Abstract
Ecomorphological studies evaluating the impact of environmental and biological factors on the brain have so far focused on morphology or size measurements, and the ecological relevance of potential multi-level variations in brain architecture remains unclear in vertebrates. Here, we exploit the extraordinary ecomorphological diversity of squamates to assess brain phenotypic diversification with respect to locomotor specialization, by integrating single-cell distribution and transcriptomic data along with geometric morphometric, phylogenetic, and volumetric analysis of high-definition 3D models. We reveal significant changes in cerebellar shape and size as well as alternative spatial layouts of cortical neurons and dynamic gene expression that all correlate with locomotor behaviours. These findings show that locomotor mode is a strong predictor of cerebellar structure and pattern, suggesting that major behavioural transitions in squamates are evolutionarily correlated with mosaic brain changes. Furthermore, our study amplifies the concept of ‘cerebrotype’, initially proposed for vertebrate brain proportions, towards additional shape characters.
Highlights
Ecomorphological studies evaluating the impact of environmental and biological factors on the brain have so far focused on morphology or size measurements, and the ecological relevance of potential multi-level variations in brain architecture remains unclear in vertebrates
To explore potential relationships between brain morphology and locomotor specializations, we used high-definition 3D reconstructions of wholebrains and isolated cerebella based on contrast-enhanced computed tomography (CT) and manual segmentation, using a representative panel of 40 lizard and snake species with different locomotor modes (Fig. 1 and Supplementary Table 1)
Along with significant changes in cerebellar shape and size across squamate species, our study indicates a peculiar heterogeneity in cortical neuron spatial distribution and gene expression pattern, which are all intimately associated with locomotor specialization
Summary
Ecomorphological studies evaluating the impact of environmental and biological factors on the brain have so far focused on morphology or size measurements, and the ecological relevance of potential multi-level variations in brain architecture remains unclear in vertebrates. We hypothesise that locomotor behaviour could be a strong predictor of cerebellar complexity at different levels of organisation, including volume, shape, neuron spatial arrangement, and gene expression pattern To test this hypothesis, we use squamate reptiles—lizards and snakes—as the main model system because of their high levels of morphological diversity, including in the size as well as general anatomical and cellular organisation of the cerebellum[15,36,37,38,39]. Along with changes in cerebellar shape and size, we show heterogeneity in Purkinje cell spatial distribution and dynamic gene expression pattern, which are all associated with locomotor specialization These data indicate that locomotor pattern is a strong predictor of cerebellar architecture, and highlight the importance of mosaic brain evolution in generating brain patterns shared by groups of squamate species with behavioural similarities
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