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

Abstract

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 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 molecular features underlying optic gland function are unknown. Here, we identify major signaling systems of the 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 upregulation and downregulation 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 the optic glands. Our study expands the classic optic gland-pituitary gland analogy and more specifically, it indicates that, rather than a single 'self-destruct' hormone, the maternal optic glands employ multiple pathways as systemic hormonal signals of behavioral regulation.

Cephalopod Senescence and Parasitology

“…For instance, arm regeneration may not occur in injured senescent cuttlefish (Féral 1988) and host defence against parasite infection may be impaired in senescent octopuses (Pascual et al 2010). The presence of 'unhealed wounds' in senescent female octopuses may be possibly related to an impairment of the immune responses (Wang and Ragsdale 2018).…”

“…Behavioural changes are also observed in senescent cephalopods. A recent study with sexually matured female Octopus bimaculoides described four stages of reproductive behavioural stages: (i) non-mated; (ii) feeding; (iii) fasting; and (iv) declining (Wang and Ragsdale 2018). The most remarkable characteristics commonly observed in senescent animals (e.g.…”

“…In the majority of the shallow-water cephalopod species, senescence is a short stage of their lifespan, which takes place at the end of sexual maturity (Tait 1986(Tait , 1987Anderson et al 2002). After mating, female octopuses adopt an 'extreme pattern of maternal care' (Wang and Ragsdale 2018). The mother abstains from food and exclusively takes care of the eggs, which will cost its own life; death usually occurs by the time of the offspring hatching (Wells 1978;Hanlon and Messenger 1996;Anderson et al 2002).…”

Alternative Animal Models of Aging Research

“…Interestingly, parental behavior in octopods depends on a specific organ, the optic gland. During brooding the optic gland induces fasting by expression of steroids and insulin signaling regulators (Wang and Ragsdale, 2018). The removal of optic glands prolongs life and prevents parental care in octopuses (Wodinsky, 1977;Wang and Ragsdale, 2018).…”

“…During brooding the optic gland induces fasting by expression of steroids and insulin signaling regulators (Wang and Ragsdale, 2018). The removal of optic glands prolongs life and prevents parental care in octopuses (Wodinsky, 1977;Wang and Ragsdale, 2018). Furthermore, octopuses are the most highly organized invertebrates: their large neural and sensory systems as well as complex behavior keep gaining researchers' attention (Huffard, 2013).…”