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

了解哺乳动物中耳和下颌关节在犬齿兽-哺乳类过渡过程中的功能进化

• 批准号: NE/K01496X/1
• 负责人: Emily Rayfield
• 金额: $ 48.23万
• 依托单位: University of Bristol
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2013
• 资助国家: 英国
• 起止时间: 2013 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FK01496X%2F1
• 关键词: Understanding; functional; evolution; mammalian; middle

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.

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，也是进化过渡的教科书例子。大约 2.3 亿年前，化石记录记录了一系列保存得异常完好的过渡化石，这些化石演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（或小骨）、锤骨、砧骨和镫骨组成的更精细的中耳。与螺旋式耳蜗一起，这种结构可以实现高频声音检测。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着例子：形成哺乳动物祖先下颌关节的骨骼转变为哺乳动物微小的中耳结构。我们知道，随着承载牙齿的骨（齿骨）尺寸的增大，颌关节骨变得更小并且连接松散。最终，齿骨接触头骨的鳞状部分，形成真正的哺乳动物“齿状鳞状”（颞下颌）铰链。我们甚至知道，在哺乳动物进化的某一时刻，动物存在着两个下颌铰链，具有双重进食和听觉功能。一个长期存在的争论点是，祖先下颌铰链的骨头如何能够减小尺寸，同时仍然充当可行的下颌关节。另外令人费解的是，在这个转变过程中，头骨应该会增强，因为闭合下颌的肌肉组织会重组，成为更有效的力量产生系统。颌关节应该变得更强，而不是变弱和退化。也许最令人吃惊的是，这种转变已经发生了不止一次。20世纪70年代和80年代提出的理论模型表明，下颌肌肉组织的重组导致哺乳动物祖先下颌关节的负荷减轻，从而使祖先铰链变得更小并能够检测声音，同时新的哺乳动物铰链接管。这些预测对于哺乳动物下巴和耳朵的进化至关重要，但从未经过测试。这主要是因为直到最近我们还没有办法超越理论。我们现在能够引入我们作为一个团队开创的新的计算生物力学技术，来解决最终的哺乳动物中耳和下颌关节如何能够进化并保持功能可行的问题。我们获得了五个关键过渡类群的 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祖先形式的建议。利用 3D 肌肉重建和多体动力学分析，我们将确定祖先的双颌关节和真正的哺乳动物颌关节在进食行为期间如何发挥作用。我们将测试双颌关节的进化是否如预测的那样，从祖先到现代哺乳动物的功能发生了转移。例如，双关节的各组成部分是否承受载荷，能否在关节不脱节的情况下发挥作用？以及在这个转变过程中负载如何从祖先的铰链转移到现代的铰链。我们将使用有限元模型测试颌铰链的骨骼如何承受喂食过程中的负载和应变。我们将测试头骨是否确实如预测的那样在过渡过程中变得更强，以及这与预测的咬合力有何关系。比较解剖学家、生物力学学家、进化和发育生物学家、古生物学家和生物医学工程师将从这项工作中受益。英国科学的好处包括年轻科学家的多学科培训和海外合作。这项工作的视觉效果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。

项目成果

Open data and digital morphology.

• DOI: 10.1098/rspb.2017.0194
• 发表时间: 2017-04-12
• 期刊: Proceedings. Biological sciences
• 作者: Davies TG;Rahman IA;Lautenschlager S;Cunningham JA;Asher RJ;Barrett PM;Bates KT;Bengtson S;Benson RB;Boyer DM;Braga J;Bright JA;Claessens LP;Cox PG;Dong XP;Evans AR;Falkingham PL;Friedman M;Garwood RJ;Goswami A;Hutchinson JR;Jeffery NS;Johanson Z;Lebrun R;Martínez-Pérez C;Marugán-Lobón J;O'Higgins PM;Metscher B;Orliac M;Rowe TB;Rücklin M;Sánchez-Villagra MR;Shubin NH;Smith SY;Starck JM;Stringer C;Summers AP;Sutton MD;Walsh SA;Weisbecker V;Witmer LM;Wroe S;Yin Z;Rayfield EJ;Donoghue PC
• 通讯作者: Donoghue PC

Morphological evolution of the mammalian jaw adductor complex.

• DOI: 10.1111/brv.12314
• 发表时间: 2017-11
• 期刊: Biological reviews of the Cambridge Philosophical Society
• 作者: Lautenschlager S;Gill P;Luo ZX;Fagan MJ;Rayfield EJ
• 通讯作者: Rayfield EJ

Functional reorganisation of the cranial skeleton during the cynodont-mammaliaform transition.

• DOI: 10.1038/s42003-023-04742-0
• 发表时间: 2023-04-12
• 期刊: COMMUNICATIONS BIOLOGY
• 影响因子: 5.9
• 作者: Lautenschlager, Stephan;Fagan, Michael J.;Luo, Zhe-Xi;Bird, Charlotte M.;Gill, Pamela;Rayfield, Emily J.
• 通讯作者: Rayfield, Emily J.

The diversity of Triassic South American sphenodontians: a new basal form, clevosaurs, and a revision of rhynchocephalian phylogeny

• DOI: 10.1080/14772019.2021.1976292
• 发表时间: 2021-09-20
• 期刊: JOURNAL OF SYSTEMATIC PALAEONTOLOGY
• 影响因子: 2.6
• 作者: Chambi-Trowell, Sofia A. V.;Martinelli, Agustin G.;Rayfield, Emily J.
• 通讯作者: Rayfield, Emily J.

A virtual world of paleontology

古生物学的虚拟世界

• DOI: 10.3929/ethz-b-000096966
• 发表时间: 2014
• 作者: Cunningham, John A.