Developmental origins of mosaic brain evolution: Morphometric analysis of the developing zebra finch brain

Abstract

In adult zebra finches (Taeniopygia guttata), the telencephalon occupies 64% of the entire brain. This fraction is similar to what is seen in parrots, but many other birds possess a significantly smaller telencephalon. The aim of the present study was to determine the developmental time course and cellular basis of telencephalic enlargement in zebra finches, and then to compare these findings with what is known about telencephalic enlargement in other birds. To this end we estimated the volumes of all major brain regions from serial sections in embryonic and post-hatching zebra finches. We also labeled proliferating cells with antibodies against proliferating cell nuclear antigen and phosphorylated histone H3. An important finding to emerge from this work is that the telencephalon of zebra finches at hatching contains a thick proliferative subventricular zone (SVZ) that extends from the subpallium into the dorsal pallium. The data also show that the onset and offset of telencephalic neurogenesis are both delayed in zebra finches relative to quail (Galliformes). This delay in neurogenesis, in conjunction with the expanded SVZ, probably accounts for most of the telencephalic enlargement in passerines such as the zebra finch. In addition, passerines enlarged their telencephalon by decreasing the proportional size of their midbrain tectum. Because the presumptive tectum is proportionally smaller in zebra finches than quail before neurogenesis begins, this difference in tectum size cannot be due to evolutionary alterations in neurogenesis timing. Collectively these findings indicate that several different developmental mechanisms underlie the evolution of a large telencephalon in passerines.

Expansion, folding, and abnormal lamination of the chick optic tectum after intraventricular injections of FGF2

“…To test this hypothesis, we computed the fraction of all tectal cells that is proliferative, rather than postproliferative. We have previously used this proliferative zone fraction (PZF) measure to demonstrate species differences in neurogenesis timing (7,9). Here we extend the approach by staining ED7 brains with proliferating cell nuclear antigen (PCNA), a relatively specific marker for proliferating cells (21) (Fig.…”

“…Specifically, we reasoned that FGF2 injections into ventricles of embryonic chicks should, by analogy to the work in mammals (14), increase telencephalon volume, effectively creating chickens with a telencephalon as large as that of parrots and songbirds (7,9). However, our FGF2 injections did not significantly alter telencephalon development.…”

“…Recent work in evolutionary developmental neurobiology has shown that these evolutionary increases in brain region volumes are often caused by delays in cell cycle exit of neuronal precursors (5,6). Among birds, for example, parrots and songbirds exhibit delayed telencephalic neurogenesis relative to chicken-like birds (7)(8)(9). Among mammals, cell cycle exit in the neocortex is similarly delayed in primates, which have a disproportionately enlarged neocortex (5,(10)(11)(12).…”

Asymmetry of different brain structures in homing pigeons with and without navigational experience

“…If the brain composition of homing pigeons is represented by the 'developmental constraints theory' (Finlay and Darlington, 1995), we had to expect that changes in the size of one brain structure would be correlated with changes in all other brain structures. Recently, mosaic evolution has been demonstrated for the brain of wild mammals (Barton and Harvey, 2000), bats and whales (Clark et al, 2001) and wild avian species (Iwaniuk et al, 2004;Iwaniuk and Hurd, 2005;Charvet and Striedter, 2009), and it seems to be that mosaic evolution characterises the diversification of avian and mammalian brain composition without excluding domesticated species. Apparently, it is not just the subsystems of the brain that might follow different trends of alteration independently from others but even the left or right parts of a subsystem.…”

Building brains that can evolve: Challenges and prospects for evo-devo neurobiology

“…After all, brain development can be studied at several different levels of analysis -ranging from gene regulation to tissue formation -and each level can be considered a «causal mechanism» in its own right. For example, my own research has shown that the expansion of the telencephalon in parrots and songbirds, relative to other birds, is caused by an evolutionary delay in neurogenesis (which increases the number of telencephalic precursor cells; Charvet & Striedter, 2009). We do not know the molecular mechanism underlying this change in neurogenesis timing, but our finding is nonetheless mechanistic.…”