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Dietary specializations and diversity in feeding ecology of the earliest stem mammals

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Abstract

The origin and radiation of mammals are key events in the history of life, with fossils placing the origin at 220 million years ago, in the Late Triassic period1. The earliest mammals, representing the first 50 million years of their evolution and including the most basal taxa, are widely considered to be generalized insectivores1,2. This implies that the first phase of the mammalian radiation—associated with the appearance in the fossil record of important innovations such as heterodont dentition, diphyodonty and the dentary–squamosal jaw joint1,3—was decoupled from ecomorphological diversification2,4. Finds of exceptionally complete specimens of later Mesozoic mammals have revealed greater ecomorphological diversity than previously suspected, including adaptations for swimming, burrowing, digging and even gliding2,5,6, but such well-preserved fossils of earlier mammals do not exist1, and robust analysis of their ecomorphological diversity has previously been lacking. Here we present the results of an integrated analysis, using synchrotron X-ray tomography and analyses of biomechanics, finite element models and tooth microwear textures. We find significant differences in function and dietary ecology between two of the earliest mammaliaform taxa, Morganucodon and Kuehneotherium—taxa that are central to the debate on mammalian evolution. Morganucodon possessed comparatively more forceful and robust jaws and consumed ‘harder’ prey, comparable to extant small-bodied mammals that eat considerable amounts of coleopterans. Kuehneotherium ingested a diet comparable to extant mixed feeders and specialists on ‘soft’ prey such as lepidopterans. Our results reveal previously hidden trophic specialization at the base of the mammalian radiation; hence even the earliest mammaliaforms were beginning to diversify—morphologically, functionally and ecologically. In contrast to the prevailing view2,4, this pattern suggests that lineage splitting during the earliest stages of mammalian evolution was associated with ecomorphological specialization and niche partitioning.

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Figure 1: Digital reconstructions and biomechanical analyses of Morganucodon and Kuehneotherium jaws.
Figure 2: Quantitative textural analysis of microwear in bats and fossil mammaliaforms.

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Acknowledgements

We thank G. Armstrong, R. Asher, E. Bernard, P. Brewer, J. Bright, I. Corfe, A. Currant, A. Gill, T. Goddard, C. Hintermueller, J. Hooker, G. Jones, S. Lautenschlager, M. Lowe, F. Marone, F. Marx, C. Palmer, M. Pound, M. Ruecklin and J. Sibbick. This work was funded by Natural Environment Research Council grants NE/E010431/1 and NE/K01496X/1 to E.J.R. and P.G.G.; M.A.P. was supported by NE/G018189/1. Use of the Swiss Light Source, Paul Scherrer Institut, was supported by the European Commission 6th Framework Programme (RII3-CT-2004-506008).

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Authors and Affiliations

Authors

Contributions

E.J.R., P.G.G. and M.A.P. designed the study and wrote the paper; P.G.G., E.J.R., N.J.G. and M.S. collected the synchrotron radiation X-ray tomographic microscopy data; K.R.B. and P.G.G. collected the micro-computed tomography scan data; P.G.G. created the reconstructions and digital models, and analysed the biomechanical results; P.G.G. and E.J.R. interpreted the biomechanical results; P.G.G. prepared and acquired specimens for microwear analysis, M.A.P. and N.C. collected the microwear data, M.A.P. analysed and interpreted the microwear results.

Corresponding authors

Correspondence to Pamela G. Gill or Emily J. Rayfield.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Phylogenetic relationships of major Mesozoic mammal lineages.

Relative tree positions of Morganucodon and Kuehneotherium in red. Based on figure 1 in ref. 61. The filled green circle denotes the node for the mammalian crown group.

Extended Data Figure 2 Pontalun 3 fissure locality.

a, Map to show location of the Glamorgan quarries in South Wales, UK. The black square denotes the area of the map shown in b. Map attribution: Jhamez84. CC-BY-SA-3.0 (http://creativecommons.org/licenses/by-sa/3.0). b, Location of the Glamorgan quarries yielding tetrapod remains, with white arrow marking Pontalun quarry. Carboniferous limestone upland areas in grey. Modified from ref. 62.

Extended Data Figure 3 Molar form and specimens scanned to create the digital reconstructions of the dentaries of Morganucodon and Kuehneotherium.

a, NHMUK PV M92538, an isolated M. watsoni right lower molar (identified as m4) in lingual view. b, NHM NHMUK PV M9277, an isolated K. praecursoris right lower molar (mid-row) in lingual view; note the triangulation of the cusp arrangement. Both molars digitally reconstructed from micro-computed tomography scans and reversed to fit with views of the dentaries. ce, Specimens used for the digital reconstruction of M. watsoni: c, UMZC Eo.D.61 with m4 in situ; d, UMZC Eo.D.45 with p4, m1, m3 and m4 in situ; e, NHMUK PV M85507 with i1–i4 (NB the only Glamorgan specimen known with complete incisors in situ). fi, Specimens used for the digital reconstruction of K. praecursoris: f, NHMUK PV M19766 (paratype C865 in ref. 13) with coronoid process and condylar region; g, NHMUK PV M19749 (paratype C864 in ref. 13) postdentary trough region; h, UMZC Sy.97 with complete alveoli for m5–m6 and partial alveoli for m3–m4; i, NHMUK PV M92779 with alveoli for p1–m4 (U73 in ref. 63). All from Pontalun 3 fissure, except f and g from Pontalun 1 fissure, which ref. 30 assigned to the same hypodigm. All images show medial view. All are left dentaries, except c and d, which are reversed for ease of reference to the reconstructions in Fig. 1.

Extended Data Figure 4 Static loaded finite element models to represent the jaw at the moment of biting.

Right mandible models in lateral view of (a) Morganucodon and (b) Kuehneotherium to show muscle loading, constraints and bite points. Inset in a shows modelled rigid body used to simulate missing coronoid process, for posterior temporalis loading. AT, anterior temporalis; PT, posterior temporalis; SM, superficial masseter; DM, deep masseter. Constraints indicated at the jaw joint and three individual bite points at the mid molar (m2 in Morganucodon and m3 in Kuehneotherium), ultimate premolar (p4 in Morganucodon and p6 in Kuehneotherium) and canine. The muscle origin positions are shown for (c) Morganucodon and (d) Kuehneotherium. Morganucodon skull reconstruction from ref. 36 and Brasilitherium skull, used as a proxy for the unknown Kuehneotherium skull, from ref. 37. The teeth have been removed for consistency with the mandible models. See Methods for explanations.

Extended Data Table 1 Specimens used for the microtextural analysis of tooth microwear
Extended Data Table 2 Trophic categorization and diets of British bat species used for validation of microtextural analysis of early mammal teeth
Extended Data Table 3 Correlations between roughness parameters from Morganucodon and Kuehneotherium teeth and principal component axes 1 and 2 derived from analysis of the nine roughness parameters that differ between bat species
Extended Data Table 4 Loadings (eigenvectors) for roughness parameters onto principal component axes 1 and 2 for the PCA of bat species
Extended Data Table 5 Short definitions and categorization of three-dimensional areal surface texture parameters

Supplementary information

Supplementary Information

This file contains links to scan data videos and further FE model images. Information is also provided on systematics, repositories, choice of specimens, evidence for sympatry and potential prey. (PDF 194 kb)

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Gill, P., Purnell, M., Crumpton, N. et al. Dietary specializations and diversity in feeding ecology of the earliest stem mammals. Nature 512, 303–305 (2014). https://doi.org/10.1038/nature13622

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