Study of pallial neurogenesis in shark embryos and the evolutionary origin of the subventricular zone

Abstract

The dorsal part of the developing telencephalon is one of the brain areas that has suffered most drastic changes throughout vertebrate evolution. Its evolutionary increase in complexity was thought to be partly achieved by the appearance of a new neurogenic niche in the embryonic subventricular zone (SVZ). Here, a new kind of amplifying progenitors (basal progenitors) expressing Tbr2, undergo a second round of divisions, which is believed to have contributed to the expansion of the neocortex. Accordingly, the existence of a pallial SVZ has been classically considered exclusive of mammals. However, the lack of studies in ancient vertebrates precludes any clear conclusion about the evolutionary origin of the SVZ and the neurogenic mechanisms that rule pallial development. In this work, we explore pallial neurogenesis in a basal vertebrate, the shark Scyliorhinus canicula, through the study of the expression patterns of several neurogenic markers. We found that apical progenitors and radial migration are present in sharks, and therefore, their presence must be highly conserved throughout evolution. Surprisingly, we detected a subventricular band of ScTbr2-expressing cells, some of which also expressed mitotic markers, indicating that the existence of basal progenitors should be considered an ancestral condition rather than a novelty of mammals or amniotes. Finally, we report that the transcriptional program for the specification of glutamatergic pallial cells (Pax6, Tbr2, NeuroD, Tbr1) is also present in sharks. However, the segregation of these markers into different cell types is not clear yet, which may be linked to the lack of layering in anamniotes.

Mosaic heterochrony in neural progenitors sustains accelerated brain growth and neurogenesis in the juvenile killifish N. furzeri

“…In mammals, the expansion of the pallium during evolution is thus driven by the emergence and diversification of basally-located progenitors, which amplify neuronal production downstream of apical RG (Romero and Borrell, 2015). While no basal progenitors are present in the pallium of birds, reptiles and teleost fish, some have been observed in a shark, highlighting a flexibility in pallial lineage patterns (Docampo-Seara et al, 2018). The strategy to amplify basal progenitors to boost neuronal production in mammals differs from what we observed in killifish.…”

Mosaic Heterochrony in Neural Progenitors Sustains Accelerated Brain Growth and Neurogenesis in the Juvenile Killifish N. furzeri

“…In mammals, amplification and diversification of basal progenitors indeed contribute to increase pallial size. Some basal progenitors have also been observed in a shark, highlighting a recurrent point of flexibility in pallial lineage patterns [37]. Our work shows that a different strategy has been deployed in killifish to boost neuronal production.…”

The Zebrafish Amygdaloid Complex – Functional Ground Plan, Molecular Delineation, and Everted Topology

“…Important for a better understanding of the early evolution of vertebrate amygdala and isocortex-homolog will be the identification of EmT territories in more basally derived fish. The probably highly conserved territories in actinopterygian and non-actinopterygian fish, such as agnathans (lamprey) and chondrichthyes (sharks and manta rays), might allow to solve disagreements about their forebrain evolution (Puelles, 2001;Pombal et al, 2009;Mueller, 2011;Northcutt, 2011;Schluessel, 2015;Docampo-Seara et al, 2018). Similarly, the discovery of EmT and nLOT enabled in this study to effectively compare the everted zebrafish with the evaginated forebrain of mammals.…”