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Derived faunivores are the forerunners of major synapsid radiations

Nature Ecology & Evolution volume 7, pages 1903–1913 (2023)Cite this article

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Abstract

Evolutionary radiations generate most of Earth’s biodiversity, but are there common ecomorphological traits among the progenitors of radiations? In Synapsida (the mammalian total group), ‘small-bodied faunivore’ has been hypothesized as the ancestral state of most major radiating clades, but this has not been quantitatively assessed across multiple radiations. To examine macroevolutionary patterns in a phylogenetic context, we generated a time-calibrated metaphylogeny (‘metatree’) comprising 1,888 synapsid species from the Carboniferous through the Eocene (305–34 Ma) based on 269 published character matrices. We used comparative methods to investigate body size and dietary evolution during successive synapsid radiations. Faunivory is the ancestral dietary regime of each major synapsid radiation, but relatively small body size is only established as the common ancestral state of radiations near the origin of Mammaliaformes in the Late Triassic. The faunivorous ancestors of synapsid radiations typically have numerous novel characters compared with their contemporaries, and these derived traits may have helped them to survive faunal turnover events and subsequently radiate.

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Fig. 1: Testing the hypothesis that small faunivores are the forerunners of synapsid radiations using diet and body size patterns through time.
Fig. 2: Diet and jaw length plotted against patristic distance for each of the five major synapsid radiations.

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Data availability

All data used in this study are available through the main tables and the Supplementary Information.

Code availability

A simplified version of the R code used for this study is available as a supplementary text file. The code used to create the metatree is available at https://github.com/graemetlloyd/metatree.

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Acknowledgements

For discussions and feedback, we thank G. Slater, G. W. Mantilla, L. Weaver, S. Santana, K.-D. Benton, A. Bormet, C. Law and E. Panciroli. This work was funded by the National Science Foundation: DEB-1754502 (to K.D.A) and DBI-1812126 (to D.M.G.).

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Author notes

  1. These authors contributed equally: Spencer M. Hellert, David M. Grossnickle.

Authors and Affiliations

  1. Negaunee Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA

    Spencer M. Hellert & Kenneth D. Angielczyk

  2. Department of Science and Mathematics, Columbia College Chicago, Chicago, IL, USA

    Spencer M. Hellert

  3. Department of Biology, University of Washington, Seattle, WA, USA

    David M. Grossnickle

  4. Natural Sciences Department, Oregon Institute of Technology, Klamath Falls, OR, USA

    David M. Grossnickle

  5. Independent Researcher, Amble, UK

    Graeme T. Lloyd

  6. North Carolina Museum of Natural Sciences, Raleigh, NC, USA

    Christian F. Kammerer

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Contributions

S.M.H., D.M.G. and K.D.A. designed the study. S.M.H., G.T.L. and D.M.G. produced the metatree phylogeny. All authors (S.M.H., D.M.G., G.T.L., C.F.K. and K.D.A.) helped in collecting data and writing the paper. S.M.H. and D.M.G. performed analyses.

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Correspondence to Spencer M. Hellert.

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Extended data

Extended Data Fig. 1 Jaw length (log10 mm) and diet regressed against patristic distance for pelycosaur subclades.

The dashed lines are used for clades in which there is only a single diet. Grey bands are 95% confidence intervals.

Extended Data Fig. 2 Jaw length (log10 mm) and diet regressed against patristic distance for therapsid subclades.

We do not include a quasibinomial model for Therocephalia because the model algorithm did not converge on a reasonable result; we instead present a linear model (dashed line). We did not fit regression models for diets of Biarmosuchia or Gorgonopsia because their members all have the same diets – the dashed lines are included to help emphasize the lack of diet change. Grey bands are 95% confidence intervals.

Extended Data Fig. 3 Jaw length (log10 mm) and diet regressed against patristic distance for cynodont subclades.

We do not include a quasibinomial model for Probainognathia because the model algorithm did not converge on a reasonable result; we instead present a linear model (dashed line). Grey bands are 95% confidence intervals.

Extended Data Fig. 4 Jaw length (log10 mm) and diet regressed against patristic distance for mammaliaform subclades.

The dashed lines are used for clades in which there is only a single diet. Grey bands are 95% confidence intervals.

Extended Data Fig. 5 Jaw length (log10 mm) and diet regressed against patristic distance for therian subclades.

Grey bands are 95% confidence intervals.

Extended Data Fig. 6 Diet (A) and jaw lengths (B) for all synapsids in our sample are plotted against patristic distance.

These are the similar plots to those in Figs. 1B and C, but the subclades (rather than five major radiations) are highlighted in this figure. The smaller, straight lines represent linear regressions for synapsid subclades, and the grey curves are LOESS fitted regression curves (fitted to all data) and associated 95% confidence interval bands. For diet, we plot linear models rather than quasibinomial models (such as in Fig. 2) because quasibinomial models could not be fit to many of the subclades (for example, see Extended Data Fig. 1–5). Multituberculates are not included in this plot as a separate group, but they are the major clade within Allotheria (Extended Data Fig. 4).

Extended Data Fig. 7 Ancestral state reconstructions of discrete diets.

The pie charts illustrate the scaled likelihood probabilities of the three diet categories. See Supplementary Fig. 1 for a phylogeny with tip labels, and see the Fig. 1 caption for silhouette sources.

Supplementary information

Supplementary Information

Supplementary Methods, Results, Fig. 1 and Tables 1–7.

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Supplementary Tables 6 and 7

Supplementary Table 6 Morphological character matrices used to create the phylogenetic metatree. Supplementary Table 7 Morphometric, diet and geologic age information on the sampled species (n = 404).

Supplementary Data 1

Nexus file of the dated majority-rule metatree for the sampled species (n = 404).

Supplementary Data 2

Nexus file of the full dated majority-rule metatree.

Supplementary Data 3

Nexus file of the full undated majority-rule metatree.

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Hellert, S.M., Grossnickle, D.M., Lloyd, G.T. et al. Derived faunivores are the forerunners of major synapsid radiations. Nat Ecol Evol 7, 1903–1913 (2023). https://doi.org/10.1038/s41559-023-02200-y

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