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

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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.

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Data Availability

Materials used in this work are available in the collection of the institute where the work has been carried out (LHYEDEC, FCV, UNLP, Argentina). All the data obtained is included in this submission.

Code Availability

Software, package and codes used in this work are freely available.

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Acknowledgements

Helpful comments made by the Editor, Olivia Plateau and a second anonymous Reviewer greatly improved the manuscript. Thanks to Dr. Federico J. Degrange and Dr. Juan José Rustán for the help in collecting samples. This research was supported by Grant PICT 2017-1899 from FONCyT-ANPCyT to JC. DR-G was funded by Grant BFU2015-70927-R. We are grateful to CONICET for permanent support.

Funding

JC was funded by Grant: PICT 2017-1899, FONCyT, ANPCyT, Argentina. DR-G was funded by Grant: BFU2015-70927-R, España.

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Authors and Affiliations

  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

    Julieta Carril

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

    Claudia P. Tambussi

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

    Diego Rasskin-Gutman

Authors
  1. Julieta Carril
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  2. Claudia P. Tambussi
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  3. Diego Rasskin-Gutman
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Contributions

JC: study conception and design-equal, material preparation and data collection-lead, writing original draft-equal, writing-review & editing-equal. CPT: study conception and design-equal, writing original draft-equal, writing-review & editing-equal. DR-G: study conception and design-supporting, formal data analysis-lead, writing-review & editing-equal.

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Correspondence to Julieta Carril.

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The authors declare that the materials used were obtained complying with the current laws of the country in which they were performed (Argentina).

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Electronic supplementary material

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Supplementary Material 1

Matrixes of the skeleton and throughout the ontogenetic trajectory of Myiopsitta monachus, from embryonic stage 34 to adult, where 1 indicates presence and 0 indicates absence of connection. For references see abbreviations of each node in Table 1. The connectivity value (ki) of each node is shown (in bold) in the last column of each matrix. (XLS 2348 kb)

Supplementary Material 2

Detail of anatomical networks of the skeleton of Myiopsitta monachus throughout development (from embryological stage 34 to adult). For references see abbreviations of each node in Table 1. (PDF 2921 kb)

Electronic supplementary material 3 (DOC 48 kb)

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Carril, J., Tambussi, C.P. & Rasskin-Gutman, D. The Network Ontogeny of the Parrot: Altriciality, Dynamic Skeletal Assemblages, and the Avian Body Plan. Evol Biol 48, 41–53 (2021). https://doi.org/10.1007/s11692-020-09522-w

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