Metamorphosis in Insect Muscle: Insights for Engineering Muscle-Based Actuators.

One of the major limitations to advancing the development of soft robots is the absence of lightweight, effective soft actuators. While synthetic systems, such as pneumatics and shape memory alloys, have created important breakthroughs in soft actuation, they typically rely on large external power sources and some rigid components. Muscles provide an ideal actuator for soft constructs, as they are lightweight, deformable, biodegradable, silent, and powered by energy-dense hydrocarbons such as glucose. Vertebrate cell lines and embryonic cultures have allowed critical foundational work to this end, but progress there is limited by the difficulty of identifying individual pathways in embryonic development, and the divergence of immortal cell lines from these normal developmental programs. An alternative to culturing muscles from embryonic cells is to exploit the advantages of species with metamorphic stages. In these animals, muscles develop from a predefined pool of myoblasts with well-characterized contacts to other tissues. In addition, the endocrine triggers for development into adult muscles are often known and tractable for experimental manipulation. This is particularly true for metamorphic muscle development in holometabolous insects, which provide exciting new avenues for tissue engineering. Using insect tissues for actuator development confers additional benefits; insect muscles are more robust to varying pH, temperature, and oxygenation than are vertebrate cells. Given that biohybrid robots are likely to be used in ambient conditions and changing environments, this sort of hardiness is likely to be required for practical use. In this study, we summarize key processes and signals in metamorphic muscle development, drawing attention to those pathways that offer entry points for manipulation. By focusing on lessons learned from insect development, we propose that future culture designs will be able to use more systematic, hypothesis-driven approaches to optimizing engineered muscle. Impact statement This review summarizes our current understanding of metamorphic muscle development in insects. It provides a framework for engineering muscle-based actuators that can be used in robotic applications in a wide range of ambient conditions. The focus is on identifying key processes that might be manipulated to solve current challenges in controlling tissue development such as myoblast proliferation, myotube formation and fusion, cytoskeletal alignment, myotendinous attachment and full differentiation. An important goal is to gather findings that cross disciplinary boundaries and to promote the development of better bioactuators for nonclinical applications.