Developmental Modes and Developmental Mechanisms can Channel Brain Evolution - PubMed (original) (raw)

Developmental Modes and Developmental Mechanisms can Channel Brain Evolution

Christine J Charvet et al. Front Neuroanat. 2011.

Abstract

Anseriform birds (ducks and geese) as well as parrots and songbirds have evolved a disproportionately enlarged telencephalon compared with many other birds. However, parrots and songbirds differ from anseriform birds in their mode of development. Whereas ducks and geese are precocial (e.g., hatchlings feed on their own), parrots and songbirds are altricial (e.g., hatchlings are fed by their parents). We here consider how developmental modes may limit and facilitate specific changes in the mechanisms of brain development. We suggest that altriciality facilitates the evolution of telencephalic expansion by delaying telencephalic neurogenesis. We further hypothesize that delays in telencephalic neurogenesis generate delays in telencephalic maturation, which in turn foster neural adaptations that facilitate learning. Specifically, we propose that delaying telencephalic neurogenesis was a prerequisite for the evolution of neural circuits that allow parrots and songbirds to produce learned vocalizations. Overall, we argue that developmental modes have influenced how some lineages of birds increased the size of their telencephalon and that this, in turn, has influenced subsequent changes in brain circuits and behavior.

Keywords: bird; development; evolution; mode; proliferation.

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Figures

Figure 1

Figure 1

A plot of telencephalon volume versus overall brain volume shows that the telencephalon is disproportionately large in parrots, songbirds (i. e., oscine passerines), and anseriform birds (ducks and geese) compared with galliform birds and diverse other avian species. The other avian species in this graph include mainly pigeons, shorebirds and falcons. Data are from Iwaniuk and Hurd (2005).

Figure 2

Figure 2

Phylogeny of archosaurs (alligators and birds) shows their modes of development. Parrots, songbirds, suboscines (manakins, antbirds, tyrant-flycatchers), and kingfishers are altricial, whereas falcons and owls are semi-altricial. Because most land birds (e.g., suboscines and falcons) are either altricial or semi-altricial, the ancestors of parrots and songbirds were probably either altricial or semi-altricial. This, in turn, implies that the expansion of the telencephalon in parrots and songbirds evolved in a lineage that was at least semi-altricial. In contrast, many reptiles (e.g., alligators), paleognaths (e.g., emus), and basal lineages of Neoaves (e.g., galliform and anseriform birds) are precocial. Thus, ducks and geese were probably precocial when they expanded their telencephalon. The phylogeny is based on Hackett et al. (2008).

Figure 3

Figure 3

Comparative analysis of avian post-hatching brain growth is measured by the ratio of adult to hatchling brain weight. Altricial species with proportionally small telencephalons (e.g., swifts and pigeons) exhibit more post-hatching brain growth than precocial species (e.g., anseriform and galliform birds). Parrots and songbirds (i.e., oscine passerines) exhibit even more post-hatching brain growth than many other altricial species. Among songbirds, corvids (carrion crows, magpies) exhibit some of the largest post-hatching brain growth. Because the telencephalon is born late in development, post-hatching brain growth is due primarily to the expansion of the telencephalon (see Striedter and Charvet, ; Charvet and Striedter, 2009a). Data are from Portmann (1947b).

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