Understanding the functional evolution of the mammalian middle ear and jaw joint across the cynodont-mammaliaform transition

哺乳动物的起源和进化是脊椎动物进化史上的一个关键事件，也是进化转型的教科书范例。从大约2.3亿年前开始，化石记录记录了一系列保存完好的过渡化石，这些化石进化出了哺乳动物的关键特征，如乳牙和恒牙，大大脑，坚固的头骨和独特的哺乳动物中耳。哺乳动物的中耳不是单一的中耳骨，而是由三块小骨组成，即锤骨、砧骨和镫骨。沿着盘绕的耳蜗，该结构使得能够进行高频声音检测。来自化石记录、胚胎学和发育的综合证据揭示了结构和功能转变的一个显著例子：哺乳动物祖先形成颌关节的骨骼转变为哺乳动物的微小中耳结构。我们知道，随着承载牙齿的骨骼--齿骨--尺寸的增加，颌骨关节骨变得更小，连接更松散。最后，齿骨与头骨的鳞部接触，形成真正的哺乳动物“齿鳞”（颞下颌关节）铰链。我们甚至知道，在哺乳动物进化的某个阶段，动物存在两个下颚铰链，具有双重进食和听觉功能。一个长期存在的争论点是，祖先下颌铰链的骨骼如何能够缩小尺寸，同时仍然作为一个可行的下颌关节发挥作用。另外令人困惑的是，在这个过渡期间，头骨应该是加强的，因为下颚闭合的肌肉组织重组成为一个更有效的力量产生系统。颌关节应该变得更强壮，而不是变弱和退化。也许最令人吃惊的是，这种转变发生了不止一次。20世纪70年代和80年代提出的理论模型表明，颌骨肌肉组织的重组导致哺乳动物祖先颌骨关节的负荷减少，使祖先的铰链变得更小，并在新的哺乳动物铰链接管时检测声音。这些预测对于哺乳动物的下颚和耳朵如何进化至关重要，但它们从未被验证过。这在很大程度上是因为直到最近，我们还没有办法超越理论。我们现在能够带来新的计算生物力学技术，我们作为一个团队已经开创，以解决问题的最终哺乳动物中耳和下颌关节能够进化，但仍然保持功能可行。我们已经获得了五个关键的过渡类群的CT扫描。通过对化石标本的详细研究，我们将重建整个哺乳动物起源的肌肉骨骼进化模式，特别是根据新的化石发现和逆转回祖先形式的建议。使用3D肌肉重建和多体动力学分析，我们将确定祖先，双颌关节和真正的哺乳动物颌关节在进食行为中的功能。我们将测试是否有一个从祖先到现代哺乳动物的功能转移与双颌关节的进化预测。例如，双关节的组成部分是否承受载荷，它们是否可以在没有关节分离的情况下发挥作用;以及在这种过渡期间，载荷如何从祖先转移到现代铰链。使用有限元模型，我们将测试如何在喂养过程中的颌骨铰链承受负荷和应变的骨头。我们将测试头骨是否会像预测的那样在过渡期变得更强壮，以及这与预测的咬合力之间的关系。比较解剖学家，生物力学，进化和发育生物学家，古生物学家和生物医学工程师将受益于这项工作。对英国科学的好处包括对年轻科学家的多学科培训和海外合作。这项工作的视觉方面和对哺乳动物的关注可能会吸引公众，提供参与机会和媒体兴趣。

The origin and evolution of mammals is a key event in vertebrate evolutionary history, and a textbook example of an evolutionary transition. From around 230 million years ago, the fossil record documents an uncharacteristically well-preserved sequence of transitional fossils evolving key mammalian features such as deciduous and permanent teeth, a large brain, strong skull and the unique mammalian middle ear. Rather than a single middle ear bone, mammals have a more finely tuned middle ear comprising three small bones, or ossicles, the malleus, incus and the stapes. Along with a coiled cochlea, this structure enables high frequency sound detection. Combined evidence from the fossil record, embryology and development reveal a remarkable example of transformation in structure and function: bones forming the jaw joint of mammalian ancestors transform into the minute middle ear structures of mammals. We know that as the tooth-bearing bone, the dentary, increases in size, the jaw joint bones become smaller and loosely attached. Eventually the dentary contacts the squamosal part of the skull forming a true mammalian 'dentary-squamosal' (temperomandibular) hinge. We even know that at one point in mammalian evolution, animals existed with two jaw hinges with a dual feeding and auditory function. A long-standing point of debate is how the bones of the ancestral jaw hinge were able to reduce in size, whilst at the same time still functioning as a viable jaw joint. Additionally puzzling, is that during this transition, the skull is supposed to be strengthening, as the jaw-closing musculature reorganises to become a more efficient force generating system. The jaw joint should become stronger, not weaker and degenerate. Perhaps most startling, is that this transition has happened more than once.Theoretical models proposed in the 1970s and 80s suggested that reorganization of the jaw musculature lead to reduced loading at the jaw joint in the ancestors of mammals, allowing the ancestral hinge to become smaller and detect sound whilst the new mammalian hinge took over. These predictions are central to how the mammalian jaw and ear evolved, yet they have never been tested. This is largely because we have not had the means, until recently, to go beyond theory. We are now able to bring new computational biomechanical techniques, that we as a team have pioneered, to address the question of how the definitive mammalian middle ear and jaw joint were able to evolve yet remain functionally viable. We have obtained CT scans of five key transitional taxa. Through detailed study of fossil specimens we will reconstruct the patterns of musculoskeletal evolution across the origin of mammals, particularly in light of new fossil discoveries and suggestions of reversal back to ancestral forms. Using 3D muscle reconstructions and multibody dynamics analysis, we will determine how the ancestral, dual jaw joint and true mammalian jaw joint function during feeding behaviour. We will test if there is a transfer of function from ancestral to modern mammals with the evolution of the dual jaw joint as predicted. For example, do the component parts of the dual joint bear load, and can they function without joint disarticulation; and how is load transferred from the ancestral to modern hinge during this transition. Using finite element models we will test how the bones of the jaw hinge withstand load and strains during feeding. We will test if skulls do become stronger across the transition, as predicted, and how this relates to predicted bite forces. Comparative anatomists, biomechanists, evolutionary and developmental biologists, palaeontologists and biomedical engineers will benefit from this work. Benefits to UK science include multidisciplinary training of a young scientist and overseas collaboration. The visual aspect of this work and the focus on mammals is likely to appeal to the general public, offering engagement opportunities and media interest.