The Network Ontogeny of the Parrot: Altriciality, Dynamic Skeletal Assemblages, and the Avian Body Plan

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RESEARCH ARTICLE

The Network Ontogeny of the Parrot: Altriciality, Dynamic Skeletal Assemblages, and the Avian Body Plan Julieta Carril1   · Claudia P. Tambussi2 · Diego Rasskin‑Gutman3 Received: 3 August 2020 / Accepted: 8 November 2020 © Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract We analyze the connectivity patterns and fusion events among bones leading to the adult skeletal organization during the development of the superaltricial monk parakeet (Myiopsitta monachus, Psittaciformes), providing insights about the functional and evolutionary significance in the avian structural design. By using whole mount specimens stained for cartilage and bone, we apply anatomical network analysis (AnNA) to study the ontogenetic trajectory of the entire skeleton from embryonic stage 34 to adult. As bones condense, connect, and fuse to each other, we follow skeletal assemblages forming networks that change dynamically as the monk parakeet grows. Our results show that the pelvic girdle connects with the vertebral column prior to the pectoral girdle and that the pelvic girdle and hindlimbs connection begins and ends before that of the pectoral girdle and the forelimbs. We hypothesize that connections of the girdles and limbs could be linked to the altriciality of the species due to requirements for active movement in the use of the hindlimbs inside the nest, but not the need to use forelimbs to fly until much later. Further, as bones of the skull and pelvis fuse during development they form the largest and more connected assemblages, acting as attractors to connect to other bones, showing congruence between the connectivity pattern at each ontogenetic stage and the characteristic avian body plan. Keywords  Anatomical network analysis · Evo-Devo · Bauplan · Burden rank · Myiopsitta monachus · Skeletogenesis

Introduction Despite a multitude of differing ways of life, whether flying or flightless, there is a body plan that unequivocally groups all birds and segregates them from the rest of the vertebrates. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1169​2-020-09522​-w) contains supplementary material, which is available to authorized users. * Julieta Carril [email protected] 1



Laboratorio de Histología y Embriología Descriptiva, Experimental y Comparada (LHYEDEC), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

2



Centro de Investigaciones en Ciencias de La Tierra (CICTERRA), Universidad Nacional de Córdoba, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Córdoba, Argentina

3

Grupo de Investigación en Biología Teórica, Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Universidad de Valencia, Valencia, España



Major structural features that characterize the avian body plan (bauplan) are present at the skeleton level, with a reorganization of both limbs and a general simplification du