The evolution of terrestrial locomotor performance in early tetrapod vertebrates

早期四足脊椎动物陆地运动性能的进化

• 批准号: NE/K004751/1
• 负责人: John Hutchinson
• 金额: $ 53.57万
• 依托单位: Royal Veterinary College
• 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%2FK004751%2F1
• 关键词: evolution; terrestrial; locomotor; performance; early

Tetrapods, or bony animals with limbs instead of fins, evolved the ability to support their body weight and move on land sometime in the Middle to Late Devonian period - around 350-400 million years ago. However, the ability to stand on all four legs seems to have evolved after the appearance of fully developed limbs with digits and other skeletal features which are now thought to have arisen in aquatic animals. Our prior NERC-funded work focused on the locomotor behaviours of two key Devonian animals, Ichthyostega and Acanthostega, to reconstruct how early tetrapods transitioned from swimming in water to walking on land. Through the use of 3D modelling and simple static biomechanics, we found these evolutionary pioneers had limited capacity to move their limbs in certain directions which hindered their ability to walk like a modern land animal. This raises the question: when and how did modern walking styles evolve? Furthermore, were all tetrapods similarly sedate or could some forms move more quickly than others? The technology and biological understanding now exists to answer such fundamental evolutionary questions. To answer them, we need to determine what kinds of forces and speeds that different tetrapods could generate.We aim to reconstruct dynamic motions in a series of early tetrapods bracketing the water-to-land transition using the latest computer simulation techniques. These animals include the mainly aquatic Ichthyostega and Acanthostega and two more recent Carboniferous forms that seem to have been more terrestrial, Pederpes and Proterogyrinus. To validate the simulation technique, cutting-edge 3D experimental data will be collected on walking/trotting modern salamanders for the first time. We will also measure how land-adapted salamanders change their speed capacity as they grow, which by analogy should give insights into the evolutionary progression of walking capabilities in progressively more terrestrially adapted early tetrapods. These experimental studies will test (1) how important the limbs and backbone are in supporting movements on land and (2) whether maximal speed capacity is constant or changes during growth.The experimental data from salamanders will be fed into a computer model in which a novel, high-fidelity dynamic simulation of how muscles drive locomotion will be created. In addition, whole body 3D models of the early tetrapods will be constructed with simplified, abstract representations of the major limb/backbone muscles. The salamander data will then be used as a template to simulate locomotion in the extinct animals; how each species of tetrapod moved and how quickly they could do it will be estimated. Locomotor abilities of each animal will then be compared to determine the sequence of evolutionary events that ultimately gave rise to walking capabilities, made possible because each species is successively more closely related to living tetrapods. The evolutionary changes will also be compared to the walking aptitude of growing salamanders to see if the two are mutually informative -- i.e. broadly speaking, does 'ontogeny recapitulate phylogeny' in tetrapod locomotion?This project will uncover how evolutionary changes in anatomy impacted the ways in which early tetrapods could move, ultimately illuminating how vertebrates eventually conquered the terrestrial realm. It is curiosity-driven science that aims to tackle one of the most awe-inspiring and pivotal evolutionary events in Earth's history. As such, it will engender a great deal of public interest (as demonstrated by our previous NERC grant), which we will vigorously capitalize upon by creating interactive public/scientific fora to communicate and disseminate our research. Further, it will advance the field of evolutionary biomechanics by creating a novel simulation approach, firmly grounded in empirical data, which will be distributed to scientists studying locomotion in living and extinct organisms.

四足动物，或者说有四肢而不是鳍的多骨动物，在泥盆纪中期到晚期的某个时候进化出了支撑体重和在陆地上移动的能力-大约3.5亿到4亿年前。然而，用四条腿站立的能力似乎是在完全发育的四肢出现后进化而来的，这些四肢有手指和其他骨骼特征，现在被认为是在水生动物中出现的。我们之前的NERC资助的工作集中在两个关键的泥盆纪动物的运动行为，鱼石螈和螈，重建早期四足动物如何从水中游泳过渡到陆地上行走。通过使用3D建模和简单的静态生物力学，我们发现这些进化先驱在某些方向上移动四肢的能力有限，这阻碍了他们像现代陆地动物一样行走的能力。这就提出了一个问题：现代步行方式是何时以及如何演变的？此外，所有的四足动物都是一样的稳重吗？或者是某些形式比其他形式移动得更快吗？现在的技术和生物学知识可以回答这些基本的进化问题。为了回答这些问题，我们需要确定不同的四足动物可以产生什么样的力和速度。我们的目标是使用最新的计算机模拟技术来重建一系列早期四足动物的动态运动，包括水到陆地的过渡。这些动物包括主要是水生的鱼石螈属（英语：Ichthyostega）和螈属（英语：Atomostega），以及石炭纪的两种更接近陆地的动物，Pederpes和Proterogyrinus。为了验证模拟技术，将首次收集现代蝾螈行走/小跑的尖端3D实验数据。我们还将测量陆地适应的蝾螈如何随着它们的生长而改变它们的速度能力，通过类比，应该可以深入了解逐渐适应陆地的早期四足动物的步行能力的进化过程。这些实验研究将测试（1）四肢和脊椎在支持陆地运动中的重要性，以及（2）最大速度能力是恒定的还是在生长过程中发生变化。来自蝾螈的实验数据将被输入计算机模型，在该模型中将创建一个新的高保真动态模拟肌肉如何驱动运动。此外，早期四足动物的全身3D模型将使用主要肢体/脊柱肌肉的简化，抽象表示来构建。蝾螈的数据将被用作模板来模拟灭绝动物的运动;每种四足动物如何移动以及它们移动的速度将被估计。然后将比较每种动物的运动能力，以确定最终产生行走能力的进化事件的顺序，这是因为每个物种都与现存的四足动物有着更密切的关系。进化的变化也将与生长中的蝾螈的行走能力进行比较，看看这两者是否相互提供信息--也就是说，在四足动物的运动中，“个体发育重演了个体发育”？该项目将揭示解剖学的进化变化如何影响早期四足动物的移动方式，最终阐明脊椎动物最终如何征服陆地。这是好奇心驱动的科学，旨在解决地球历史上最令人敬畏和关键的进化事件之一。因此，它将产生大量的公共利益（正如我们以前的NERC赠款所证明的那样），我们将通过创建互动的公共/科学论坛来交流和传播我们的研究来大力利用这些利益。此外，它将通过创建一种新的模拟方法来推进进化生物力学领域，该方法牢固地建立在经验数据的基础上，将分发给研究活的和灭绝的生物体运动的科学家。

项目成果

Low effective mechanical advantage of giraffes' limbs during walking reveals trade-off between limb length and locomotor performance

长颈鹿四肢在行走过程中的低有效机械优势揭示了四肢长度和运动性能之间的权衡

• DOI: 10.1101/2021.04.29.441773
• 发表时间: 2021
• 作者: Basu C

The extinct, giant giraffid Sivatherium giganteum: skeletal reconstruction and body mass estimation.

• DOI: 10.1098/rsbl.2015.0940
• 发表时间: 2016-01
• 期刊: Biology letters
• 影响因子: 3.3
• 作者: Basu C;Falkingham PL;Hutchinson JR
• 通讯作者: Hutchinson JR

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

Low effective mechanical advantage of giraffes' limbs during walking reveals trade-off between limb length and locomotor performance.

• DOI: 10.1073/pnas.2108471119
• 发表时间: 2022-07-12
• 期刊: Proceedings of the National Academy of Sciences of the United States of America
• 影响因子: 11.1

Temporal and phylogenetic evolution of the sauropod dinosaur body plan.

• DOI: 10.1098/rsos.150636
• 发表时间: 2016-03
• 期刊: Royal Society open science
• 影响因子: 3.5
• 作者: Bates KT;Mannion PD;Falkingham PL;Brusatte SL;Hutchinson JR;Otero A;Sellers WI;Sullivan C;Stevens KA;Allen V
• 通讯作者: Allen V