Cells with contractile functions are present in almost all metazoans, and so are the related processes of muscle homeostasis and regeneration. Regeneration itself is a complex process unevenly spread across metazoans that ranges from full-body regeneration to partial reconstruction of damaged organs or body tissues, including muscles. The cellular and molecular mechanisms involved in regenerative processes can be homologous, co-opted, and/or evolved independently. By comparing the mechanisms of muscle homeostasis and regeneration throughout the diversity of animal body-plans and life cycles, it is possible to identify conserved and divergent cellular and molecular mechanisms underlying muscle plasticity. In this review we aim at providing an overview of muscle regeneration studies in metazoans, highlighting the major regenerative strategies and molecular pathways involved. By gathering these findings, we wish to advocate a comparative and evolutionary approach to prompt a wider use of “non-canonical” animal models for molecular and even pharmacological studies in the field of muscle regeneration.

The octopus arm is a ‘one of a kind’ muscular hydrostat, as demonstrated by its high maneuverability and complexity of motions. It is composed of a complex array of muscles and intramuscular connective tissue, allowing force and shape production. In this study, we investigated the organization of the intramuscular elastic fibers in two main muscles composing the arm bulk: the longitudinal (L) and the transverse (T) muscles. We assessed their contribution to the muscles’ passive elasticity and stiffness and inferred their possible roles in limb deformation. First, we performed confocal imaging of whole-arm samples and provided evidence of a muscle-specific organization of elastic fibers (more chaotic and less coiled in T than in L). We next showed that in an arm at rest, L muscles are maintained under 20% compression and T muscles under 30% stretching. Hence, tensional stresses are inherently present in the arm and affect the strain of elastic fibers. Because connective tissue in muscles is used to transmit stress and store elastic energy, we investigated the contribution of elastic fibers to passive forces using step-stretch and sinusoidal length-change protocols. We observed a higher viscoelasticity of L and a higher stiffness of T muscles, in line with their elastic fiber configurations. This suggests that L might be involved in energy storage and damping, whereas T is involved in posture maintenance and resistance to deformation. The elastic fiber configuration thus supports the specific role of muscles during movement and may contribute to the mechanics, energetics and control of arm motion.