Anatomical networks reveal the musculoskeletal modularity of the human head

Abstract

Mosaic evolution is a key mechanism that promotes robustness and evolvability in living beings. For the human head, to have a modular organization would imply that each phenotypic module could grow and function semi-independently. Delimiting the boundaries of head modules, and even assessing their existence, is essential to understand human evolution. Here we provide the first study of the human head using anatomical network analysis (AnNA), offering the most complete overview of the modularity of the head to date. Our analysis integrates the many biological dependences that tie hard and soft tissues together, arising as a consequence of development, growth, stresses and loads, and motion. We created an anatomical network model of the human head, where nodes represent anatomical units and links represent their physical articulations. The analysis of the human head network uncovers the presence of 10 musculoskeletal modules, deep-rooted in these biological dependences, of developmental and evolutionary significance. In sum, this study uncovers new anatomical and functional modules of the human head using a novel quantitative method that enables a more comprehensive understanding of the evolutionary anatomy of our lineage, including the evolution of facial expression and facial asymmetry.

Figure 1. Modules of the human head identified using AnNA.

In red, the lower jaw/inner ear complex; in blue, the mid/upper face complex; in green, the laryngeal complex; in yellow, the neck complex; in orange and purple, the oral/ocular complexes; in light and dark grey, the superficial ear complexes; and in light and dark pink, the inner ear complexes. Strength of modularity (Q-value) 0.5921. See labels in Methods. This figure was drawn by Christopher Smith.

Figure 2. Modules of the head skeleton identified using AnNA.

In red, the cranial complex; in blue, the facial complex; in green, the thyroid complex; in yellow, the thoracic complex; in cyan, the cervical complex; in light and dark purple, the ossicles complexes; and in orange, the hyoid one-bone module. Strength of modularity (Q-value) 0.4977. See labels in Methods. This figure was drawn by Christopher Smith.

Figure 3. Modules of the head musculature identified using AnNA.

In yellow, the ocular/upper face complex; in light and dark blue, the orofacial complexes; and in grey, the 21 smaller blocks of inter-connected muscles. In the absence of bones, most muscles are totally disconnected from the three major muscle modules (in white). Strength of modularity (Q-value) 0.8323. See labels in Methods. This figure was drawn by Christopher Smith.