Phylogenetic origins of early alterations in brain region proportions

Abstract

Adult galliform birds (e.g. chickens) exhibit a relatively small telencephalon and a proportionately large optic tectum compared with parrots and songbirds. We previously examined the embryonic origins of these adult species differences and found that the optic tectum is larger in quail than in parakeets and songbirds at early stages of development, prior to tectal neurogenesis onset. The aim of this study was to determine whether a proportionately large presumptive tectum is a primitive condition within birds or a derived feature of quail and other galliform birds. To this end, we examined embryonic brains of several avian species (emus, parrots, songbirds, waterfowl, galliform birds), reptiles (3 lizard species, alligators, turtles) and a monotreme (platypuses). Brain region volumes were estimated from serial Nissl-stained sections. We found that the embryos of galliform birds and lizards exhibit a proportionally larger presumptive tectum than all the other examined species. The presumptive tectum of the platypus is unusually small. The most parsimonious interpretation of these data is that the expanded embryonic tectum of lizards and galliform birds is a derived feature in both of these taxonomic groups.

Fig. 1

a Variations in presumptive tectum size mapped onto a phylogeny of amniotes [Meyer and Zardoya, 2003; Hackett et al., 2008]. The gray bars indicate the average size of the presumptive tectum in early embryos of the indicated taxonomic groups. The major conclusion of the present study is that galliform birds (chickens, turkeys, quail) and lizards (chameleons, wall lizards, skinks) exhibit a proportionally larger presumptive tectum than the other examined species. The photographs in (b) and (c) respectively show an emu embryo at embryonic day 8 and a chicken embryo at day 4. The white lines point to the presumptive tectum. Scale bars = 1 mm.

Fig. 2

a Presumptive tectum fraction (expressed as a percentage of brain volume) plotted against embryonic age. In order to control for species differences in maturation rate, embryonic age is expressed as a percentage of the species’ normal incubation time. Previous analyses showed that neurogenesis onset is highly predictable in several precocial species once age is expressed as a percentage of normal incubation period [Charvet and Striedter, 2009b, c]. Specifically, the presumptive optic tectum becomes morphologically identifiable at approximately 14% of the normal incubation period and tectal neurogenesis onset occurs roughly around 30% of normal incubation period in the examined precocial species. b Histograms of the mean presumptive tectum fraction for each examined species plotted along with individual data points show that the optic tectum is proportionally enlarged in galliform birds and lizards compared with the other species we examined. c Scatterplot of embryonic tectum fraction versus adult tectum fraction for 8 species in which both adult and embryonic data were available, together with the regression line.