pertaining to phrasing is in clustering analysis section (and also in some places in the text).

Added italics

The authors use “intermediate morphologies” to refer to intermediate forms or intermediate morphotypes throughout the text, and this should be corrected.

Replaced

Other minor points:

Line 44: add a comma between “motion [11]” and “feeding”

Added

Lines 165-166: “in Tyrannosaurus”: here the authors might mean “in tyrannosaurids”

Fixed

Line 166: delete “t” before “closely appressed”

fixed

Line 237: the authors might mean “< 2000 kg”

Fixed

Line 742: replace “Horizontal line” with “Vertical line”

This refers to a horizontal line here actually

Reviewer 2 Report

Comments and Suggestions for Authors

This manuscript is convincing and well constructed. The authors convincingly make the case for two or more tyrannosaur taxa in the latest Cretaceous of North America. Especially significant are the data from growth curves, from ontogenetically invariant characters, and from putative juvenile Tyrannosaurus specimens. I think that this work is ready to publish as-is after a once-over for grammar. However, I do have a few suggestions. These are only suggestions and should not hold up publication of the work. They follow, with PDF line numbers:

• 51: You might mention here that the issue isn’t whether they represent two similar species, but in fact two really disparate species. 

• 79: comma after ornithomimid

• 84: Remove comma after Brown. 

• 89: comma after 5866

• 102: Remove comma after Larson

• 103: Comma after and

• 121-123: Repetition of field party from Cleveland

• 127: Comma after and

• 137: I’d suggest removing “then” 

• 149: remove “as” before Aublysodon

• 156: comma after and 

• 165: comma after however; in general, check punctuation throughout

• 171: colon instead of comma

• 237: Reverse sign to <

• 308-309: Are at least some of these characters also stable between smaller and larger individuals of other tyrannosaurs, or even other archosaurs in general? This would permit a stronger statement owing to phylogenetic bracketing.

• 346: Also Marshosaurus.

• 387: Please somehow mark the characters you have explicitly found to be ontogenetically stable in this section and perhaps also the characters that are unknown re stability because you can’t see the relevant parts in comparative specimens (e.g., the tarbosaurus juvenile) and the characters that may be ontogenetically labile.

• 436: characters

• 460: can you cite a paper that shows such a continuum for an ontogenetic series analyzed using NJ (and say “as in….”)?

• 473: is there a citation for the obfuscation statement?

• 489: comma after variable

• 508: Can you make a table or better show a photo or two of the juvenile tarbosaurus pointing out the tyrannosaurine characters absent in Nanotyrannus? Maybe you can get a photo from Larry Witmer or pull one from the Witmer Lab website etc.? Could show next to the Nanotyrannus skull just for emphasis? 

• https://journals.sagepub.com/doi/abs/10.1177/1559827617695783?

• 613: How rugose are the bones of the nano holotype?

• 819: check punctuation etc. in this sentence.

• 971: Also mention the UCMP frontal here.

• 1134: Needs a second dash

• Maybe in general/somewhere you can write a short, more specific refutation of Carr (2020), citing the issues with this work that cause it to reach the wrong conclusion and/or the new information considered by you that would change that conclusion.

 

Author Response

Response to Reviewer 1 (see also attached file)

• 51: You might mention here that the issue isn’t whether they represent two similar species, but in fact two really disparate species.

Changed to “…which showed remarkable variation through development, or highly distinct genera”

• 79: comma after ornithomimid

added

• 84: Remove comma after Brown.

removed

• 89: comma after 5866

added

• 102: Remove comma after Larson

Removed

• 103: Comma after and

Added

• 121-123: Repetition of field party from Cleveland

Deleted

• 127: Comma after and

Added

• 137: I’d suggest removing “then”

Removed

• 149: remove “as” before Aublysodon

Removed

• 156: comma after and

Added

• 165: comma after however; in general, check punctuation throughout

Added

• 171: colon instead of comma

fixed

• 237: Reverse sign to <

Fixed

• 308-309: Are at least some of these characters also stable between smaller and larger individuals of other tyrannosaurs, or even other archosaurs in general? This would permit a stronger statement owing to phylogenetic bracketing.

We found a number of the characters to be stable in Tarbosaurus and mark these in a supplementary table.

• 346: Also Marshosaurus.

ADDED

• 387: Please somehow mark the characters you have explicitly found to be ontogenetically stable in this section and perhaps also the characters that are unknown re stability because you can’t see the relevant parts in comparative specimens (e.g., the tarbosaurus juvenile) and the characters that may be ontogenetically labile.

We have marked these in a supplementary table.

• 436: characters

Fixed

• 460: can you cite a paper that shows such a continuum for an ontogenetic series analyzed using NJ (and say “as in….”)?

Not sure- our technique seems to be novel? It’s not a brilliant, high-tech approach (it takes about 3 seconds on PAUP, it’s far faster than other techniques) but unlike cladistic approaches it factors in branch lengths.

• 473: is there a citation for the obfuscation statement?

We found this experimentally- the algorithm has trouble calculating similarity when there are few overlapping scorings. In the end we found that the UPGMA algorithm fixed this issue; it is able to produce clusters that capture the gappiness of the data, even with very fragmentary taxa.

• 489: comma after variable

Fixed

• 508: Can you make a table or better show a photo or two of the juvenile tarbosaurus pointing out the tyrannosaurine characters absent in Nanotyrannus? Maybe you can get a photo from Larry Witmer or pull one from the Witmer Lab website etc.? Could show next to the Nanotyrannus skull just for emphasis?

We have added a character showing ontogenetically invariant characters in young Tarbosaurus, which are absent in Nanotyrannus.

• https://journals.sagepub.com/doi/abs/10.1177/1559827617695783?

??

• 613: How rugose are the bones of the nano holotype?

Quite rugose. We have added a figure.

• 819: check punctuation etc. in this sentence.

Needs an “of”, added

• 971: Also mention the UCMP frontal here.

This should mention the frontal not the LACM specimen; corrected

• 1134: Needs a second dash

added

• Maybe in general/somewhere you can write a short, more specific refutation of Carr (2020), citing the issues with this work that cause it to reach the wrong conclusion and/or the new information considered by you that would change that conclusion.

We have added a “Critique of Previous Work” section discussing problems with Carr 1999, Carr and Williamson, 2004, and Carr 2020.

 

 

Reviewer 3 Report

Comments and Suggestions for Authors

This is a well-written and convincing paper dealing with the long-enduring problem of the status of Nanotyrannus. The authors use several independent approaches to determine whether it should be considered as a juvenile Tyrannosaurus rex or not, and conclude that should not, since all lines of evidence point in the same direction. I found the author's arguments generally convincing. I am moderately impressed by comparisons of species diversity with predatory mammals and marine vertebrates, but the reader may form his own opinion. I am not an expert on bone histology, but the demonstrations based on this line of evidence seem logical and convincing. The final section about species recognition in palaeontology is rather long and a little rambling but it is nonetheless interesting, although not essential to the paper. As there is no real length limits for papers published in this journal, I see no special reason to shorten or delete it.

The paper can be published after minor corrections are made. I have noted many small typos or mistakes directly on the MS. A recurrent problem is the lack of italics for generic and specific taxon names - this should be checked carefully. Similarly, the list of references deserves a thorough check. I have noted several incomplete references and there may be more. In addition, the references do not follow the journal style, according to which the names of periodicals should be abbreviated.

Once these minor issues are attended to, the paper can be published without any major changes.

Comments for author File: Comments.pdf

Comments on the Quality of English Language

The auhors being native English speakers, the quality of the English is generally excellent - only a few minor typos and errors should be corrected.

Author Response

RESPONSE TO REVIEWER 2. 

NOTE- in addition we have attached responses made directly to the PDF, because the comments are not always clear out-of-context. -NL

This is a well-written and convincing paper dealing with the long-enduring problem of the status of Nanotyrannus. The authors use several independent approaches to determine whether it should be considered as a juvenile Tyrannosaurus rex or not, and conclude that should not, since all lines of evidence point in the same direction. I found the author's arguments generally convincing. I am moderately impressed by comparisons of species diversity with predatory mammals and marine vertebrates, but the reader may form his own opinion. I am not an expert on bone histology, but the demonstrations based on this line of evidence seem logical and convincing. The final section about species recognition in palaeontology is rather long and a little rambling but it is nonetheless interesting, although not essential to the paper. As there is no real length limits for papers published in this journal, I see no special reason to shorten or delete it.

The paper can be published after minor corrections are made. I have noted many small typos or mistakes directly on the MS. A recurrent problem is the lack of italics for generic and specific taxon names - this should be checked carefully. Similarly, the list of references deserves a thorough check. I have noted several incomplete references and there may be more. In addition, the references do not follow the journal style, according to which the names of periodicals should be abbreviated.

Once these minor issues are attended to, the paper can be published without any major changes.

We thank the reviewer for a refreshingly constructive review.

39. This is debatable (see claims about Giganotosaurus and other very large theropods) and not really important in the context of this paper.

Whether T. rex is the largest dinosaur or not is scientifically not relevant here, but it is part of the larger fascination with T. rex (no pun intended). What’s interesting isn’t just the debate but that it’s been such a protracted debate, not on an obscure animal, but a very famous, well-studied one.

45. I find this debatable

One can go on Google Scholar and search “Tyrannosaurus” and it goes on for at least 50 pages (this paper is on page 50, where we stopped, as a preprint!)

There are something like 5500 mammal species, around 10,000 birds, 10,000 lizards, 8,000 frogs. It seems unlikely most of these have been published on as much as T. rex, and for many species there are probably fewer in museums than there are for Tyrannosaurus.

Again what is interesting here is not just the science, but how the science is done. It would be unsurprising for an obscure, understudied, poorly known dinosaur to be debated. What’s bizarre is that it is so well-known and well studied, and yet (we argue) people have gotten it very wrong

70. delete

Deleted

74. to some extent only, since its real description was published several years after the deaths of Marsh and Cope

fair enough, have added “ although it would not be known or studied in detail until many years later. “

123. Delete

Deleted

150. Delete

Deleted

166. do you really mean Tyrannosaurus ? Rather Tyrannosauridae, maybe.

Changed to “Tyrannosauridae”

179. a

Added “a”

183. Italics

Fixed

189. sectioned

Changed to sectioned

224. dozens

Changed to “dozens”

225. delete

Deleted

226. are

added                                                   

237. should be the reverse

Reversed

241. italics
242. italics
243. italics

Italicized

244. delete

Deleted

248. delete

Deleted

255. delete

Deleted

279. circle ?

Corrected

305. should be "are" since postcrania are meant. Or use ^"postcranium"

Corrected

367. of

Added

398. characters

Added

1. 21 italics

added

454 we

We think the original reads better here

671. is "teenage" the right term for a dinosaur ?

Literally a specimen in this size range would be about 15… but this may be confusing, so we’ve changed it to “juvenile”

816. Italics

Fixed

899. italics

Italicized

918. to

Added

Individuals

Fixed

1068. Develop in

Fixed

1277. incomplete reference

Fixed

1325 Incomplete reference

Fixed

1331. Chen, P.J.

Fixed

1398. incomplete reference

Fixed

1515. incomplete reference

Fixed

1531. Incomplete reference

Fixed

1542. Incomplete reference

Fixed

1569. incomplete reference

Fixed

Author Response File: Author Response.pdf