Two main models have been proposed to explain how the relative size of neural structures varies through evolution. In the mosaic evolution model, individual brain structures vary in size independently of each other, whereas in the concerted evolution model developmental constraints result in different parts of the brain varying in size in a coordinated manner. Several studies have shown variation of the relative size of individual nuclei in the vertebrate brain, but it is currently not known if nuclei belonging to the same functional pathway vary independently of each other or in a concerted manner. The visual system of birds offers an ideal opportunity to specifically test which of the two models apply to an entire sensory pathway. Here, we examine the relative size of 9 different visual nuclei across 98 species of birds. This includes data on interspecific variation in the cytoarchitecture and relative size of the isthmal nuclei, which has not been previously reported. We also use a combination of statistical analyses, phylogenetically corrected principal component analysis and evolutionary rates of change on the absolute and relative size of the nine nuclei, to test if visual nuclei evolved in a concerted or mosaic manner. Our results strongly indicate a combination of mosaic and concerted evolution (in the relative size of nine nuclei) within the avian visual system. Specifically, the relative size of the isthmal nuclei and parts of the tectofugal pathway covary across species in a concerted fashion, whereas the relative volume of the other visual nuclei measured vary independently of one another, such as that predicted by the mosaic model. Our results suggest the covariation of different neural structures depends not only on the functional connectivity of each nucleus, but also on the diversity of afferents and efferents of each nucleus.
The turkey vulture (Cathartes aura) is a widespread, scavenging species in the Western Hemisphere that locates carrion by smell. Scent guided foraging is associated with an expansion of the olfactory bulbs of the brain in vertebrates, but no such neuroanatomical data exists for vultures. We provide the first measurements of turkey vulture brains, including the size of their olfactory bulbs and numbers of mitral cells, which provide the primary output of the olfactory bulbs. Comparative analyses show that the turkey vulture has olfactory bulbs that are 4× larger and contain twice as many mitral cells as those of the sympatric black vulture (Coragyps atratus), despite having brains that are 20% smaller. The turkey vulture has the largest olfactory bulbs in absolute terms and adjusted for brain size among birds, but the number of mitral cells is proportional to the size of their olfactory bulbs. The combination of large olfactory bulbs, high mitral cell counts and a greatly enlarged nasal cavity likely reflects a highly sensitive olfactory system. We suggest that this sensitive sense of smell allowed the turkey vulture to colonize biomes that are suboptimal for scavenging birds and become the most widespread vulture species in the world.
The song system of songbirds has provided significant insight into the underlying mechanisms and behavioural consequences of seasonal neuroplasticity. The extent to which seasonal changes in brain region volumes occur in non-songbird species has, however, remained largely untested. Here, we tested whether brain region volumes varied with season in the ruffed grouse (Bonasa umbellus), a gallinaceous bird that produces a unique wing-beating display known as ‘drumming' as its primary form of courtship behaviour. Using unbiased stereology, we measured the sizes of the cerebellum, nucleus rotundus, telencephalon, mesopallium, hippocampal formation, striatopallidal complex and arcopallium across spring males, fall males and fall females. The majority of these brain regions did not vary significantly across these three groups. The two exceptions were the striatopallidal complex and arcopallium, both of which were significantly larger in spring males that are actively drumming. These seasonal changes in volume strongly implicate the striatopallidal complex and arcopallium as key structures in the production and/or modulation of the ruffed grouse drumming display and represent the first evidence of seasonal plasticity in the telencephalon underlying a non-vocal courtship behaviour. Our findings also suggest that seasonal plasticity in the striatopallidal complex and arcopallium might be a trait that is shared across many bird species and that both structures are related to the production of multiple forms of courtship and not just learned song.
Although it is clear that neural structures scale with body size, the mechanisms of this relationship are not well understood. Several recent studies have shown that the relationship between neuron numbers and brain (or brain region) size are not only different across mammalian orders, but also across auditory and visual regions within the same brains. Among birds, similar cellular scaling rules have not been examined in any detail. Here, we examine the scaling of auditory structures in birds and show that the scaling rules that have been established in the mammalian auditory pathway do not necessarily apply to birds. In galliforms, neuronal densities decrease with increasing brain size, suggesting that auditory brainstem structures increase in size faster than neurons are added; smaller brains have relatively more neurons than larger brains. The cellular scaling rules that apply to auditory brainstem structures in galliforms are, therefore, different to that found in primate auditory pathway. It is likely that the factors driving this difference are associated with the anatomical specializations required for sound perception in birds, although there is a decoupling of neuron numbers in brain structures and hair cell numbers in the basilar papilla. This study provides significant insight into the allometric scaling of neural structures in birds and improves our understanding of the rules that govern neural scaling across vertebrates.
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