Post-reproductive life in the female octopus is characterized by an extreme pattern of maternal care: the mother cares for her clutch of eggs without feeding until her death. These maternal behaviors are completely eradicated if the optic glands, the octopus analog of the vertebrate pituitary gland, are removed from brooding females. Despite the optic gland’s importance in regulating maternal behavior, the possible mechanisms underlying optic gland function are unknown. In this thesis, I investigate the optic glands from molecular, anatomical, and neurochemical perspectives to uncover its mechanisms of function in octopus maternal behaviors. To identify signaling systems implicated in end-of-life behaviors, I observed behavior in non-mated and brooding female octopuses and performed transcriptomic analyses on their optic glands. I categorized adult life of Octopus bimaculoides females into four distinct phases: non-mated, feeding, fasting, and senescent decline. I found that the optic gland undergoes remarkable molecular changes coincident with transitions between these behavioral stages. These include the dramatic up- and down-regulation of catecholamine, steroid, insulin, and feeding peptide pathways. Transcriptome analyses in other tissues demonstrate that these molecular changes are not generalized markers of senescence, but instead, specific features of optic gland maturation. My findings indicate that, rather than a single “self-destruct” hormone, the optic glands employ multiple pathways as systemic hormonal signals of behavioral control. How these different signals are produced in the optic glands is unclear: they are functionally analogous to the vertebrate pituitary gland, but the optic glands have classically been described as having no internal organization. By contrast, separate populations of pituitary cells produce different hormones that act on the gonads and other downstream targets. To explore the cellular architecture of the optic glands, I used parallel bioinformatic approaches to identify putative markers of the optic gland. I queried the optic gland transcriptomes for transcripts with sequence homology to known invertebrate neuropeptides, and performed a bioinformatic survey on the most enriched transcripts to identify novel prepropeptides. With traditional histochemistry and in situ hybridization, I revealed that the optic gland has regional organization along the oral/aboral axis. At least two major signaling territories divide the optic glands of non-mated females: a steroidogenic region at the most aboral end of the optic gland and a multi-ligand zone that extends to the oral end of the optic gland. The non-steroidogenic, multi-ligand zone includes both neuropeptidergic and catecholaminergic cells. These data draw a functional connection between the optic glands and the pituitary gland: both neuroendocrine organs utilize neuropeptides for signaling. However, unlike the pituitary gland, the optic gland also employs steroid signaling, as evidenced in both the in situ and transcriptomic data. To identify the possible steroid secretions of the optic gland, I performed tandem liquid chromatography-mass spectrometry on extracts from the optic glands of non-mated and mated feeding female octopuses. We identified steroid hormones and found ~200 compounds that showed at least a 4-fold change between non-mated and mated females. The presence of 7-dehydrocholesterol in the optic glands indicates conserved enzymatic activity of the putative cholesterol desaturase we identified bioinformatically. Our study shows, for the first time, that the optic gland produces steroid hormones and demonstrates a link between steroid biosynthesis in the optic glands and octopus behavior. Findings from this thesis represent the first major contribution to the understanding of octopus neuroendocrinology and reproductive behaviors in almost half a century. The methods and results detailed here are applicable beyond octopus biology and offer new approaches to the study of mechanisms underlying natural behaviors in large, invertebrate animals.




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