Response of optic gland pathways to thermal stress in the reproductive phase of female Octopus maya

Abstract

The octopus optic glands are the source of multiple signalling molecules that control the transitions through different physiological stages, such as maturation, ageing and death. This study focused on the role of the optic glands during the reproductive phase of Octopus maya, investigating the molecular mechanisms that prevent reproduction at elevated temperatures. RNA sequencing was used to analyse and compare optic gland transcriptomic profiles of female O. maya before, during and after egg-laying under optimal and thermal stress (elevated temperature) conditions. Each stage showed well-defined transcriptomic patterns, and all were strongly affected by thermal stress. At optimal temperature, the optic glands contribute importantly to regulating the energetic balance, as suggested by the expression of genes that modulate the metabolic rate, arterial blood pressure and the management of ATP sources in response to food deprivation. At elevated temperatures, the optic glands of mated females (before egg-laying) showed upregulation of genes encoding neuropeptides (FMRF-amide, APGW-amide, PRQFV-amide, FCAP, buccalin and myomodulin) and the dopamine beta-hydroxylase gene. During egg-laying at elevated temperatures, the neuropeptide receptor capaR and the sex peptide receptor were upregulated whereas homologs of fetuin-B and oviduct-specific glycoprotein genes, crucial for fertilization, were downregulated. These changes in optic gland gene expression in O. maya may be the basis for the high-temperature inhibition of egg-laying, previously observed from this octopus species. Furthermore, after egg-laying, during egg incubation thermal stress affected the expression of genes involved in steroid and thyroid hormone biosynthesis and in inflammatory and apoptotic pathways.

Climate change consequences on the systemic heart of female Octopus maya: oxidative phosphorylation assessment and the antioxidant system

“…Despite the additional effects that provoke high temperature on the ovary of O. maya females are still not known, possibly, a heart energetically limited by the high temperature may also produce limitations in pumping oxygenated hemolymph, consequently, in oxygen transport to tissues to satisfy the energetic demands that occur in the ovary and oviductal gland – two critical organs involved in the octopus reproduction ( Domínguez-Estrada et al, 2022 ; Juárez et al, 2022 ; Olivares et al, 2017 ). In this sense, a question arises: How would the systemic heart mitochondria control reproduction in octopus?…”

“…In such cases, thermally stressed females spawn, even when embryos are at thermal risk. However, the results obtained in the laboratory have demonstrated that in temperatures higher than 27°C, the octopus spawn is inhibited, suggesting that other more complex processes regulate O. maya reproduction during thermal stress ( Di Cosmo and Polese, 2014 ; Domínguez-Estrada et al, 2022 ; Juárez et al, 2015 , 2019 ; Ventura-López et al, 2022 ). Considering the previous results, a second question arises: Could the strength of the oxygen flow pumped from the systemic heart be the signal to the brain that triggers the complex regulatory mechanisms directed to preserve the embryos’ integrity, inhibiting spawning at high temperatures?…”

“…The results obtained in the present study show that at 26°C cardiac mitochondria of this acclimation group (26°C) have the highest State 3 respiration, indicating that this temperature is where the cardiac activity is the highest (maximum activity of the proton transport chain and ATP production) and consequently for the transport of oxygen to the rest of tissues, including the reproductive ones. Juárez et al (2015 , 2022 ), Domínguez-Estrada et al (2022) , and Ventura-López et al (2022) studied gene expression in O. maya females exposed to different temperatures. These authors found that in the interval from 24 to 26°C many genes are involved in biochemical processes that ensure the sperm maintenance and egg fertilization success, upregulating in O. maya brain and oviductal gland, probably due to high oxygen availability.…”

“…For its part, we have been observing that O. maya ( Voss and Solís-Ramírez, 1966 ) is particularly sensitive to high temperatures, which suggests that its cardiovascular system could be less tolerant than S. officinalis . It explains, at least in part, the relatively limited thermal tolerance observed in embryos ( Caamal-Monsreal et al, 2016 ; Domínguez-Castanedo et al, 2023 ), juveniles ( Noyola et al, 2013a , b ; Vargas-Abúndez et al, 2023 ) and adults ( Domínguez-Estrada et al, 2022 ; Juárez et al, 2015 , 2016 , 2022 ; Meza-Buendía et al, 2021 ; Pascual et al, 2019 ).…”

Feeding habits and diet composition of Octopus cyanea (Gray, 1849) in Zanzibar waters, Tanzania

“…For example, during the spawning stage, octopuses stop feeding while focusing exclusively on laying and caring for eggs (Anderson et al, 2002). During this period of no or less feeding, octopuses rely on energy in the form of adenosine triphosphate (ATP) from body reserves (Domínguez-Estrada et al, 2022). Because an excessive amount of ATP is required throughout the brooding period, their muscles deteriorate and animals become physically less active, hence unable to hunt (Meza-Buendía et al, 2021).…”