Computational Analysis of Gene Expression in the Teleost Forebrain and the Cellular Basis of a Social Behavior
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Gruenhagen, George Wolfgang
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Abstract
Teleosts (ray-finned fish) are the largest vertebrate clade, comprising roughly half of all extant vertebrate species, and can perform complex behaviors requiring advanced cognition. A species of teleost fish, Mchenga conophoros (MC), performs a social behavior called bower-building, whereby males repetitively manipulate sand to form a structure called a bower, over which they court females and chase away competing males. Comparative genomic analysis has revealed that this social behavior performed by MC is associated with a region of high genomic divergence on linkage group 11. While the genetic basis of this behavior has been investigated, the brain regions and cell populations involved are unknown. Furthermore, the homology of brain regions in the teleost to the mammalian brain is unclear due to the unique folding of the teleost brain during development. This work aims to 1) identify the cellular basis of bower-building in MC and 2) uncover the relationships between cell-types and anatomical regions in the teleost brain to other vertebrates - amphibians, reptiles, birds and mammals.
To address the first aim, we performed single nuclei RNA-sequencing (snRNA-seq) on 19 males actively performing bower-building and 19 control males that were not performing bower-building. This resulted in a total of 33,674 nuclei. I linked genes associated with the evolution of bower-building behavior to a subpopulation of quiescent stem-like cells. We found evidence that behavior-associated neural activity may result in a departure from quiescence and a differential supply of new neurons to a specific region in the teleost brain, the ventral subdivision of the dorsal lateral pallium (Dl-v).
To determine the relationship of teleostean brain regions, such as the Dl-v, to other vertebrates, we performed spatial transcriptomics, which profiles gene expression within tissue architecture, unlike snRNA-seq. Together, with these complementary technologies, we created a spatially resolved atlas of gene expression in the MC forebrain and compared expression profiles of thousands of genes across vertebrates. I identified ancestral features of non-neuronal and neuronal populations in MC, including hippocampal and surprisingly neocortical populations. The presence of neocortical-like structures in non-mammals is widely debated. Here I find evidence of neocortical transcriptional signatures in the teleost granule zone of the dorsal lateral pallium (Dl-g). Additionally, I found conserved molecular features of the hippocampus in the teleost Dl-v. In summary, we identified forebrain populations involved in bower-building behavior and ascertained their evolutionary relationships to other vertebrates.
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2023-08-18
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