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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References
Kielan-Jaworowska, Z., Cifelli, R. & Luo, Z.-X. Mammals from the Age of Dinosaurs. Origins, Evolution, and Structure (Columbia Univ. Press, 2004)
Luo, Z.-X. Transformation and diversification in early mammal evolution. Nature 450, 1011–1019 (2007)
Kemp, T. S. The Origin and Evolution of Mammals Ch. 4 (Oxford Univ. Press, 2005)
Bromham, L., Phillips, M. J. & Penny, D. Growing up with dinosaurs: molecular dates and the mammalian radiation. Trends Ecol. Evol. 14, 113–118 (1999)
Ji, Q., Luo, Z.-X., Yuan, C. X. & Tabrum, A. R. A swimming mammaliaform from the Middle Jurassic and ecomorphological diversification of early mammals. Science 311, 1123–1127 (2006)
Meng, J., Hu, Y., Wang, Y., Wang, X. & Li, C. A Mesozoic gliding mammal from northeastern China. Nature 444, 889–893 (2006)
Meredith, R. W. et al. Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334, 521–524 (2011)
dos Reis, M., Inoue, J., Asher, R. J., Donoghue, P. C. J. & Yang, Z. Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc. R. Soc. B 279, 3491–3500 (2012)
O’Leary, M. A. et al. The placental mammal ancestor and the post–K-Pg radiation of placentals. Science 339, 662–667 (2013)
Wilson, G. P. et al. Adaptive radiation of multituberculate mammals before the extinction of dinosaurs. Nature 483, 457–460 (2012)
Grossnickle, D. M. & Polly, P. D. Mammal disparity decreases during the Cretaceous angiosperm radiation. Proc. R. Soc. B 280, 20132110 (2013)
Kermack, K. A., Mussett, F. & Rigney, H. W. Lower jaw of Morganucodon. Zool. J. Linn. Soc. 53, 87–175 (1973)
Kermack, D. M., Kermack, K. A. & Mussett, F. The Welsh pantothere Kuehneotherium praecursoris. Zool. J. Linn. Soc. 47, 407–423 (1968)
Luo, Z.-X. Developmental patterns in Mesozoic evolution of mammal ears. Annu. Rev. Ecol. Evol. Syst. 42, 355–380 (2011)
Allin, E. F. & Hopson, J. A. in The Evolutionary Biology of Hearing (eds Webster, D. B., Fay, R. R. & Popper, A. N. ) 587–614 (Springer, 1992)
Crompton, W. A. & Jenkins, F. A. American Jurassic symmetrodonts and Rhaetic pantotheres. Science 155, 1006–1009 (1967)
Tseng, Z. J., Mcnitt-Gray, J. L., Flashner, H., Wang, X. & Enciso, R. Model sensitivity and use of the comparative finite element method in mammalian jaw mechanics: mandible performance in the gray wolf. PLoS ONE 6, e19171 (2011)
Therrien, F. Mandibular force profiles of extant carnivorans and implications for the feeding behaviour of extinct predators. J. Zool. 267, 249–270 (2005)
Freeman, P. W. & Lemen, C. A. Simple predictors of bite force in bats: the good, the better and the better still. J. Zool. 282, 284–290 (2010)
Rayfield, E. J. Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annu. Rev. Earth Planet. Sci. 35, 541–576 (2007)
Evans, A. R. & Sanson, G. D. Biomechanical properties of insects in relation to insectivory: cuticle thickness as an indicator of insect ‘hardness’ and ‘intractability’. Aust. J. Zool. 53, 9–19 (2005)
Dumont, E. R. & Herrel, A. The effects of gape angle and bite point on bite force in bats. J. Exp. Biol. 206, 2117–2123 (2003)
Aguirre, L. F., Herrel, A., Van Damme, R. & Matthysen, E. Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community. Proc. R. Soc. Lond. B 269, 1271–1278 (2002)
Gardiner, B. G. New Rhaetic and Liassic beetles. Palaeontology 1, 87–88 (1961)
Grimaldi, D. & Engel, M. S. Evolution of the Insects 469–472 (Cambridge Univ. Press, 2005)
Freeman, P. W. & Lemen, C. A. Using scissors to quantify hardness of insects: do bats select or size or hardness? J. Zool. 271, 469–476 (2007)
Aguirre, L. F., Herrel, A., van Damme, R. & Matthysen, E. The implications of food hardness for diet in bats. Funct. Ecol. 17, 201–212 (2003)
Currey, J. D. Bones: Structure and Mechanics 58–60 (Princeton Univ. Press, 2002)
Purnell, M. A., Crumpton, N., Gill, P. G. & Rayfield, E. J. Within-guild dietary discrimination from 3-D textural analysis of tooth microwear in insectivorous mammals. J. Zool. 291, 249–257 (2013)
Gill, P. G. Kuehneotherium from the Mesozoic Fissure Fillings of South Wales. PhD thesis, Univ. Bristol. (2004)
Marinescu, R., Daegling, D. J. & Rapoff, A. J. Finite-element modeling of the anthropoid mandible: the effects of altered boundary conditions. Anat. Rec. 283, 300–309 (2005)
Bright, J. A. & Rayfield, E. J. The response of cranial biomechanical finite element models to variations in mesh density. Anat. Rec. 294, 610–620 (2011)
Dumont, E. R., Grosse, I. R. & Slater, G. J. Requirements for comparing the performance of finite element models of biological structures. J. Theor. Biol. 256, 96–103 (2009)
Cox, P. G., Fagan, M. J., Rayfield, E. J. & Jeffery, N. Finite element modelling of squirrel, guinea pig and rat skulls: using geometric morphometrics to assess sensitivity. J. Anat. 219, 696–709 (2011)
Crompton, A. W. & Hylander, W. L. in The Ecology and Biology of Mammal-like Reptiles (eds Hotton, N., MacLean, P. D., Roth, J. J. & Roth, E. C. ) 263–282 (Smithsonian Institution, 1986)
Kermack, K. A., Mussett, F. & Rigney, H. W. The skull of Morganucodon. Zool. J. Linn. Soc. 71, 1–158 (1981)
Bonaparte, J. F., Martinelli, A. G., Schultz, C. L. & Rubert, R. The sister group of mammals: small cynodonts from the Late Triassic of southern Brazil. Rev. Brasil. Paleont. 5, 5–27 (2003)
Bonaparte, J. F., Martinelli, A. G. & Schultz, C. L. New information on Brasilodon and Brasilitherium (Cynodontia, Probainognathia) from the Late Triassic, southern Brazil. Rev. Brasil. Paleont. 8, 25–46 (2005)
Hiiemae, K. W. & Houston, J. B. The structure and function of the jaw muscles in the rat (Rattus norvegicus L.). Zool. J. Linn. Soc. 50, 75–99 (1971)
Wainwright, P. C., Bellwood, D. R., Westneat, M. W., Grubrich, J. R. & Hoey, A. S. A functional morphospace for the skull of labrid fishes: patterns of diversity in a complex biomechanical system. Biol. J. Linn. Soc. 82, 1–25 (2004)
Bellwood, D. R., Wainwright, P. C., Fulton, C. J. & Hoey, A. S. Functional versatility supports coral reef biodiversity. Proc. R. Soc. B 273, 101–107 (2006)
Cuff, A. R. & Rayfield, E. J. Feeding mechanics in spinosaurid theropods and extant crocodilians. PLoS ONE 8, e65295 (2013)
Dumont, E. R. & Nicolay, C. W. Cross-sectional geometry of the dentary in bats. Zoology 109, 66–74 (2007)
Rasband, W. S. ImageJ (US National Institutes of Health, Bethesda, Maryland, 2012)
Davis, J. L., Santana, S. E., Dumont, E. R. & Grosse, I. R. Predicting bite force in mammals: two-dimensional versus three-dimensional lever models. J. Exp. Biol. 213, 1844–1851 (2010)
McHenry, C. R., Wroe, S., Clausen, P. D., Moreno, K. & Cunningham, E. Supermodeled sabercat, predatory behavior in Smilodon fatalis revealed by high-resolution 3D computer simulation. Proc. Natl Acad. Sci. USA 104, 16010–16015 (2007)
Donald, B. J. M. Practical Stress Analysis with Finite Elements Ch. 7 (Glasnevin, 2007)
Christiansen, P. A dynamic model for the evolution of sabrecat predatory bite mechanics. Zool. J. Linn. Soc. 162, 220–242 (2011)
Tseng, Z. J. & Binder, W. J. Mandibular biomechanics of Crocuta crocuta, Canis lupus, and the late Miocene Dinocrocuta gigantea (Carnivora, Mammalia). Zool. J. Linn. Soc. 158, 683–696 (2010)
Dumont, E. R., Piccirillo, J. & Grosse, I. R. Finite-element analysis of biting behavior and bone stress in the facial skeletons of bats. Anat. Rec. A 283, 319–330 (2005)
Scott, R. S. et al. Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436, 693–695 (2005)
Scott, R. S. et al. Dental microwear texture analysis: technical considerations. J. Hum. Evol. 51, 339–349 (2006)
Ungar, P. Dental microwear texture analysis of varswater bovids and Early Pliocene paleoenvironments of Langebaanweg, Western Cape Province, South Africa. J. Mamm. Evol. 14, 163–181 (2007)
Ungar, P. S., Grine, F. E. & Teaford, M. F. Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PLoS ONE 3, e2044 (2008)
Purnell, M. A., Hart, P. J. B., Baines, D. C. & Bell, M. A. Quantitative analysis of dental microwear in threespine stickleback: a new approach to analysis of trophic ecology in aquatic vertebrates. J. Anim. Ecol. 75, 967–977 (2006)
Calandra, I., Schulz, E., Pinnow, M., Krohn, S. & Kaiser, T. M. Teasing apart the contributions of hard dietary items on 3D dental microtextures in primates. J. Hum. Evol. 63, 85–98 (2012)
International Organization for Standardization. ISO 25178-2:2012. Geometrical Product Specifications (GPS) – Surface Texture: Areal – Part 2: Terms, Definitions and Surface Texture Parameters (International Organization for Standardization, 2012)
Vaughan, N. The diets of British bats (Chiroptera). Mammal Rev. 27, 77–94 (1997)
Barlow, K. E. The diets of two phonic types of the bat Pipistrellus pipistrellus in Britain. J. Zool. 243, 597–609 (1997)
Purnell, M. A., Seehausen, O. & Galis, F. Quantitative three-dimensional microtextural analysis of tooth wear as a tool for dietary discrimination in fishes. J. R. Soc. Interface http://dx.doi.org/10.1098/rsif.2012.0140 (4 April 2012)
Luo, Z.-X., Kielan-Jaworowska, Z. & Cifelli, R. L. In quest for a phylogeny of Mesozoic mammals. Acta Palaeontol. Pol. 47, 1–78 (2002)
Evans, S. E. & Kermack, K. A. in In the Shadow of the Dinosaurs, Early Mesozoic Tetrapods (eds Fraser, N. C. & Sues, H.-D. ) 271–283 (Cambridge Univ. Press, 1994)
Gill, P. G. Resorption of premolars in the early mammal Kuehneotherium praecursoris. Arch. Oral Biol. 19, 327–328 (1974)
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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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.
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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. c–e, 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). f–i, 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.
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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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DOI: https://doi.org/10.1038/nature13622
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