Steroid hormones of the octopus self-destruct system

Summary

Among all invertebrates, soft-bodied cephalopods have the largest central nervous systems and the greatest brain-to-body mass ratios, yet unlike other big-brained animals, cephalopods are unusually short lived.^1–5 Primates and corvids survive for many decades, but shallow-water octopuses, such as the California two-spot octopus (Octopus bimaculoides), typically live for only 1 year.^6,7 Lifespan and reproduction are controlled by the principal neuroendocrine center of the octopus: the optic glands, which are functional analogs to the vertebrate pituitary gland.^8–10 After mating, females steadfastly brood their eggs, begin fasting, and undergo rapid physiological decline, featuring repeated self-injury and leading to death.¹¹ Removal of the optic glands completely reverses this life history trajectory,¹⁰ but the signaling factors underlying this major life transition are unknown. Here, we characterize the major secretions and steroidogenic pathways of the female optic gland using mass spectrometry techniques. We find that at least three pathways are mobilized to increase synthesis of select sterol hormones after reproduction. One pathway generates pregnane steroids, known in other animals to support reproduction.^12–16 Two other pathways produce 7-dehydrocholesterol and bile acid intermediates, neither of which were previously known to be involved in semelparity. Our results provide insight into invertebrate cholesterol pathways and confirm a remarkable unity of steroid hormone biology in life history processes across Bilateria.