Biodiversity and Biocomplexity Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Japan.
Department of Ecology and Evolution, University of California-Los Angeles, Los Angeles, California, United States of America.
PLoS Biol. 2021 Mar 2;19(3):e3001031. doi: 10.1371/journal.pbio.3001031. eCollection 2021 Mar.
Evolutionary innovations underlie the rise of diversity and complexity-the 2 long-term trends in the history of life. How does natural selection redesign multiple interacting parts to achieve a new emergent function? We investigated the evolution of a biomechanical innovation, the latch-spring mechanism of trap-jaw ants, to address 2 outstanding evolutionary problems: how form and function change in a system during the evolution of new complex traits, and whether such innovations and the diversity they beget are repeatable in time and space. Using a new phylogenetic reconstruction of 470 species, and X-ray microtomography and high-speed videography of representative taxa, we found the trap-jaw mechanism evolved independently 7 to 10 times in a single ant genus (Strumigenys), resulting in the repeated evolution of diverse forms on different continents. The trap mechanism facilitates a 6 to 7 order of magnitude greater mandible acceleration relative to simpler ancestors, currently the fastest recorded acceleration of a resettable animal movement. We found that most morphological diversification occurred after evolution of latch-spring mechanisms, which evolved via minor realignments of mouthpart structures. This finding, whereby incremental changes in form lead to a change of function, followed by large morphological reorganization around the new function, provides a model for understanding the evolution of complex biomechanical traits, as well as insights into why such innovations often happen repeatedly.
进化创新是生物多样性和复杂性兴起的基础,这是生命历史的两个长期趋势。自然选择如何重新设计多个相互作用的部分以实现新的涌现功能?我们研究了一种生物力学创新的进化,即捕食性蚂蚁的卡锁弹簧机制,以解决两个突出的进化问题:在新的复杂特征的进化过程中,系统的形态和功能如何发生变化,以及这种创新及其产生的多样性是否可以在时间和空间上重复。利用对 470 种物种的新系统发育重建,以及对代表性分类群的 X 射线微断层扫描和高速摄像,我们发现卡锁弹簧机制在一个单一的蚂蚁属(Strumigenys)中独立进化了 7 到 10 次,导致不同大陆上不同形式的多样性重复进化。该捕捉机制使颚部加速度相对于较简单的祖先增加了 6 到 7 个数量级,目前是可重置动物运动中记录到的最快加速度。我们发现,大多数形态多样化发生在卡锁弹簧机制进化之后,而卡锁弹簧机制的进化是通过口器结构的微小调整实现的。这一发现表明,形态上的微小变化会导致功能的改变,然后围绕新功能进行大规模的形态重组,为理解复杂生物力学特征的进化提供了一个模型,也为为什么这种创新经常反复发生提供了一些见解。