Ancient origins of the chordate forebrain: Conserved patterning of the anterior neuroectoderm in amphioxus

While the general organization of the chordate central nervous system (CNS) is highly conserved and consists of a dorsal neural tube with an anterior brain, the evolutionary origin of this key aspect of the chordate body plan remains obscure. In recent years, a conserved anterior gene regulatory network (aGRN) has been shown to pattern the larval anterior nervous system of several invertebrates, including the two non-chordate deuterostome phyla (echinoderms and hemichordates), in which the aGRN controls the development of the apical organ. Although clear homologs of the apical organ are not present in chordates, most aGRN genes are expressed in the vertebrate forebrain. In this PhD thesis I trace the evolution of the aGRN across deuterostomes using the cephalochordate amphioxus as the main model organism. I first show that during amphioxus development aGRN genes are expressed in a similar pattern to the one found in echinoderms and hemichordates, are regulated by Wnt/b-catenin signalling and are active in the anterior neuroectoderm that forms the larval brain. As a comparative system, I also characterize the development of the apical organ in an understudied group of echinoderms, the crinoids. To follow the fate of the amphioxus anterior neuroectoderm, I next investigate neurogenesis, proliferation and cell type differentiation in larval and adult brains. I demonstrate the presence of a hypothalamic-like region in the anterior cerebral vesicle, which derives from the region where the aGRN is active during development. Finally, I explore how changes in the specification of the body axes and in the expression of one of the upstream aGRN genes, FoxQ2, might have underlined the evolution of the complex vertebrate brain. Taken together, the results presented in this thesis support the conservation across deuterostome evolution of an aGRN that controls the development of the anterior neuroectoderm. In the chordate lineage, the network was integrated to the neurulation program to specify retinal and hypothalamic areas of the forebrain. Furthermore, this work provides a comprehensive characterization of neuroarchitecture and cell type composition across the amphioxus life cycle, facilitating the comparison with other chordate taxa to reconstruct the evolution of the chordate nervous system.

Name dc:type.qualificationname

Doctor of Philosophy (PhD)

Level dc:type.qualificationlevel

Doctoral

Grantor dc:publisher.institution

University of Cambridge

Year dc:date.issued

2022

Author dc:creator

• Gattoni, Giacomo

Advisor dc:contributor.advisor

• Benito Gutierrez, Elia

• amphioxus
• apical organ
• evodevo
• forebrain
• gene regulatory networks
• nervous system evolution

Licence

• https://www.rioxx.net/licenses/all-rights-reserved/

Language dc:language

eng

DOI dc:identifier.doi

https://doi.org/10.17863/CAM.95556

OAI identifier oai:identifier

oai:www.repository.cam.ac.uk:1810/348137