Fish reproductive biology – Reflecting on five decades of fundamental and translational research

Abstract

Driven by the broad diversity of species and physiologies and by reproduction-related bottlenecks in aquaculture, the field of fish reproductive biology has rapidly grown over the last five decades. This review provides my perspective on the field during this period, integrating fundamental and applied developments and milestones. Our basic understanding of the brain-pituitary-gonadal axis led to overcoming the failure of farmed fish to ovulate and spawn in captivity, allowing us to close the fish life cycle and establish a predictable, year-round production of eggs. Dissecting the molecular and hormonal mechanisms associated with sex determination and differentiation drove technologies for producing better performing mono-sex and reproductively-sterile fish. The growing contingent of passionate fish biologists, together with the availability of innovative platforms such as transgenesis and gene editing, as well as new models such as the zebrafish and medaka, have generated many discoveries, also leading to new insights of reproductive biology in higher vertebrates including humans. Consequently, fish have now been widely accepted as vertebrate reproductive models. Perhaps the best testament of the progress in our discipline is demonstrated at the International Symposia on Reproductive Physiology of Fish (ISRPF), at which our scientific family has convened every four years since the grandfather of the field, the late Ronald Billard, organized the inaugural 1977 meeting in Paimpont, France. As the one person who has been fortunate enough to attend all of these meetings since their inception, I have witnessed first-hand the astounding evolution of our field as we capitalized on the molecular and biotechnological revolutions in the life sciences, which enabled us to provide a higher resolution of fish reproductive and endocrine processes, answer more questions, and dive into deeper comprehension. Undoubtedly, the next (five) decades will be similarly exciting as we continue to integrate physiology with genomics, basic and translational research, and the small fish models with the aquacultured species.

Atresia of ovarian follicles in fishes, and implications and uses in aquaculture and fisheries

“…Crowding factors have been supposed to exert an inhibitory effect on growth and reproduction and to depress heart rate (Pfuderer et al., 1974 ). Sex steroids made hydrophilic through glucuronide and sulphate conjugation and excreted to the water through fish urine, free steroids released through the gills (Zohar, 2021 and references therein cited) as well as prostaglandin F2α (Mylonas et al., 2017 ) are well‐known pheromones that facilitate successful reproduction and spawning by synchronizing reproductive activity. However, to our knowledge, the identity of purported pheromones acting as reproduction inhibitors in high‐density rearing conditions have not been discovered yet.…”

Molecular characterization of gonadotropin subunits (fshβ, lhβ and cgα) of largemouth bass ( micropterus salmoides ) and their expression in response to luteinizing hormone‐releasing hormone analogue and dopamine antagonists

“…Besides, DA was found to inhibit GnRH releasing in goldfish ( Carassius auratus ) (Trudeau, 1997) and inhibit both FSH and LH secretion, but no concomitant effects on GTH synthesis in rainbow trout ( Oncorhynchus mykiss ) (Vacher et al, 2002). DA antagonists (DOM or PIM), which can competitively bind to DA receptor 2 and relieve the inhibitory effect of DA, and are widely used for artificial reproduction in fish (Roche et al., 2018; Zohar, 2021). Combined with DOM and GnRHa treatment, an increase in GtH subunit expression has been reported in zebrafish, sablefish, and catfish ( Heteropneustes fossilis ) (Acharjee et al., 2017; Fontaine et al., 2013; Guzmán et al., 2015).…”

Reproduction of greater amberjack (Seriola dumerili) and other members of the family Carangidae

“…Although not experimentally demonstrated, combining the available endocrine research from other fish and greater amberjack, one can hypothesize that the reproductive dysfunction is related to an insufficient release of LH from the pituitary at the conclusion of oogenesis (Mylonas et al 1997(Mylonas et al , 1998(Mylonas et al , 2010. This in turn is caused by a dysfunctional release of GnRH from the hypothalamus (Zohar et al 2010;Zohar 2020). This hypothesis is in agreement with (i) the evidence that both liver vitellogenin gene expression and oocyte yolk accumulation are not impaired (Pousis et al 2018) and fully vitellogenic oocytes are commonly found in the ovary of captive-reared fish (Mylonas et al 2004;Fern andez-Palacios et al 2015a;Nyuji et al 2016;Zupa et al 2017b;Jerez et al 2018;Pousis et al 2018;Sarih et al 2018;Fakriadis et al 2019Fakriadis et al , 2020aFakriadis et al , 2020b, (ii) the absence of a peak in LH plasma concentration following the increase in pituitary lhb gene expression (Nyuji et al 2016) and (iii) the low capacity of females to complete oogenesis and spawn spontaneously (Jerez et al 2018;Sarih et al 2018).…”