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.

Abdel-Mannan O, Cheung AF, Molnár Z (2008) Evolution of cortical neurogenesis. Brain Res Bull 75:398–404.
Almli LM, Wilczynski W (2007) Regional distribution and migration of proliferating cell populations in the adult brain of Hyla cinerea (Anura, Amphibia). Brain Res 1159:112–118.
Altman J, Bayer SA (1990) Verticle compartmentation and cellular transformations in the germinal matrices of the embryonic rat cerebral cortex. Exp Neurol 107:23–35.
Bhide PG (1996) Cell cycle kinetics in the embryonic mouse corpus striatum. J Comp Neurol 374:506–522.
Bravo R, Frank R, Blundell PA, Macdonald-Bravo H (1987) Cyclin/PCNA is the auxiliary protein of DNA polymerase-δ. Nature 326:515–517.
Charvet CJ, Striedter GF (2008) Developmental species differences in brain cell cycle rates between bobwhite quail (Colinus virginianus) and parakeets (Melopsittacus undulatus): implications for mosaic brain evolution. Brain Behav Evol 72:295–306.
Charvet CJ, Striedter GF (2009) Developmental origins of mosaic brain evolution: morphometric analysis of the developing zebra finch brain. J Comp Neurol 514:203–213.
Cheung AF, Pollen AA, Tavare A, DeProto J, Molnár Z (2007) Comparative aspects of cortical neurogenesis in vertebrates. J Anat 211:164–176.
Crosby EC (1917) The forebrain of Alligator mississippiensis. J Comp Neurol 27:325–402.
Ferguson MWJ (1985) Reproductive biology and embryology of the crocodilians. In: Biology of the Reptilia, Development A vol 14 (Gans C, Billet F, Maderson PFA, eds), pp 329–491. New York: Wiley.
Goffinet AM (1983) The embryonic development of the cortical plate in reptiles: a comparative study in Emys orbicularis and Lacerta agilis. J Comp Neurol 215:437–452.
Goffinet AM, Daumerie C, Langerwerf B, Pieau C (1986) Neurogenesis in reptilian cortical structures: 3H-thymidine autoradiographic analysis. J Comp Neurol 243:106–116.
Hedges SB (1994) Molecular evidence for the origins of birds. Proc Natl Acad Sci USA 91:2621–2624.
Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360.
Källén B (1951) On the ontogeny of the reptilian forebrain-nuclear structures and ventricular sulci. J Comp Neurol 95:307–347.
Kriegstein A, Noctor S, Martínez-Cerdeño V (2006) Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7:883–890.
Martínez-Cerdeño V, Noctor SC, Kriegstein AR (2006) The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. Cereb Cortex 16(suppl 1):i152–161.
Medina L, Reiner A (2000) Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23:1–12.
Meyer A, Zardoya R (2003) Recent advances in the (molecular) phylogeny of vertebrates. Ann Rev Ecol Evol Syst 34:311–338.
Molnár Z, Métin C, Stoykova A, Tarabykin V, Price DJ, Prancis F, Meyer G, Dehay C, Kennedy H (2006) Comparative aspects of cerebral cortical development. Eur J Neurosci 23:921–934.
Nowakowski RS, Lewin SB, Miller MW (1989) Bromodeoxyuridine immunohistochmical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocyt 18:311–318.
Pritz MB (2008) Early diencephalon development in Alligator. Brain Behav Evol: 71:15–31.
Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JLR (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424:409–438.
Reynolds ML, Cavanaugh ME, Dziegelewska KM, Hinds LA, Saunders NR, Tyndale-Biscoe CH (1985) Postnatal development of the telencephalon of the tammar wallaby (Macropus eugenii). Anat Embryol 173:81–94.
Saunders NR, Adam E, Reader M, Mollgård K (1989) Monodelphis domestica (grey short-tailed opossum): an accessible model for studies of early neocortical development. Anat Embryol 180:227–236.
Simmons AM, Horowitz SS, Brown RA (2008) Cell proliferation in the forebrain and midbrain of the adult bullfrog, Rana catesbeiana. Brain Behav Evol 71:41–53.
Smart IH (1961) The subependymal layer of the mouse brain and its cell production as shown by radioautography after thymidine-H3 injection. J Comp Neurol 116:325–347.
Smart IH (1973) Proliferative characteristics of the ependymal layer during the early development of the mouse neocortex: a pilot study based on recording the number, location and plane of cleavage of mitotic figures. J Anat 116:67–91.
Smart IH (1985) Differential growth of the cell production systems in the lateral wall of the developing mouse telencephalon. J Anat 141:219–229.
Smart IH, Dehay C, Giroud P, Berland M, Kennedy H (2002) Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb Cortex 12:37–53.
Striedter GF, Charvet CJ (2008) Developmental origins of species differences in telencephalon and tectum size: morphometric comparisons between a parakeet (Melopsittacus undulatus) and a quail (Colinus virgianus). J Comp Neurol 507:1663–1675.
Striedter GF, Charvet CJ (2009) Telencephalon enlargement by the convergent evolution of expanded subventricular zones. Biol Letters 23:134–137.
Striedter GF, Keefer BB (2000) Cell migration and aggregation in the developing telencephalon: pulse-labeling chick embryos with bromodeoxyuridine. J Neurosci 20:8021–8030.
Takahashi T, Nowakowski RS, Caviness VS Jr (1995) Early ontogeny of the second proliferative population of the embryonic murine cerebral wall. J Neurosci 15:6058–6068.
Valero J, Weruaga E, Murias AR, Recio JS, Alonso JR (2005) Proliferation markers in the adult rodent brain: bromodeoxyuridine and proliferating cell nuclear antigen. Brain Res Protocols 15:127–134.
Whetstone KN, Martin LD (1979) New look at the origins of birds and crocodiles. Nature 279:234–236.
Wullimann MF, Rink E, Vernier P, Schlosser G (2005) Secondary neurogenesis in the brain of the African clawed frog, Xenopus laevis, as revealed by PCNA, Delta-1, Neurogenin-related-1 and NeuroD expression. J Comp Neurol 489:387–402.
Zecevic N, Chen Y, Filipovic R (2005) Contributions of cortical subventricular zone to the development of the human cerebral cortex. J Comp Neurol 491:109–122.
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