Multiple developmental origins of the avian propatagial muscle and their evolutionary implications.

Abstract

Ever since the origin of tetrapod limbs, the composition and arrangement of skeletal muscles in tetrapod limbs have been largely conserved throughout evolution. There are, however, several exceptions in which new musculoskeletal connections have been evolutionarily established. The propatagial muscle of birds represents such an example, and there is no comparable muscle in the other tetrapod lineages. Here, we investigate the detailed developmental process of forelimb muscles in the embryos of the chicken and the outgroup taxa. Based on histological and 3D morphological observations in the chicken, the propatagial muscle developed from multiple cell masses derived from parts of the developing musculus (m.) deltoideus scapularis, m. pectoralis, m. biceps brachii, and m. extensor carpi radialis, in association with the hypertrophied dermis along the cranial edge of the developing propatagium. We also performed in situ hybridization of Scx and found that there were no tendon progenitor cells along the cranial edge of the propatagium during this process. It is likely that the avian propatagial muscle evolved through recruitment of muscle progenitor cells derived from parts of the m. deltoideus scapularis, m. pectoralis, m. biceps brachii, and m. extensor carpi radialis, devoid of new interactions with tendon progenitor cells. This study will contribute to a better understanding of how novel musculoskeletal connections can arise from the highly evolutionarily conserved composition and arrangement of skeletal muscles in tetrapod limbs.