Evolution of craniofacial novelty in parrots through developmental modularity and heterochrony

Authors

  • Masayoshi Tokita,

    Corresponding author
    1. Department of Zoology, Graduate School of Science, Kyoto University, Kitashirakawa-Oiwakecho, Sakyo, Kyoto 606-8502, Japan
    2. Department of Orthopaedic Surgery, University of California at San Francisco, 533 Parnassus Avenue, Suite U-470 San Francisco, CA 94143-0514, USA
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  • Takuya Kiyoshi,

    1. Department of Zoology, Graduate School of Science, Kyoto University, Kitashirakawa-Oiwakecho, Sakyo, Kyoto 606-8502, Japan
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  • Kyle N. Armstrong

    1. The Kyoto University Museum, Yoshida-Honmachi, Sakyo, Kyoto 606-8501, Japan
    2. Molhar Pty Ltd, State Agricultural Biotechnology Centre, Murdoch University, Murdoch, Western Australia 6150, Australia
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*Author for correspondence (email: tokky@zoo.zool.kyoto-u.ac.jp)

Abstract

SUMMARY Parrots (order Psittaciformes) have developed novel cranial morphology. At the same time, they show considerable morphological diversity in the cranial musculoskeletal system, which includes two novel structures: the suborbital arch and the musculus (M.) pseudomasseter. To understand comprehensively the evolutionary pattern and process of novel cranial morphology in parrots, phylogenetic and developmental studies were conducted. Firstly, we undertook phylogenetic analyses based on mitochondrial ribosomal RNA gene sequences to obtain a robust phylogeny among parrots, and secondly we surveyed the cranial morphology of parrots extensively to add new information on the character states. Character mapping onto molecular phylogenies indicated strongly the repeated evolution of both the suborbital arch and the well-developed M. pseudomasseter within parrots. These results also suggested that the direction of evolutionary change is not always identical in the two characters, implying that these characters are relatively independent or decoupled structures behaving as separate modules. Finally, we compared the developmental pattern of jaw muscles among bird species and found a difference in the timing of M. pseudomasseter differentiation between the cockatiel Nymphicus hollandicus (representative of a well-developed condition) and the peach-faced lovebird Agapornis roseicollis (representative of an underdeveloped condition). On the basis of this study, we suggest that in the development of novel traits, modularity and heterochrony facilitate the diversification of parrot cranial morphology.

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