Avian cranial evolution is influenced by trade-offs in shape between hard and soft tissue traits

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Abstract
Changes in the structure and relative size of the brain are thought to be key transformations in the origins and continued evolution of birds, reflecting innovations and diversity of neurosensory and cognitive capabilities. However, these neuro-anatomical and functional changes do not occur in isolation, being accompanied by a host of other derived morphological characteristics associated with the evolution of flight. In the avian head alone, these include the evolution of a toothless beak, increase in relative eye size, and reduction and restructuring of jaw muscles. Several hypothesized developmental trade-offs have been proposed to explain the interrelationships among the hard and soft tissues of the head. How these developmental patterns translate into evolutionary trade-offs in other cranial traits is poorly understood, despite brain shape evolution being well documented in birds. Here, we use two-block partial least squares analyses and Ornstein-Uhlenbeck models of adaptive trait evolution to explore the phenotypic evolution of hard and soft cranial tissues and test hypotheses of correlated trait evolution. In pairwise analyses we found that all traits (endocast shape, neurocranium shape, rostrum shape, jaw muscle shape and residual orbit diameter) are significantly correlated. We found strongest support for a modular hypothesis of trait evolution across the whole head, with the rostrum and jaw muscles forming one module and brain, neurocranium, and eye forming the other. Within modules, traits are tightly integrated, but integration is relaxed between modules, allowing them to develop and evolve with a degree of independence. Together, these results highlight the integrated nature of the avian head and reveal that rather than being driven overwhelmingly by selection on a single trait, the shape of the avian head is a result of multiple interactions among hard and soft tissue traits.

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