Christine J. Charvet

Evo-Devo and Brain Scaling: Candidate Developmental Mechanisms for Variation and Constancy in Vertebrate Brain Evolution

Biologists have long been interested in both the regularities and the deviations in the relationship between brain, development, ecology, and behavior between taxa. We first examine some basic information about the observed ranges of fundamental changes in developmental parameters (i.e. neurogenesis timing, cell cycle rates, and gene expression patterns) between taxa. Next, we review what is known about the relative importance of different kinds of developmental mechanisms in producing brain change, focusing on mechanisms of segmentation, local and general features of neurogenesis, and cell cycle kinetics. We suggest that a limited set of developmental alterations of the vertebrate nervous system typically occur and that each kind of developmental change may entail unique anatomical, functional, and behavioral consequences for the organism. Thus, neuroecologists who posit a direct mapping of brain size to behavior should consider that not any change in brain anatomy is possible.

Systematic, balancing gradients in neuron density and number across the primate isocortex.

The cellular and areal organization of the cerebral cortex impacts how it processes and integrates information. How that organization emerges and how best to characterize it has been debated for over a century. Here we demonstrate and describe in the isocortices of seven primate species a pronounced anterior-to-posterior gradient in the density of neurons and in the number of neurons under a unit area of the cortical surface. Our findings assert that the cellular architecture of the primate isocortex is neither arranged uniformly nor into discrete patches with an arbitrary spatial arrangement. Rather, it exhibits striking systematic variation. We conjecture that these gradients, which establish the basic landscape that richer areal and cellular structure is built upon, result from developmental patterns of cortical neurogenesis which are conserved across species. Moreover, we propose a functional consequence: that the gradient in neurons per unit of cortical area fosters the integration and dimensional reduction of information along its ascent through sensory areas and toward frontal cortex.

Developmental origins of species differences in telencephalon and tectum size: Morphometric comparisons between a parakeet (Melopsittacus undulatus) and a quail (Colinus virgianus)

Parrots, including parakeets, evolved significantly larger brains than other birds, relative to their body size, and they possess a proportionately larger telencephalon. For example, the telencephalon occupies approximately 68% of the brain in parakeets but only 52% in bobwhite quail. The present study was designed to determine when and how this difference in brain region proportions arises during development. To that end, we present volumetric data on the major brain regions in parakeets and bobwhite quail at several stages of embryogenesis, at hatching and, for the parakeets, 1 week after hatching. We also report on the proportional sizes of each regions proliferative and postproliferative zones. One major finding is that parakeets develop a proportionately larger telencephalon relatively late in development and that this late increase correlates with a delay in telencephalic neurogenesis. The most prominent aspect of this delayed telencephalic development is a tremendous expansion of the proliferative subventricular zone in the telencephalon of late embryonic and posthatching parakeets. The second major finding is that the tectum is much smaller in parakeets than in quail at all developmental stages examined, suggesting that the tectums reduced size is due to an evolutionary change in how much tissue was allocated to become tectum at the time of brain regionalization. Collectively these findings indicate that evolutionary changes in brain region proportions are caused not by a single type of change but by several distinct developmental mechanisms, including changes in brain regionalization and neurogenesis timing. J. Comp. Neurol. 507:1663–1675, 2008.

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

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. J. Comp. Neurol. 514:203–213, 2009.

Phylogeny of the Telencephalic Subventricular Zone in Sauropsids: Evidence for the Sequential Evolution of Pallial and Subpallial Subventricular Zones

The telencephalon of birds and placental mammals harbors a proliferative subventricular zone (SVZ) in the subpallium as well as the pallium. Turtles, which are phylogenetically intermediate between bird, and mammals, exhibit at best a rudimentary SVZ. This suggests that SVZs evolved independently in mammals and birds, but it is not clear whether subpallial and pallial SVZs evolved with the origin of birds or in some earlier, non-avian sauropsid ancestor. To answer this question, we examined the brains of embryonic alligators (Ferguson stages 15–22) because crocodilians are the closest extant sister group to birds. To visualize the SVZ we labeled mitotic cells with antibodies against phosphorylated histone-3 (pH3) and proliferating cells with antibodies against proliferating cell nuclear antigen (PCNA). We found that the telencephalon of alligators contains an SVZ only in the subpallium. Because turtles, lizards and amphibians seem to lack SVZs, our finding suggests that a subpallial SVZ evolved in the last common ancestor of birds and crocodilians. Given that placental mammals and birds, but not marsupial mammals or reptiles, possess an SVZ within their pallium, we conclude that a pallial SVZ probably evolved independently in birds and placental mammals.

Developmental Species Differences in Brain Cell Cycle Rates between Northern Bobwhite Quail (Colinus virginianus) and Parakeets (Melopsittacus undulatus): Implications for Mosaic Brain Evolution

Adult brains differ among species in the proportional sizes of their major subdivisions. For example, the telencephalon occupies 71% of the entire brain in parakeets (Melopsittacus undulatus) but only 54% in quail (Colinus virginianus). In contrast, the tectum is smaller in parakeets than in quail. To determine whether these differences in brain region size arise because of species differences in cell cycle rates, parakeet and quail embryos were collected at various stages of development (HH24–HH37) and stained with antibodies against proliferating cell nuclear antigen (PCNA), which labels all dividing cells, and phosphorylated histone-3 (pH3), which labels M-phase cells. Analysis of pH3+ cell densities and pH3+/PCNA+ cell ratios were used to compare cell cycle rates across stages and species. Cumulative labeling with bromodeoxyuridine (BrdU) was also used to compare cell cycle rates at stages 24 and 28 in quail. We found that telencephalic cell cycle rates lengthen with age in both species, but that they lengthen significantly later in parakeets than in quail. This species difference in cell cycle rates explains, at least partly, why adult parakeets have a proportionately larger telencephalon. Tectal cell cycle rates also remain elevated for a prolonged period of time in parakeets compared to quail. This seems paradoxical at first, given that the parakeet’s adult tectum is relatively small. However, the tectum is initially much smaller but then grows more extensively in parakeets than in quail. Thus, species differences in adult brain proportions can be traced back to species differences in cell cycle kinetics.

Developmental Modes and Developmental Mechanisms can Channel Brain Evolution.

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.

Telencephalon enlargement by the convergent evolution of expanded subventricular zones

Some mammals and birds independently evolved an enlarged telencephalon. They appear to have done so, at least in part, by developing a thick telencephalic subventricular zone (SVZ). We suggest that this correlation between telencephalic enlargement and SVZ expansion is due to a mechanical constraint acting on the proliferative ventricular zone (VZ). Essentially, we argue that rapid proliferation in the VZ after post-mitotic cells in the overlying mantle zone have begun to form limits the VZs tangential expandability and forces some proliferating cells to emigrate from the VZ and expand the pool of proliferating cells that comprise the SVZ.

Modeling local and cross-species neuron number variations in the cerebral cortex as arising from a common mechanism.

Significance Despite great diversity across mammals in the number of cortical neurons and the cognitive functions they support, the fundamental process which populates the cerebral cortex with neurons changes only subtly from the smallest rodents to the largest primates. Understanding how the dynamics of neurogenesis can vary will help unravel how the genome molds normal and disrupted cortical development. We gathered data on the growing and mature cortex to build a computational model of neurogenesis. The model recapitulates how dynamics, known to vary across species and across the cortex, sculpt the basic landscape of the embryonic cortex. Features of the cortex long thought to be the result of special selection are revealed as the necessary product of a conserved mechanism. A massive increase in the number of neurons in the cerebral cortex, driving its size to increase by five orders of magnitude, is a key feature of mammalian evolution. Not only are there systematic variations in cerebral cortical architecture across species, but also across spatial axes within a given cortex. In this article we present a computational model that accounts for both types of variation as arising from the same developmental mechanism. The model employs empirically measured parameters from over a dozen species to demonstrate that changes to the kinetics of neurogenesis (the cell-cycle rate, the progenitor death rate, and the “quit rate,” i.e., the ratio of terminal cell divisions) are sufficient to explain the great diversity in the number of cortical neurons across mammals. Moreover, spatiotemporal gradients in those same parameters in the embryonic cortex can account for cortex-wide, graded variations in the mature neural architecture. Consistent with emerging anatomical data in several species, the model predicts (i) a greater complement of neurons per cortical column in the later-developing, posterior regions of intermediate and large cortices, (ii) that the extent of variation across a cortex increases with cortex size, reaching fivefold or greater in primates, and (iii) that when the number of neurons per cortical column increases, whether across species or within a given cortex, it is the later-developing superficial layers of the cortex which accommodate those additional neurons. We posit that these graded features of the cortex have computational and functional significance, and so must be subject to evolutionary selection.

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

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.