Brawn before bite in endemic Asian mammals after the end-Cretaceous extinction

Reviewer #1 (Public review):

Summary:

This work provides valuable new insights into the Paleocene Asian mammal recovery and diversification dynamics during the first ten million years post-dinosaur extinction. Studies that have examined the mammalian recovery and diversification post-dinosaur extinction have primarily focused on the North American mammal fossil record, and it's unclear if patterns documented in North America are characteristic of global patterns. This study examines dietary metrics of Paleocene Asian mammals and found that there is a body size disparity increase before dietary niche expansion and that dietary metrics track climatic and paleobotanical trends of Asia during the first 10 million years after the dinosaur extinction.

Strengths:

The Asian Paleocene mammal fossil record is greatly understudied, and this work begins to fill important gaps. In particular, the use of interdisciplinary data (i.e., climatic and paleobotanical) is really interesting in conjunction with observed dietary metric trends.

Weaknesses:

While this work has the potential to be exciting and contribute greatly to our understanding of mammalian evolution during the first 10 million years post-dinosaur extinction, the major weakness is in the dental topographic analysis (DTA) dataset.

There are several specimens in Figure 1 that have broken cusps, deep wear facets, and general abrasion. Thus, any values generated from DTA are not accurate and cannot be used to support their claims. Furthermore, the authors analyze all tooth positions at once, which makes this study seem comprehensive (200 individual teeth), but it's unclear what sort of noise this introduces to the study. Typically, DTA studies will analyze a singular tooth position (e.g., Pampush et al. 2018 Biol. J. Linn. Soc.), allowing for more meaningful comparisons and an understanding of what value differences mean. Even so, the dataset consists of only 48 specimens. This means that even if all the specimens were pristinely preserved and generated DTA values could be trusted, it's still only 48 specimens (representing 4 different clades) to capture patterns across 10 million years. For example, the authors note that their results show an increase in OPCR and DNE values from the middle to the late Paleocene in pantodonts. However, if a singular tooth position is analyzed, such as the lower second molar, the middle and late Paleocene partitions are only represented by a singular specimen each. With a sample size this small, it's unlikely that the authors are capturing real trends, which makes the claims of this study highly questionable.

Reviewer #2 (Public review):

Summary:

This study uses dental traits of a large sample of Chinese mammals to track evolutionary patterns through the Paleocene. It presents and argues for a 'brawn before bite' hypothesis - mammals increased in body size disparity before evolving more specialized or adapted dentitions. The study makes use of an impressive array of analyses, including dental topographic, finite element, and integration analyses, which help to provide a unique insight into mammalian evolutionary patterns.

Strengths:

This paper helps to fill in a major gap in our knowledge of Paleocene mammal patterns in Asia, which is especially important because of the diversification of placentals at that time. The total sample of teeth is impressive and required considerable effort for scanning and analyzing. And there is a wealth of results for DTA, FEA, and integration analyses. Further, some of the results are especially interesting, such as the novel 'brawn before bite' hypothesis and the possible link between shifts in dental traits and arid environments in the Late Paleocene. Overall, I enjoyed reading the paper, and I think the results will be of interest to a broad audience.

Weaknesses:

I have four major concerns with the study, especially related to the sampling of teeth and taxa, that I discuss in more detail below. Due to these issues, I believe that the study is incomplete in its support of the 'brawn before bite' hypothesis. Although my concerns are significant, many of them can be addressed with some simple updates/revisions to analyses or text, and I try to provide constructive advice throughout my review.

(1) If I understand correctly, teeth of different tooth positions (e.g., premolars and molars), and those from the same specimen, are lumped into the same analyses. And unless I missed it, no justification is given for these methodological choices (besides testing for differences in proportions of tooth positions per time bin; L902). I think this creates some major statistical concerns. For example, DTA values for premolars and molars aren't directly comparable (I don't think?) because they have different functions (e.g., greater grinding function for molars). My recommendation is to perform different disparity-through-time analyses for each tooth position, assuming the sample sizes are big enough per time bin. Or, if the authors maintain their current methods/results, they should provide justification in the main text for that choice.

Also, I think lumping teeth from the same specimen into your analyses creates a major statistical concern because the observations aren't independent. In other words, the teeth of the same individual should have relatively similar DTA values, which can greatly bias your results. This is essentially the same issue as phylogenetic non-independence, but taken to a much greater extreme.

It seems like it'd be much more appropriate to perform specimen-level analyses (e.g., Wilson 2013) or species-level analyses (e.g., Grossnickle & Newham 2016) and report those results in the main text. If the authors believe that their methods are justified, then they should explain this in the text.

(2) Maybe I misunderstood, but it sounds like the sampling is almost exclusively clades that are primarily herbivorous/omnivorous (Pantodonta, Arctostylopida, Anagalida, and maybe Tillodonta), which means that the full ecomorphological diversity of the time bins is not being sampled (e.g., insectivores aren't fully sampled). Similarly, the authors say that they "focused sampling" on those major clades and "Additional data were collected on other clades ... opportunistically" (L628). If they favored sampling of specific clades, then doesn't that also bias their results?

If the study is primarily focused on a few herbivorous clades, then the Introduction should be reframed to reflect this. You could explain that you're specifically tracking herbivore patterns after the K-Pg.

(3) There are a lot of topics lacking background information, which makes the paper challenging to read for non-experts. Maybe the authors are hindered by a short word limit. But if they can expand their main text, then I strongly recommend the following:

(a) The authors should discuss diets. Much of the data are diet correlates (DTA values), but diets are almost never mentioned, except in the Methods. For example, the authors say: "An overall shift towards increased dental topographic trait magnitudes ..." (L137). Does that mean there was a shift toward increased herbivory? If so, why not mention the dietary shift? And if most of the sampled taxa are herbivores (see above comment), then shouldn't herbivory be a focal point of the paper?

(b) The authors should expand on "we used dentitions as ecological indicators" (L75). For non-experts, how/why are dentitions linked to ecology? And, again, why not mention diet? A strong link between tooth shape and diet is a critical assumption here (and one I'm sure that all mammalogists agree with), but the authors don't provide justification (at least in the Introduction) for that assumption. Many relevant papers cited later in the Methods could be cited in the Introduction (e.g., Evans et al. 2007).

(c) Include a better introduction of the sample, such as explicitly stating that your sample only includes placentals (assuming that's the case) and is focused on three major clades. Are non-placentals like multituberculates or stem placentals/eutherians found at Chinese Paleocene fossil localities and not sampled in the study, or are they absent in the sampled area?

(d) The way in which "integration" is being used should be defined. That is a loaded term which has been defined in different ways. I also recommend providing more explanation on the integration analyses and what the results mean.

If the authors don't have space to expand the main text, then they should at least expand on the topics in the supplement, with appropriate citations to the supplement in the main text.

(4) Finally, I'm not convinced that the results fully support the 'brawn before bite' hypothesis. I like the hypothesis. However, the 'brawn before ...' part of the hypothesis assumes that body size disparity (L63) increased first, and I don't think that pattern is ever shown. First, body size disparity is never reported or plotted (at least that I could find) - the authors just show the violin plots of the body sizes (Figures 1B, S6A). Second, the authors don't show evidence of an actual increase in body size disparity. Instead, they seem to assume that there was a rapid diversification in the earliest Paleocene, and thus the early Paleocene bin has already "reached maximum saturation" (L148). But what if the body size disparity in the latest Cretaceous was the same as that in the Paleocene? (Although that's unlikely, note that papers like Clauset & Redner 2009 and Grossnickle & Newham 2016 found evidence of greater body size disparity in the latest Cretaceous than is commonly recognized.) Similarly, what if body size disparity increased rapidly in the Eocene? Wouldn't that suggest a 'BITE before brawn' hypothesis? So, without showing when an increase in body size diversity occurred, I don't think that the authors can make a strong argument for 'brawn before [insert any trait]".

Although it's probably well beyond the scope of the study to add Cretaceous or Eocene data, the authors could at least review literature on body size patterns during those times to provide greater evidence for an earliest Paleocene increase in size disparity.

Author response:

eLife Assessment

This important study fills a major geographic and temporal gap in understanding Paleocene mammal evolution in Asia and proposes an intriguing "brawn before bite" hypothesis grounded in diverse analytical approaches. However, the findings are incomplete because limitations in sampling design - such as the use of worn or damaged teeth, the pooling of different tooth positions, and the lack of independence among teeth from the same individuals - introduce uncertainties that weaken support for the reported disparity patterns. The taxonomic focus on predominantly herbivorous clades also narrows the ecological scope of the results. Clarifying methodological choices, expanding the ecological context, and tempering evolutionary interpretations would substantially strengthen the study.

We thank Dr. Rasmann for the constructive evaluation of our manuscript. Considering the reviewers’ comments, we plan to implement revisions to our study focusing on (1) expansion of the fossil sample description, including a detailed account of the process of excluding extremely worn or damaged teeth from all analyses, (2) expanded reporting of the analyses done on individual tooth positions, and tempering the interpretation of the pooled samples in light of the issues raised by reviewers, (3) providing a more comprehensive introduction that includes an overview of the Paleocene mammal faunas in south China, which unevenly samples certain clades whereas others are extremely rare, and why the current available fossil samples would not permit a whole-fauna analysis to be adequately conducted across the three land mammal age time bins of the Paleocene in China. We believe these revisions would substantially strengthen the study’s robustness and impact for understanding the ecomorphological evolution of the earliest abundant placental mammals during the Paleocene in Asia.

Public Reviews:

Reviewer #1 (Public review):

Summary:

This work provides valuable new insights into the Paleocene Asian mammal recovery and diversification dynamics during the first ten million years post-dinosaur extinction. Studies that have examined the mammalian recovery and diversification post-dinosaur extinction have primarily focused on the North American mammal fossil record, and it's unclear if patterns documented in North America are characteristic of global patterns. This study examines dietary metrics of Paleocene Asian mammals and found that there is a body size disparity increase before dietary niche expansion and that dietary metrics track climatic and paleobotanical trends of Asia during the first 10 million years after the dinosaur extinction.

Strengths:

The Asian Paleocene mammal fossil record is greatly understudied, and this work begins to fill important gaps. In particular, the use of interdisciplinary data (i.e., climatic and paleobotanical) is really interesting in conjunction with observed dietary metric trends.

Weaknesses:

While this work has the potential to be exciting and contribute greatly to our understanding of mammalian evolution during the first 10 million years post-dinosaur extinction, the major weakness is in the dental topographic analysis (DTA) dataset.

There are several specimens in Figure 1 that have broken cusps, deep wear facets, and general abrasion. Thus, any values generated from DTA are not accurate and cannot be used to support their claims. Furthermore, the authors analyze all tooth positions at once, which makes this study seem comprehensive (200 individual teeth), but it's unclear what sort of noise this introduces to the study. Typically, DTA studies will analyze a singular tooth position (e.g., Pampush et al. 2018 Biol. J. Linn. Soc.), allowing for more meaningful comparisons and an understanding of what value differences mean. Even so, the dataset consists of only 48 specimens. This means that even if all the specimens were pristinely preserved and generated DTA values could be trusted, it's still only 48 specimens (representing 4 different clades) to capture patterns across 10 million years. For example, the authors note that their results show an increase in OPCR and DNE values from the middle to the late Paleocene in pantodonts. However, if a singular tooth position is analyzed, such as the lower second molar, the middle and late Paleocene partitions are only represented by a singular specimen each. With a sample size this small, it's unlikely that the authors are capturing real trends, which makes the claims of this study highly questionable.

We thank Reviewer 1 for their careful review of our manuscript. A major external limitation of the application of DTA to fossil samples is the availability of specimens. Whereas a typical study design using extant or geologically younger/more abundant fossil species would preferably sample much larger quantities of teeth from each treatment group (time bins, in our case), the rarity of well-preserved Paleocene mammalian dentitions in Asia necessitates the analysis of small samples in order to make observations regarding major trends in a region and time period otherwise impossible to study (see Chow et al. 1977). That said, we plan to clarify methodological details in response to the reviewer’s comments, including a more comprehensive explanation of our criteria for exclusion of broken tooth crowns from the analyses. We also plan to expand our results reporting on individual tooth position analysis, potentially including resampling and/or simulation analyses to assess the effect of small and uneven samples on our interpretation of results. Lastly, we plan to revise the discussion and conclusion accordingly, including more explicit distinction between well-supported findings that emerge from various planned sensitivity analyses, versus those that are more speculative and tentative in nature.

Chow, M., Zhang, Y., Wang, B., and Ding, S. (1977). Paleocene mammalian fauna from the Nanxiong Basin, Guangdong Province. Paleontol. Sin. New Ser. C 20, 1–100.

Reviewer #2 (Public review):

Summary:

This study uses dental traits of a large sample of Chinese mammals to track evolutionary patterns through the Paleocene. It presents and argues for a 'brawn before bite' hypothesis - mammals increased in body size disparity before evolving more specialized or adapted dentitions. The study makes use of an impressive array of analyses, including dental topographic, finite element, and integration analyses, which help to provide a unique insight into mammalian evolutionary patterns.

Strengths:

This paper helps to fill in a major gap in our knowledge of Paleocene mammal patterns in Asia, which is especially important because of the diversification of placentals at that time. The total sample of teeth is impressive and required considerable effort for scanning and analyzing. And there is a wealth of results for DTA, FEA, and integration analyses. Further, some of the results are especially interesting, such as the novel 'brawn before bite' hypothesis and the possible link between shifts in dental traits and arid environments in the Late Paleocene. Overall, I enjoyed reading the paper, and I think the results will be of interest to a broad audience.

Weaknesses:

I have four major concerns with the study, especially related to the sampling of teeth and taxa, that I discuss in more detail below. Due to these issues, I believe that the study is incomplete in its support of the 'brawn before bite' hypothesis. Although my concerns are significant, many of them can be addressed with some simple updates/revisions to analyses or text, and I try to provide constructive advice throughout my review.

(1) If I understand correctly, teeth of different tooth positions (e.g., premolars and molars), and those from the same specimen, are lumped into the same analyses. And unless I missed it, no justification is given for these methodological choices (besides testing for differences in proportions of tooth positions per time bin; L902). I think this creates some major statistical concerns. For example, DTA values for premolars and molars aren't directly comparable (I don't think?) because they have different functions (e.g., greater grinding function for molars). My recommendation is to perform different disparity-through-time analyses for each tooth position, assuming the sample sizes are big enough per time bin. Or, if the authors maintain their current methods/results, they should provide justification in the main text for that choice.

We thank Reviewer 2 for raising several issues worthy of clarification. Separate analyses for individual tooth positions were performed but not emphasized in the first version of the study. In our revised version we plan to highlight the nuances of the results from premolar versus molar partition analyses.

Also, I think lumping teeth from the same specimen into your analyses creates a major statistical concern because the observations aren't independent. In other words, the teeth of the same individual should have relatively similar DTA values, which can greatly bias your results. This is essentially the same issue as phylogenetic non-independence, but taken to a much greater extreme.

It seems like it'd be much more appropriate to perform specimen-level analyses (e.g., Wilson 2013) or species-level analyses (e.g., Grossnickle & Newham 2016) and report those results in the main text. If the authors believe that their methods are justified, then they should explain this in the text.

We plan to emphasize individual tooth position analyses in our revisions, and provide a stronger justification for our current treatment of multiple teeth from the same individual specimens as independent samples. We recognize the statistical nonindependence raised by Reviewer 2, but we would point out that from an ecomorphological perspective, it is unclear to us that the heterodont dentition of these early Cenozoic placental mammals should represent a single ecological signal (and thus warrant using only a single tooth position as representative of an individual’s DTA values). We plan to closely examine the nature of nonindependence in the DTA data within individuals, to assess a balanced approach to maximize information content from the relatively small and rare fossil samples used, while minimizing signal nonindependence across the dentition.

(2) Maybe I misunderstood, but it sounds like the sampling is almost exclusively clades that are primarily herbivorous/omnivorous (Pantodonta, Arctostylopida, Anagalida, and maybe Tillodonta), which means that the full ecomorphological diversity of the time bins is not being sampled (e.g., insectivores aren't fully sampled). Similarly, the authors say that they "focused sampling" on those major clades and "Additional data were collected on other clades ... opportunistically" (L628). If they favored sampling of specific clades, then doesn't that also bias their results?

If the study is primarily focused on a few herbivorous clades, then the Introduction should be reframed to reflect this. You could explain that you're specifically tracking herbivore patterns after the K-Pg.

We plan to revise the introduction section to more accurately reflect the emphasis on those clades. However, we would note that conventional dietary ecomorphology categories used to characterize later branching placental mammals are likely to be less informative when applied to their Paleocene counterparts. Although there are dental morphological traits that began to characterize major placental clades during the Paleocene, distinctive dietary ecologies have not been demonstrated for most of the clade representatives studied. Thus, insectivory was probably not restricted to “Insectivora”, nor carnivory to early Carnivmorpha or “Creodonta”, each of which represented less than 5% of the taxonomic richness during the Paleocene in China (Wang et al. 2007).

Wang, Y., Meng, J., Ni, X., and Li, C. (2007). Major events of Paleogene mammal radiation in China. Geol. J. 42, 415–430.

(3) There are a lot of topics lacking background information, which makes the paper challenging to read for non-experts. Maybe the authors are hindered by a short word limit. But if they can expand their main text, then I strongly recommend the following:

(a) The authors should discuss diets. Much of the data are diet correlates (DTA values), but diets are almost never mentioned, except in the Methods. For example, the authors say: "An overall shift towards increased dental topographic trait magnitudes ..." (L137). Does that mean there was a shift toward increased herbivory? If so, why not mention the dietary shift? And if most of the sampled taxa are herbivores (see above comment), then shouldn't herbivory be a focal point of the paper?

We plan to revise the text to make clearer connections between DTA and dietary inferences, and at the same time advise caution in making one-to-one linkages between them. Broadly speaking, dental indices such as DTA are phenotypic traits, and as in other phenotypic traits, the strength of structure-function relationships needs to be explicitly established before dietary ecological inferences can be confidently made. There is, to date, no consistent connection between dental topology and tooth use proxies and biomechanical traits in extant non-herbivorous species (e.g., DeSantis et al. 2017, Tseng and DeSantis 2024), and in our analyses, FEA and DTA generally did not show strong correlations to each other. Thus, we plan to continue to exercise care in interpreting DTA data as dietary data.

DeSantis LRG, Tseng ZJ, Liu J, Hurst A, Schubert BW, Jiangzuo Q. Assessing niche conservatism using a multiproxy approach: dietary ecology of extinct and extant spotted hyenas. Paleobiology. 2017;43(2):286-303. doi:10.1017/pab.2016.45

Tseng ZJ, DeSantis LR. Relationship between tooth macrowear and jaw morphofunctional traits in representative hypercarnivores. PeerJ. 2024 Nov 11;12:e18435.

(b) The authors should expand on "we used dentitions as ecological indicators" (L75). For non-experts, how/why are dentitions linked to ecology? And, again, why not mention diet? A strong link between tooth shape and diet is a critical assumption here (and one I'm sure that all mammalogists agree with), but the authors don't provide justification (at least in the Introduction) for that assumption. Many relevant papers cited later in the Methods could be cited in the Introduction (e.g., Evans et al. 2007).

Thank you for this suggestion. We plan to expand the introduction section to better contextualize the methodological basis for the work presented.

(c) Include a better introduction of the sample, such as explicitly stating that your sample only includes placentals (assuming that's the case) and is focused on three major clades. Are non-placentals like multituberculates or stem placentals/eutherians found at Chinese Paleocene fossil localities and not sampled in the study, or are they absent in the sampled area?

We thank Reviewer 2 for raising this important point worthy of clarification. Multituberculates are completely absent from the first two land mammal ages in the Paleocene of Asia, and non-placentals are rare in general (Wang et al. 2007). We plan to provide more context for the taxonomic sampling choices made in the study.

Wang, Y., Meng, J., Ni, X., and Li, C. (2007). Major events of Paleogene mammal radiation in China. Geol. J. 42, 415–430.

(d) The way in which "integration" is being used should be defined. That is a loaded term which has been defined in different ways. I also recommend providing more explanation on the integration analyses and what the results mean.

If the authors don't have space to expand the main text, then they should at least expand on the topics in the supplement, with appropriate citations to the supplement in the main text.

We plan to clarify our usage of “integration” to enable readers to accurately interpret what we mean by it.

(4) Finally, I'm not convinced that the results fully support the 'brawn before bite' hypothesis. I like the hypothesis. However, the 'brawn before ...' part of the hypothesis assumes that body size disparity (L63) increased first, and I don't think that pattern is ever shown. First, body size disparity is never reported or plotted (at least that I could find) - the authors just show the violin plots of the body sizes (Figures 1B, S6A). Second, the authors don't show evidence of an actual increase in body size disparity. Instead, they seem to assume that there was a rapid diversification in the earliest Paleocene, and thus the early Paleocene bin has already "reached maximum saturation" (L148). But what if the body size disparity in the latest Cretaceous was the same as that in the Paleocene? (Although that's unlikely, note that papers like Clauset & Redner 2009 and Grossnickle & Newham 2016 found evidence of greater body size disparity in the latest Cretaceous than is commonly recognized.) Similarly, what if body size disparity increased rapidly in the Eocene? Wouldn't that suggest a 'BITE before brawn' hypothesis? So, without showing when an increase in body size diversity occurred, I don't think that the authors can make a strong argument for 'brawn before [insert any trait]".

Although it's probably well beyond the scope of the study to add Cretaceous or Eocene data, the authors could at least review literature on body size patterns during those times to provide greater evidence for an earliest Paleocene increase in size disparity.

We plan to provide a broader discussion and any supporting evidence from the Cretaceous and Eocene to either make a stronger case for “brawn before bite”, or to refine what we mean by brawn/size/size disparity.