Eat, heat and listen: on becoming a mammal

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Mammals share unique characters such as warm bloodedness (endothermy), anterior teeth that replace only once (diphyodonty), three high-frequency sound detecting bones in the ear and a novel jaw joint, enhanced senses, hair or fur, and lactation. The appearance of mammals heralded the replacement of 'ancient' faunas with animals we recognise today including birds, lizards and snakes and the origins of modern terrestrial ecosystems. The traditional view holds that these traits evolved in an integrated fashion, however new data and methods suggest either stepwise or mosaic evolution of traits, challenging our perspective of the evolutionary drivers of mammalian origins. The aim of this proposal is to resolve this problem and determine how, why and when three key mammalian traits evolved: endothermy, diphyodonty, and the jaw joint - middle ear complex. Bony traits such as teeth, jaws and ear bones are recorded in the fossil record. 'Soft' traits such as sensory abilities or endothermy do not fossilize and are inferred from other evidence. In the past 10 years, new fossils and technologies have enriched our understanding but present a complex picture. Current studies date the origins of endothermy to anywhere from the Carboniferous to the Early Cretaceous - a range of nearly 200 million years. Our team have questioned the traditional, textbook narrative of ear and jaw evolution, and whether the closest ancestors of mammals were already warm-blooded. These questions are far from resolved. Furthermore, we lack a thorough perspective as South American fossils closely related to mammal ancestors are yet to be included in quantitative analysis. Moreover, despite data on the development of the jaw and ear in living mammals being pivotal to the mammalian origins debate for decades, we still lack real integration of developmental and palaeontological data in understanding mammalian jaw, ear and tooth evolution. In this proposal we seek to resolve the phylogenetic and temporal basis of the evolution of jaws, ears, teeth and endothermy across the origin of mammals via a multidisciplinary approach that involves: a, working with partners and new fossil data from South America key to understanding mammalian origins; b, integrating the study of fossils and developmental sequence data; c, applying novel methods to deduce 'soft' traits, growth and endothermic potential. We will generate high-resolution X-ray tomography datasets of fossils that span mammalian origins. We will use novel techniques pioneered by our team to count rings in acellular dental cementum, that, like tree rings, preserve the age of an individual fossil and its teeth. This will tell us (a) how old teeth were when they erupted and the pattern and rate of tooth replacement pre- and post mammalian origins, producing a mechanistic model for early mammalian dental evolution. Then, using the number and width of cementum bands, we will (b) determine relative growth rates and use correlates with living animals to ascertain whether transition fossils possess a mammalian or 'reptilian' physiology, resolving the endothermy debate. Finally, we will use developmental sequences of platypus, echidna, opossum and mouse, including mutant c-Fos mice that retain postdentary bones at birth, along with new fossil datasets, to i. establish developmental and evolutionary anatomy; ii. using finite element analysis compare the function of developing joints to the anatomy and function of fossil jaw joints across the origin of mammals. This will tell us whether similar functional constraints and adaptation are at play in the evolution of the mammalian jaw as occur during development. This novel, multidisciplinary and cutting-edge combination of methods and datasets has never been applied to questions of mammalian, or indeed vertebrate evolution. The project will uncover fundamental new insights on the origin of mammals and will set a precedent for future studies of this kind.