Multiple optic gland signaling pathways implicated in octopus maternal behaviors and death

Abstract

0. Summary statementOctopus optic glands employ a multiplex progression of signaling molecules to regulate maternal behaviors.\n\n1. AbstractPost-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 glands importance in regulating maternal behavior, the molecular features underlying optic gland function are unknown. Here, we identify major signaling systems of the Octopus bimaculoides optic gland. Through behavioral analyses and transcriptome sequencing, we report that the optic gland undergoes remarkable molecular changes that coincide with transitions between 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 aging and senescence, but instead, specific features of the optic glands. Our results provide strong evidence for the functional conservation of signaling molecules across evolutionarily distant species. For example, elevated levels of insulin growth factor binding proteins are associated with cachexia-like tissue wasting in flies, humans, and, reported here, octopuses. Our study expands the classic optic gland-pituitary gland analogy and indicates that, rather than a single \"self-destruct\" hormone, the maternal optic glands employ multiple pathways as systemic hormonal signals of behavioral control.