Evolutionary origins of the avian brain

Journal name:
Nature
Volume:
501,
Pages:
93–96
Date published:
DOI:
doi:10.1038/nature12424
Received
Accepted
Published online

Features that were once considered exclusive to modern birds, such as feathers and a furcula, are now known to have first appeared in non-avian dinosaurs1. However, relatively little is known of the early evolutionary history of the hyperinflated brain that distinguishes birds from other living reptiles and provides the important neurological capablities required by flight2. Here we use high-resolution computed tomography to estimate and compare cranial volumes of extant birds, the early avialan Archaeopteryx lithographica, and a number of non-avian maniraptoran dinosaurs that are phylogenetically close to the origins of both Avialae and avian flight. Previous work established that avian cerebral expansion began early in theropod history and that the cranial cavity of Archaeopteryx was volumetrically intermediate between these early forms and modern birds3, 4. Our new data indicate that the relative size of the cranial cavity of Archaeopteryx is reflective of a more generalized maniraptoran volumetric signature and in several instances is actually smaller than that of other non-avian dinosaurs. Thus, bird-like encephalization indices evolved multiple times, supporting the conclusion that if Archaeopteryx had the neurological capabilities required of flight, so did at least some other non-avian maniraptorans. This is congruent with recent findings that avialans were not unique among maniraptorans in their ability to fly in some form5, 6.

At a glance

Figures

  1. Coelurosaur phylogeny and partitioned endocranial casts.
    Figure 1: Coelurosaur phylogeny and partitioned endocranial casts.

    ae, Endocasts of Citipati osmolskae (IGM 100/978) (a), unnamed troodontid (IGM 100/1126) (b), Archaeopteryx lithographica (BMNH 37001) (c), Struthio camelus (ostrich) (d), and Melanerpes aurifrons (woodpecker) (e) divided into neuroanatomical partitions based on homologous osteological landmarks using computed tomography data. Partitions roughly correlate to the olfactory bulbs (orange), cerebrum (green), optic lobes (pink), cerebellum (blue) and brain stem (yellow). Endocasts are not scaled to size. f, Sagittally sectioned skull of Phaethon rubricauda with osteological landmarks highlighted to correspond to the regions shown in the endocasts. g, Phylogeny of included taxa. Proposed episodes of encephalization are indicated by changes in colour. Phylogeny adapted from ref. 30.

  2. Bivariate plots of log-transformed body-mass data.
    Figure 2: Bivariate plots of log-transformed body-mass data.

    a, b, Body mass (kg) plotted against total endocranial volume (cm3) (a) and cerebral volume (b). Crown birds display apomorphically high endocranial and cerebral volumes with respect to body size. Colours indicate crown birds (blue), non-maniraptoran theropods (white), Shuvuuia deserti (purple), oviraptorosaurs (red), deinonychosaurs (yellow), Archaeopteryx lithographica (green). Reduced major-axis regression line for entire sample (solid line), crown birds (large dashes), and non-avian theropods (small dashes). Regression statistics given in Supplementary Table 3.

  3. Bivariate plots of log-transformed total-endocranial-volume data.
    Figure 3: Bivariate plots of log-transformed total-endocranial-volume data.

    a, b, Total endocranial volume (cm3) plotted against cerebral (a) and cerebellar (b) volumes. Colours are the same as in Fig. 2. Highlighting on the tree indicates those groups that share crown-like volumes. These can be interpreted as being either homologous (synapomorphic for a more inclusive group including crown birds) or convergent (appears in crown birds and more distantly related groups). Regression statistics are given in Supplementary Table 4.

  4. Principal components analysis plot of neuroanatomical region volumes.
    Figure 4: Principal components analysis plot of neuroanatomical region volumes.

    Colours are the same as in Fig. 2. Complete volumetric isolation is indicated for Oviraptorosauria. A paravian (see Fig. 1) group is recovered in the principal components analysis (PCA) plot, but not an avialan (Archaeopteryx plus crown birds) volumetric grouping. PCA loadings are provided in Supplementary Table 5.

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Affiliations

  1. American Museum of Natural History, Division of Paleontology, New York, New York 10024, USA

    • Amy M. Balanoff,
    • Gabe S. Bever &
    • Mark A. Norell
  2. Columbia University, Department of Earth and Environmental Sciences, New York, New York 10027, USA

    • Amy M. Balanoff
  3. New York Institute of Technology, College of Osteopathic Medicine, Old Westbury, New York 11568, USA

    • Gabe S. Bever
  4. Jackson School of Geosciences, The University of Texas at Austin, Austin, Texas 78712, USA

    • Timothy B. Rowe
  5. Present address: Department of Anatomical Sciences, Stony Brook University School of Medicine, Stony Brook, New York 11794, USA.

    • Amy M. Balanoff

Contributions

A.M.B., G.S.B. and M.A.N. designed the study. A.M.B. wrote the paper, performed data entry and analytical work, and prepared figures. G.S.B. assisted in data interpretation and helped to write the paper. T.B.R. contributed computed tomography data and assisted in data interpretation. M.A.N. provided computed tomography data and assisted in writing the paper.

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The authors declare no competing financial interests.

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Supplementary information

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  1. Supplementary Information (2.5 MB)

    This file contains Supplementary Figures 1- 3, Supplementary Tables 1 -5 and Supplementary References.

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