Abstract

BackgroundIn comparative neurobiology, major transitions in behavior are thought to be associated with proportional size changes in brain regions. Bird-line theropod dinosaurs underwent a drastic locomotory shift from terrestrial to volant forms, accompanied by a suite of well-documented postcranial adaptations. To elucidate the potential impact of this locomotor shift on neuroanatomy, we first tested for a correlation between loss of flight in extant birds and whether the brain morphology of these birds resembles that of their flightless, non-avian dinosaurian ancestors. We constructed virtual endocasts of the braincase for 80 individuals of non-avian and avian theropods, including 25 flying and 19 flightless species of crown group birds. The endocasts were analyzed using a three-dimensional (3-D) geometric morphometric approach to assess changes in brain shape along the dinosaur-bird transition and secondary losses of flight in crown-group birds (Aves).ResultsWhile non-avian dinosaurs and crown-group birds are clearly distinct in endocranial shape, volant and flightless birds overlap considerably in brain morphology. Phylogenetically informed analyses show that locomotory mode does not significantly account for neuroanatomical variation in crown-group birds. Linear discriminant analysis (LDA) also indicates poor predictive power of neuroanatomical shape for inferring locomotory mode. Given current sampling, Archaeopteryx, typically considered the oldest known bird, is inferred to be terrestrial based on its endocranial morphology.ConclusionThe results demonstrate that loss of flight does not correlate with an appreciable amount of neuroanatomical changes across Aves, but rather is partially constrained due to phylogenetic inertia, evident from sister taxa having similarly shaped endocasts. Although the present study does not explicitly test whether endocranial changes along the dinosaur-bird transition are due to the acquisition of powered flight, the prominent relative expansion of the cerebrum, in areas associated with flight-related cognitive capacity, suggests that the acquisition of flight may have been an important initial driver of brain shape evolution in theropods.

Highlights

  • In comparative neurobiology, major transitions in behavior are thought to be associated with proportional size changes in brain regions

  • To determine if there is a link between neuroanatomy and loss of flight, we examined the endocasts of multiple independent pairs of flightless birds and their closest volant relatives to test for modifications in brain shape

  • Principal components analyses The principal components analysis (PCA) of the Aves dataset generated 17 PC axes accounting for 95% of the symmetric component of shape variation, with the first three axes associated with 66.6% of the variation (36.4, 16.2, and 13.8%, respectively) (Additional file 1: Figure S1; overall distribution of data points resemble Coelurosaur dataset, Fig. 3)

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Summary

Introduction

Major transitions in behavior are thought to be associated with proportional size changes in brain regions. Major behavioral transitions often correlate with neuroanatomical changes because novel sensory inputs and motor control pathways can form new or more robust connections, increasing the volume and density of associated regions of the brain [1,2,3,4,5]. One such evolutionary transition, from non-volancy to powered flight, has been acquired independently by three different vertebrate groups—pterosaurs, bats, and birds [6]. Neural pathways important in creating and regulating locomotor behavior often are distributed differentially among multiple regions of the brain [5], understanding the regional shape changes has the potential to inform the evolutionary tempo and mode of fight capacity along the theropod lineage

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