Bigger brains cycle faster before neurogenesis begins: a comparison of brain development between chickens and bobwhite quail

Abstract

The chicken brain is more than twice as big as the bobwhite quail brain in adulthood. To determine how this species difference in brain size emerges during development, we examined whether differences in neurogenesis timing or cell cycle rates account for the disparity in brain size between chickens and quail. Specifically, we examined the timing of neural events (e.g. neurogenesis onset) from Nissl-stained sections of chicken and quail embryos. We estimated brain cell cycle rates using cumulative bromodeoxyuridine labelling in chickens and quail at embryonic day (ED) 2 and at ED5. We report that the timing of neural events is highly conserved between chickens and quail, once time is expressed as a percentage of overall incubation period. In absolute time, neurogenesis begins earlier in chickens than in quail. Therefore, neural event timing cannot account for the expansion of the chicken brain relative to the quail brain. Cell cycle rates are also similar between the two species at ED5. However, at ED2, before neurogenesis onset, brain cells cycle faster in chickens than in quail. These data indicate that chickens have a larger brain than bobwhite quail mainly because of species differences in cell cycle rates during early stages of embryonic development.

Figure 1.

(a) When compared in absolute days, neural events generally occur later in bobwhite quail than in chickens. (b) When compared in percentage of normal incubation period, the timing of neural events overlaps in chickens and quail. Neurogenesis onset events are represented in italics. Hatching was not considered a neural event in our statistical analysis. Diamonds, chicken; filled circles, quail.

Figure 2.

Brain volumes of chickens and quail plotted against age expressed as a percentage of normal incubation period. By 19% of incubation, the chicken brain is already more than twice as big as the incubation-matched quail brain. The species difference in brain size persists throughout embryonic development. Diamonds, chicken; filled circles, quail.

Figure 3.

At 11% of incubation, the brain pH3+/PCNA+ ratios is higher in chickens than in quail. These findings suggest that brain cells cycle faster in chickens when compared with quail at 11% of incubation. Values are expressed as means and standard errors.

Figure 4.

These graphs show how the fraction of BrdU+ cells in the brain (i.e. tectum, telencephalon) VZ increases with survival time after BrdU application in chickens and quail at (a) 11% of incubation (i.e. ED2–3) and (b) 22% of incubation (i.e. ED5). The slopes of these lines are inversely proportional to cell cycle duration. Furthermore, the LIs saturate at similar levels in the two species. These data indicate that (a) brain precursor cells cycle faster in chickens than in quail at 11% of incubation. (b) However, brain precursor cells cycle at a similar rate in chickens and quail at 22% of incubation. Diamonds, chicken brain; filled circles, quail brain.

Figure 5.

Hatchling brain and body weights correlate positively with incubation period in some galliform birds, but this correlation is noisy. Bobwhite quail have a longer incubation period than chickens yet hatchling brains of chickens are larger than those of quail. Data are from Portmann (1947b). Black-filled circles, brain weights; grey-filled circles, body weights.