Pamela G. Gill

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

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 period. The earliest mammals, representing the first 50 million years of their evolution and including the most basal taxa, are widely considered to be generalized insectivores. 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 joint—was decoupled from ecomorphological diversification. 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 gliding, but such well-preserved fossils of earlier mammals do not exist, 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 view, this pattern suggests that lineage splitting during the earliest stages of mammalian evolution was associated with ecomorphological specialization and niche partitioning.

Modeling the effects of cingula structure on strain patterns and potential fracture in tooth enamel

The mammalian cingulum is a shelf of enamel, which rings the base of the molar crown (fully or partially). Certain nonmammalian cynodonts show precursors of this structure, indicating that it may be an important dental character in the origins of mammals. However, there is little consensus as to what drove the initial evolution of the cingulum. Recent work on physical modeling of fracture mechanics has shown that structures which approximate mammalian dentition (hard enamel shell surrounding a softer/tougher dentine interior) undergo specific fracture patterns dependent on the material properties of the food items. Soft materials result in fractures occurring at the base of the stiff shell away from the contact point due to heightened tensile strains. These tensile strains occur around the margin in the region where cingula develop. In this article, we test whether the presence of a cingulum structure will reduce the tensile strains seen in enamel using basic finite element models of bilayered cones. Finite element models of generic cone shaped “teeth” were created both with and without cingula of various shapes and sizes. Various forces were applied to the models to examine the relative magnitudes and directions of average maximum principal strain in the enamel. The addition of a cingulum greatly reduces tensile strains in the enamel caused by “soft‐food” forces. The relative shape and size of the cingulum has a strong effect on strain magnitudes as well. Scaling issues between shapes are explored and show that the effectiveness of a given cingulum to reducing tensile strains is dependent on how the cingulum is created. Partial cingula, which only surround a portion of the tooth, are shown to be especially effective at reducing strain caused by asymmetrical loads, and shed new light on the potential early function and evolution of mammalian dentitions. J. Morphol., 2011.

Within-guild dietary discrimination from 3-D textural analysis of tooth microwear in insectivorous mammals

Resource exploitation and competition for food are important selective pressures in animal evolution. A number of recent investigations have focused on linkages between diversification, trophic morphology and diet in bats, partly because their roosting habits mean that for many bat species diet can be quantified relatively easily through faecal analysis. Dietary analysis in mammals is otherwise invasive, complicated, time consuming and expensive. Here we present evidence from insectivorous bats that analysis of three-dimensional (3-D) textures of tooth microwear using International Organization for Standardization (ISO) roughness parameters derived from sub-micron surface data provides an additional, powerful tool for investigation of trophic resource exploitation in mammals. Our approach, like scale-sensitive fractal analysis, offers considerable advantages over two-dimensional (2-D) methods of microwear analysis, including improvements in robustness, repeatability and comparability of studies. Our results constitute the first analysis of microwear textures in carnivorous mammals based on ISO roughness parameters. They demonstrate that the method is capable of dietary discrimination, even between cryptic species with subtly different diets within trophic guilds, and even when sample sizes are small. We find significant differences in microwear textures between insectivore species whose diet contains different proportions of ‘hard’ prey (such as beetles) and ‘soft’ prey (such as moths), and multivariate analyses are able to distinguish between species with different diets based solely on their tooth microwear textures. Our results show that, compared with previous 2-D analyses of microwear in bats, ISO roughness parameters provide a much more sophisticated characterization of the nature of microwear surfaces and can yield more robust and subtle dietary discrimination. ISO-based textural analysis of tooth microwear thus has a useful role to play, complementing existing approaches, in trophic analysis of mammals, both extant and extinct.

Models in palaeontological functional analysis

Models are a principal tool of modern science. By definition, and in practice, models are not literal representations of reality but provide simplifications or substitutes of the events, scenarios or behaviours that are being studied or predicted. All models make assumptions, and palaeontological models in particular require additional assumptions to study unobservable events in deep time. In the case of functional analysis, the degree of missing data associated with reconstructing musculoskeletal anatomy and neuronal control in extinct organisms has, in the eyes of some scientists, rendered detailed functional analysis of fossils intractable. Such a prognosis may indeed be realized if palaeontologists attempt to recreate elaborate biomechanical models based on missing data and loosely justified assumptions. Yet multiple enabling methodologies and techniques now exist: tools for bracketing boundaries of reality; more rigorous consideration of soft tissues and missing data and methods drawing on physical principles that all organisms must adhere to. As with many aspects of science, the utility of such biomechanical models depends on the questions they seek to address, and the accuracy and validity of the models themselves.

A new symmetrodont from the Early Cretaceous of England

Mesozoic symmetrodont mammals have long been of interest because of their ‘reversed triangle’ cusp pattern, considered a significant advance in molar evolution. Unfortunately, they are poorly represented in the fossil record. The genus Spalacotherium Owen 1854 was created from material collected from the earliest Cretaceous of Dorset, England. Other acute-angle symmetrodonts have been found from the lower Cretaceous of Spain (Krebs, 1985) and Texas (Patterson, 1956), the middle and late Cretaceous of Utah (Cifelli and Madsen, 1986, 1999; Cifelli, 1990; Cifelli and Gordon, 1999), and the late Cretaceous of Alberta (Fox, 1972, 1976, 1985). A complete skeleton of a symmetrodont, Zhangheotherium, was recently found in China (Hu et al, 1997), but generally knowledge of symmetrodont diversity is poor.

The mandible and dentition of the Early Cretaceous monotreme Teinolophos trusleri

Rich, T.H., Hopson, J.A., Gill, P.G., Trusler, P., Rogers-Davidson, S., Morton, S., Cifelli, R.L., Pickering, D., Kool, L., Siu, K., Burgmann, F.A., Senden, T., Evans, A.R., Wagstaff, B.E., Seegets-Villiers, D., Corfe, I.J., Flannery, T.F., Walker, K., Musser, A.M., Archer, M., Pian, R. & Vickers-Rich, P., June 2016. The mandible and dentition of the Early Cretaceous monotreme Teinolophos trusleri. Alcheringa 40, xx–xx. ISSN 0311-5518. The monotreme Teinolophos trusleri Rich, Vickers-Rich, Constantine, Flannery, Kool & van Klaveren, 1999 from the Early Cretaceous of Australia is redescribed and reinterpreted here in light of additional specimens of that species and compared with the exquisitely preserved Early Cretaceous mammals from Liaoning Province, China. Together, this material indicates that although T. trusleri lacked a rod of postdentary bones contacting the dentary, as occurs in non-mammalian cynodonts and basal mammaliaforms, it did not share the condition present in all living mammals, including monotremes, of having the three auditory ossicles, which directly connect the tympanic membrane to the fenestra ovalis, being freely suspended within the middle ear cavity. Rather, T. trusleri appears to have had an intermediate condition, present in some Early Cretaceous mammals from Liaoning, in which the postdentary bones cum ear ossicles retained a connection to a persisting Meckel’s cartilage although not to the dentary. Teinolophos thus indicates that the condition of freely suspended auditory ossicles was acquired independently in monotremes and therian mammals. Much of the anterior region of the lower jaw of Teinolophos is now known, along with an isolated upper ultimate premolar. The previously unknown anterior region of the jaw is elongated and delicate as in extant monotremes, but differs in having at least seven antemolar teeth, which are separated by distinct diastemata. The dental formula of the lower jaw of Teinolophos trusleri as now known is i2 c1 p4 m5. Both the deep lower jaw and the long-rooted upper premolar indicate that Teinolophos, unlike undoubted ornithorhynchids (including the extinct Obdurodon), lacked a bill. Thomas H. Rich [trich@museum.vic.gov.au], Sally Rogers-Davidson [srogers@museum.vic.gov.au], David Pickering [dpick@museum.vic.gov.au], Timothy F. Flannery [tim.flannery@textpublishing.com.au], Ken Walker [kwalker@museum.vic.gov.au], Museum Victoria, PO Box 666, Melbourne, Victoria 3001, Australia; James A. Hopson [jhopson@uchicago.edu], Department of Organismal Biology & Anatomy, University of Chicago,1025 East 57th Street, Chicago, IL 60637, USA; Pamela G. Gill [pam.gill@bristol.ac.uk], School of Earth Sciences, University of Bristol, Bristol BS8 1RJ, U.K. and Earth Science Department, The Natural History Museum, Cromwell Road, London SW7 5BD, UK; Peter Trusler [peter@petertrusler.com.au], Lesley Kool [koollesley@gmail.com], Doris Seegets-Villiers [doris.seegets-villiers@monash.edu], Patricia Vickers-Rich [pat.rich@monash.edu], School of Earth, Atmosphere and Environment, Monash University, Victoria 3800, Australia; Steve Morton [steve.morton@monash.edu], Karen Siu [karen.siu@monash.edu], School of Physics and Astronomy, Monash University, Victoria 3800, Australia; Richard L. Cifelli [rlc@ou.edu] Sam Noble Oklahoma Museum of Natural History, University of Oklahoma, Norman, OK 73072, USA; Flame A. Burgmann [flame.burgmann@monash.edu], Monash Centre for Electron Microscopy, 10 Innovation Walk, Monash University, Clayton, Victoria 3800, Australia; Tim Senden [Tim.Senden@anu.edu.au], Department of Applied Mathematics, Research School of Physical Sciences and Engineering, The Australian National University, Canberra, Australian Capital Territory 0200, Australia; Alistair R. Evans [alistair.evans@monash.edu], School of Biological Sciences, Monash University, Victoria 3800, Australia; Barbara E. Wagstaff [wagstaff@unimelb.edu.au], School of Earth Sciences, The University of Melbourne, Victoria 3010, Australia; Ian J. Corfe [ian.corfe@helsinki.fi], Institute of Biotechnology, Viikinkaari 9, 00014, University of Helsinki, Finland; Anne M. Musser [anne.musser@austmus.gov.au], Australian Museum, 1 College Street, Sydney NSW 2010 Australia; Michael Archer [m.archer@unsw.edu.au], School of Biological, Earth, and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia; Rebecca Pian [rpian@amnh.org], Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024-5192, USA. Received 7.4.2016; accepted 14.4.2016.

Morphological evolution of the mammalian jaw adductor complex

The evolution of the mammalian jaw during the transition from non‐mammalian synapsids to crown mammals is a key event in vertebrate history and characterised by the gradual reduction of its individual bones into a single element and the concomitant transformation of the jaw joint and its incorporation into the middle ear complex. This osteological transformation is accompanied by a rearrangement and modification of the jaw adductor musculature, which is thought to have allowed the evolution of a more‐efficient masticatory system in comparison to the plesiomorphic synapsid condition. While osteological characters relating to this transition are well documented in the fossil record, the exact arrangement and modifications of the individual adductor muscles during the cynodont–mammaliaform transition have been debated for nearly a century.

The role of miniaturization in the evolution of the mammalian jaw and middle ear

The evolution of the mammalian jaw is one of the most important innovations in vertebrate history, and underpins the exceptional radiation and diversification of mammals over the last 220 million years1,2. In particular, the transformation of the mandible into a single tooth-bearing bone and the emergence of a novel jaw joint—while incorporating some of the ancestral jaw bones into the mammalian middle ear—is often cited as a classic example of the repurposing of morphological structures3,4. Although it is remarkably well-documented in the fossil record, the evolution of the mammalian jaw still poses the paradox of how the bones of the ancestral jaw joint could function both as a joint hinge for powerful load-bearing mastication and as a mandibular middle ear that was delicate enough for hearing. Here we use digital reconstructions, computational modelling and biomechanical analyses to demonstrate that the miniaturization of the early mammalian jaw was the primary driver for the transformation of the jaw joint. We show that there is no evidence for a concurrent reduction in jaw-joint stress and increase in bite force in key non-mammaliaform taxa in the cynodont–mammaliaform transition, as previously thought5–8. Although a shift in the recruitment of the jaw musculature occurred during the evolution of modern mammals, the optimization of mandibular function to increase bite force while reducing joint loads did not occur until after the emergence of the neomorphic mammalian jaw joint. This suggests that miniaturization provided a selective regime for the evolution of the mammalian jaw joint, followed by the integration of the postdentary bones into the mammalian middle ear.Biomechanical analyses of mammaliaform and cynodont fossils demonstrate that miniaturization drove the evolutionary transformation of the mammalian jaw, which preceded the optimization of bite force-to-joint load in the mandible

Digital cranial endocast of Riograndia guaibensis (Late Triassic, Brazil) sheds light on the evolution of the brain in non-mammalian cynodonts

Abstract A digital cranial endocast of the specimen UFRGS-PV-596-T of Riograndia guaibensis was obtained from μCT scan images. This is a small cynodont, closely related to mammaliaforms, from the Late Triassic of Brazil. Riograndia has large olfactory bulb casts and the cerebral hemispheres region is relatively wider than in other non-mammaliaform cynodonts. Impressions of vessels were observed and a conspicuous mark on the dorsal surface was interpreted as the transverse sinus. The calculated encephalization quotient is greater than the range seen in most other non-mammaliaform cynodonts. The ratios between linear and area measurements of the dorsal surface suggest four evolutionary changes from a basal eucynodont morphology to mammaliaforms, involving an evolutionary increase of the relative size of the olfactory bulbs and the width of the cerebral hemispheres and cerebellum. The data supports the hypothesis of the neurological evolution of the mammalian lineage starting with a trend for an increase of the olfactory bulbs, which is associated with adaptations in the nasal cavity. This trend is suggested to be linked to the selective pressures for small-sized faunivorous, and probably nocturnal, animals, and represents an initial improvement of the sensory receptor system, subsequently leading to further development of the ‘superior’ structures for sensorial processing and integration.