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Abstract

Within the clade of amniotes (including mammals, birds, and non-avian reptiles), two lineages—birds and mammals—are renowned for their remarkable cognitive abilities. These capabilities likely evolved through innovations in the forebrain, particularly in the dorsal telencephalon, or pallium. Since the last common ancestor of amniotes approximately 320 million years ago, the pallium has undergone extensive morphological diversification. In mammals, the pallium is dominated by layered structures like the isocortex, whereas birds and reptiles primarily feature nuclear-organized regions, such as the dorsal ventricular ridge (DVR). While non-avian reptiles possess a small layered cortex, birds lack a layered cortex entirely and instead possess the hyperpallium, a unique nuclear-organized dorsal structure. These profound differences have sparked debates about pallial evolution, leading to competing hypotheses—some emphasizing homology of cell types performing analogous roles in a conserved neural microcircuit, while others focus on shared developmental origins in distinct pallial domains. In my dissertation, I addressed these debates by investigating the cellular composition, development, and evolution of the pallium across amniotes. To this end, I generated spatially resolved cell type atlases of the entire adult chicken pallium and its developmental stages using single-nucleus RNA sequencing and spatial transcriptomics. I compared these data to equivalent datasets from mammals and reptiles, including those I generated, as well as publicly available datasets, to reconstruct the evolutionary history of pallial structures and cell types. Within chickens, I found remarkable similarity between neurons in the hyperpallium and the nidopallium (ventral DVR), despite their topologically distinct locations. This similarity likely arises from extensive gene expression convergence during late development, suggesting that embryonic topological location does not always dictate the gene expression programs underlying adult functional properties in birds. Across species, my findings confirm conserved gene expression patterns in inhibitory neurons, but reveal an expansion of a cell type predominantly found in the mammalian amygdala that is distributed throughout the avian pallium. I also identified conserved excitatory neuron types in the hippocampal regions of birds, non-avian reptiles, and mammals, as well as homologous populations of claustrum-like neurons in the mesopallium (anterior DVR) of birds. Additionally, certain cell types in the avian mesopallium resemble neurons in the deep layers of the mammalian isocortex. In contrast, some populations in the hyperpallium and nidopallium show substantial divergence. Developmental analyses suggest these neurons evolved distinct identities in birds, diverging significantly from their mammalian counterparts. These findings challenge previous circuitry-based models, which propose homologies largely unsupported by my observations. Although my results align more closely with development-based homology hypotheses, they also argue against the notion of simple one-to-one correspondences between pallial regions. Instead, they reveal a mosaic pattern of evolution: some excitatory cell types are conserved across species, even when located in different pallial domains, whereas others have diverged significantly. This dissertation also includes an investigation into the cellular evolution of the mammalian isocortex across major mammalian lineages. For example, I highlight the conservation of the principal claustral cell type across mammals, setting the stage for future studies on pan-mammalian cellular features of the pallium. Overall, this work provides critical insights into the anatomy, development, and evolution of the amniote pallium—particularly the avian pallium. It confirms previously suggested homologies, such as those among inhibitory or hippocampal excitatory neurons, while uncovering novel relationships, such as those between avian mesopallial excitatory neurons and mammalian deep-layer isocortical neurons. My findings underscore the importance of developmental data in testing evolutionary models and challenge longstanding assumptions about regional homology in the amniote pallium. By highlighting conserved, divergent, and convergent aspects of pallial evolution, this dissertation lays the foundation for understanding the molecular mechanisms underlying advanced cognitive abilities in birds.