Developmental basis for telencephalon expansion in waterfowl: enlargement prior to neurogenesis

Abstract

Some altricial and some precocial species of birds have evolved enlarged telencephalons compared with other birds. Previous work has shown that finches and parakeets, two species that hatch in an immature (i.e. altricial) state, enlarged their telencephalon by delaying telencephalic neurogenesis. To determine whether species that hatch in a relatively mature (i.e. precocial) state also enlarged their telencephalon by delaying telencephalic neurogenesis, we examined brain development in geese, ducks, turkeys and chickens, which are all precocial. Whereas the telencephalon occupies less than 55 per cent of the brain in chickens and turkeys, it occupies more than 65 per cent in ducks and geese. To determine how these species differences in adult brain region proportions arise during development, we examined brain maturation (i.e. neurogenesis timing) and estimated telencephalon, tectum and medulla volumes from serial Nissl-stained sections in the four species. We found that incubation time predicts the timing of neurogenesis in all major brain regions and that the telencephalon is proportionally larger in ducks and geese before telencephalic neurogenesis begins. These findings demonstrate that the expansion of the telencephalon in ducks and geese is achieved by altering development prior to neurogenesis onset. Thus, precocial and altricial species evolved different developmental strategies to expand their telencephalon.

Figure 1.

Photographs of (a) a chicken and (b) a duck at ED 5.75 (Hamburger–Hamilton stage 29, approx. 27% incubation) and ED 7 (Hamburger–Hamilton stage 28, approx. 27% incubation), respectively. These images show that the telencephalon (white lines) is larger in ducks compared with incubation-matched chickens. Scale bar, 1 mm.

Figure 2.

Analysis of the PZF data shows that neurogenesis timing is highly conserved across waterfowl (Anseriformes) and chicken-like species (Galliformes) once age is expressed in terms of per cent incubation. (a) A plot of telencephalic PZFs versus age in days shows that the telencephalon matures earlier in chickens than in other chicken-like birds or waterfowl. In contrast, if PZFs are plotted against per cent incubation, then tissue maturation becomes highly predictable for the (b) telencephalon, (c) the tectum and (d) the medulla. Hatching typically occurs after 30, 28, 26 and 21 days of incubation in geese, turkeys, ducks and chickens, respectively. Open circle, goose; filled circle, duck; open diamond, turkey; filled diamond, chicken.

Figure 3.

Brain region growth curves reveal that the telencephalon is larger in waterfowl (Anseriformes) than in incubation-matched chicken-like birds (Galliformes). (a) If absolute telencephalon volume is plotted against age in days, then the telencephalon seems to grow faster in chickens (filled diamond) than in turkeys (open diamond), quail (diamond with a dot), geese (open circle) or ducks (filled circle). (b) However, if telencephalon volume is plotted against age expressed as per cent of the incubation period, then the telencephalon is consistently larger in Anseriformes than in Galliformes. (c) Similarly, telencephalon size relative to overall brain size (i.e. fractional telencephalon volume) is consistently larger in Anseriformes than in incubation-matched Galliformes. (d) The size of the telencephalon relative to the medulla is likewise larger in Anseriformes than in Galliformes, at least until approximately 40 per cent incubation. Volumetric measurements of the brain of bobwhite quail are from an earlier study that used identical methods (Striedter & Charvet 2008).

Figure 4.

(a) The absolute volume of the tectum is similar in waterfowl (Anseriformes) and incubation-matched chicken-like birds (Galliformes), but (b) the medulla is slightly larger in the waterfowl. (c) The tectum's volume fraction is smaller in waterfowl than in chicken-like birds, but (d) the tectum/medulla ratio is similar in the two orders until approximately 30 per cent of incubation. Thereafter, the tectum/medulla ratio is larger in chicken-like birds. The data for bobwhite quail (C. virgianus) are from Striedter & Charvet (2008). Filled circle, duck; open circle, goose; filled diamond, chicken; open diamond, turkey; diamond with a dot, quail.