Phylogeny of the telencephalic subventricular zone in sauropsids: evidence for the sequential evolution of pallial and subpallial subventricular zones

Abstract

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.