Jaw myogenesis in the monk parakeet: evidence of developmental reprogramming in the emergence of novel muscles in Psittaciformes (Aves)

Abstract

Psittaciformes have apomorphies in the muscles of the jaw that include both the adductors m. ethmomandibularis (EM) and m. pseudomasseter (PM) which are equally responsible for the generation of strong bite forces. While the EM is present in all Psittaciformes, the PM can be absent or present, and even under-developed or well-developed. The aim of this study is to identify developmental reprogramming processes by comparing the myogenesis of the jaw of the monk parakeet Myiopsitta monachus with the information available about other species of Psittaciformes. Seventeen specimens including embryos at different developmental stages, and nestlings of different ages were studied through the analysis of serial histological sections. At embryonic stage 24 (S24) the muscle precursor was observed in the first pharyngeal arch. At S27 the muscle precursor was found to be divided into lateral, intermediate and medial portions. At S31 the independent development of the EM as a rostro-dorsal projection of the mm. pterygoidei could be observed. At S36 the individualization of all muscles was complete. Finally, the PM was detected two days after hatching as an aponeurotic dorsal projection of the m. adductor mandibulae externus superficialis, located lateral to the arcus jugalis. Our results suggest that in M. monachus the muscles EM and PM emerge as a result of a process of heterotipy, and variations in the degree of development of the PM are associated to a heterochronic process of post-displacement, with M. monachus having an underdeveloped PM with respect to basal Psittaciformes.