Self-assembly of biological networks via adaptive patterning revealed by avian intradermal muscle network formation

Abstract

Networked structures integrate numerous elements into one functional unit, while providing a balance between efficiency, robustness, and flexibility. Understanding how biological networks self-assemble will provide insights into how these features arise. Here, we demonstrate how nature forms exquisite muscle networks that can repair, regenerate, and adapt to external perturbations using the feather muscle network in chicken embryos as a paradigm. The selfassembled muscle networks arise through the implementation of a few simple rules. Muscle fibers extend outward from feather buds in every direction, but only those muscle fibers able to connect to neighboring buds are eventually stabilized. After forming such a nearest-neighbor configuration, the network can be reconfigured, adapting to perturbed bud arrangement or mechanical cues. Our computational model provides a bioinspired algorithm for network self-assembly, with intrinsic or extrinsic cues necessary and sufficient to guide the formation of these regenerative networks. These robust principles may serve as a useful guide for assembling adaptive networks in other contexts. feather | skin appendage | morphogenesis | regeneration | network assembly

Transition from natal downs to juvenile feathers: conserved regulatory switches in Neoaves

“…In addition to ECM and the WNT/β-catenin related pathways, many other known molecular mechanisms were also enriched. In both early embryonic and juvenile skin development (levels 1 to 5), muscle formation genes were enriched, consistent with the previous finding that muscle development is important for feather positioning (Supplementary Tables 3 and 4) 38 . In late juvenile skin development (levels 6 to 11), planar cell polarity (PCP) signaling pathway genes were enriched.…”

Cell shape anisotropy contributes to self-organized feather pattern fidelity in birds

“…Second, because the loss of cell shape anisotropy in penguin explants is coupled to the shrinking of the skin ( S12 Fig ), we designed a mechanical test to externally influence cell elongation. To do so, we cultured competent dorsal skin portions on gels of collagen to which we applied controlled directional stretch prior to primordia emergence as in [ 37 ] (see Materials and methods ). Approximately 8 h after applying to Japanese quail explants a stretch orthogonal to the normal axis of pattern formation (i.e., a dorso-ventral stretch; Fig 6A and 6B ), anisotropy amplitude decreased compared to non-stretched control explants, and cells reoriented along the dorso-ventral axis ( Fig 6C ).…”

“…Higher values of cell Fig 6 . Stretch-induced dermal cell anisotropy modifies explant pattern fidelity. (A) Japanese quail skin explants at competence stage (in orange) were placed on collagen gels (in white) on Petri dishes (in gray) and stretched along the dorso-ventral axis by pulling on Velcro bands (in yellow) attached to the gels as in [37] (and see Materials and methods). They were cultured during 8 h (to assess cell shape anisotropy).…”

“…African penguin and emu explants were cultured on insert membranes during 96 h (i.e., to differentiation stage; n = 6 and 4, respectively, for both control and drug-treated explants). For stretching experiments, skin explants were cultured on 80% collagen gels (Corning) previously poured on Velcro bands as in [ 37 ]. Stretch was exerted manually by pulling on Velcro bands parallelly or orthogonally to the axis of the explant and fixing Velcro bands to the Petri dish using dissection pins (see Fig 5A ).…”