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Abstract

Cephalopods have a highly derived body plan and a suite of innovations with no obvious correlates in other animals. One of the most striking novelties in cephalopods is their embryogenesis, which lacks any trace of the spiral cleavage pattern found in non-cephalopod molluscs and other spiralians. Instead, cephalopod embryos undergo bilateral, meroblastic cleavage on top of a large yolk, greatly resembling early embryogenesis in fish and constituting a striking convergence between these two distantly related groups. In this thesis, I explore cephalopod development from a molecular perspective, leveraging genomics, transcriptomics, and gene expression studies to shed light on the development of these remarkable animals. To identify the gene networks important in this highly derived developmental program, we analyzed the genome and transcriptomes of the California two-spot octopus, Octopus bimaculoides. The core developmental gene repertoire of the octopus is broadly similar to that found in typical invertebrate bilaterians, except for massive expansions in the protocadherins and the C2H2 zinc finger transcription factor gene families. I identified hundreds of cephalopod-specific genes, many of which showed elevated expression levels in such specialized cephalopod structures as the skin, the suckers, and the nervous system. Comparative genome structure analysis suggests that substantial expansion of a handful of gene families, along with extensive remodeling of genome linkages, drove the evolution of cephalopod morphological novelties. A prominent cephalopod innovation is their large, complex nervous system. The morphological structure of the cephalopod embryonic brain was studied with molecular markers of neuronal development. Expression of pan-neuronal genes indicated that early neurogenic territories in octopus are arranged as concentric cords rather than pairs of ganglia, an arrangement hypothesized to be characteristic of the ancestral molluscan nervous system. The expression of a highly conserved developmental transcription factor cassette that is characteristic of the vertebrate midbrain-hindbrain boundary identified the major division in the cephalopod brain, that between the supraesophageal and subesophageal masses. Similar to the vertebrate midbrain-hindbrain boundary, this territory is a signaling center, although the signaling ligands detected in octopus are greatly expanded from those described in other animals. Gene expression study later in development indicated a shared transcription factor “fingerprint” between cephalopods and other animals of neurosecretory and higher motor centers. In contrast, the cephalopod frontal-vertical system, which is a higher integrative center implicated in learning, memory and decision-making, proved to have a different molecular signature from that of the analogous structures in vertebrates and annelids. Finally, I examined the deployment of highly conserved developmental toolkit genes using both bioinformatics and gene expression. Analysis of Hox gene expression indicated that, despite the absence of a Hox genomic cluster, these genes are expressed in a canonical pattern of anterior-posterior nested domains, one modified to reflect the radial morphology of the cephalopod embryo. Bioinformatic analyses detected the Hox genes and other highly conserved developmental toolkit genes primarily during stages that coincide with the emergence of the body plan, but not before. Notably, many of the genes differentially expressed in the early transcriptomes are taxonomically restricted. Our results support a mid-developmental period of highly conserved toolkit gene expression preceded by the deployment of taxonomically restricted genes. These results suggest the surprising conclusion that it is cephalopod-specific genes that underlie the “fish-like” embryogenesis of cephalopods.

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