Reproduction and gonadal development in bony fishes

Fish - is an important source of dietary protein around the globe.Aquaculture aims to fulfill the supply gaps created by insufficient number of fish captured from the wild to meet the ever-increasing demand. One approach to address this renewed yield goal is by enhancing reproduction in fish used in aquaculture. However, enhancing reproduction necessitates a deeper understanding of our fundamental knowledge on reproductive endocrinology and physiology of fishes.There are many teleost fishes used for human consumption and the species choice largely depends on regional availability and geographical factors. This creates a need to study individual species to better understand the species-specific biology of reproduction in fishes. In line with this, research by fish reproductive biologists is generating significant new knowledge on fishes of interest in aquaculture, many of which are endemic to specific regions where humans inhabit.

Fishes display a variety of sexual development and reproductive patterns including gonochorism, protandry, protogyny, hermaphroditism, androgenesis and gynogenesis. A variety of genes and endogenous determinants, including hormones as well as transcription factors, play a crucial role in sexual development, gonadal growth, and gametogenesis in fish. In addition, environmental factors including photoperiod and temperature set gonadal growth and recrudescence, thereby entraining the annual/seasonal reproductive cycle. The induction of physiological responses through stress and adaptive behaviour also regulates various reproductive events. The interplay of these factors exists from the development of fish embryo till sexual maturity. Among the numerous determinants studied, the hypothalamo-hypophyseal-gonadal axis has an important role in reproductive success through the feedback regulation during gamete maturation and puberty. In recent years, pioneering research in sex determination, differentiation as well as endocrine disruption using fish models has unravelled various novel molecular mechanisms. Incidentally, piscine sex determining genes outnumber more evolved vertebrate models indicating the phylogenetic significance of studying fish reproduction. Fishes are considered‘champions of sex reversal’ due to their inherent ability of sexual plasticity involving various molecular events at different stages of sexual development. This process is also variable across species thereby fishes seem vulnerable and/or adaptive to endocrine disruption. Hence, understanding the cascade of molecular mechanisms of gonadal development leading to reproductive function is highly challenging with the information available. In view of this, this special issue on “Reproduction and Gonadal Development in Bony Fishes”is a compilation of primary research articles and reviews on reproduction, gonadogenesis and gamete development in bony fishes. This special issue was conceived and compiled as a part of the collaborative activities of Profs.Balasubramanian Senthilkumaran and Suraj Unniappan, under the University of Saskatchewan Global Ambassadors Program (2021–2022)visiting professorship aimed to facilitate the exchange of international experts in their respective disciplines. This issue is a collection offifteen articles from expert fish reproductive biologists around the world. We are delighted that researchers from Canada, China, India, Japan,Malaysia, and the USA have contributed to this special issue. Among the manuscripts received, six were primary research articles and nine were reviews on topics of importance in fish reproduction and aquaculture.All these articles addressed important current concepts in fish reproduction.

The primary research articles explored nuclear receptors, steroidogenic enzymes, factors regulating oocyte maturation, metabolic regulation of endocrine regulators, fish morphology, and the effects of ovariectomy on the brain sex steroid milieu. Yan, Chen, and Qi (2022)detailed their primary research on nuclear receptors (nr) in the ovoviviparous black rock fish,Sebastes schlegelli.They have identified a very conserved nuclear receptor isoforms (alpha and beta) in this teleost.Both nrα and nrβ were found expressed in the testis (in Sertoli cells) and ovary of black rock fish. The testicular expression was linked to the development stages of the gamete with a gradual reduction seen towards late spermatogenesis. Such changes were absent in the ovary. Overall,these results suggest a role for the nrα and nrβ in gamete development and the reproductive physiology and behavior of black rock fish.Chourasia, Chaube, and Joy (2022) provided new information on 2-hydroxyestradiol-17β, an important enzyme in the gonadal steroidogenesis in female cat fishHeteropneustes fossilis. They found both seasonal(reproductive phase) and gonadal developmental stage-specific variations in enzymes that mediate gonadal steroidogenesis. In addition, the estrogen metabolite 2-hydroxyestradiol-17β (2-OHE2) caused signi ficant alterations in ovarian steroidogenesis by promoting C21steroidogenesis and downregulating C19–C18pathways. Using the same species(female cat fish;Heretopneustes fossilis),Mishra and Chaube (2022)showed how brain steroid levels change in response to ovariectomy and estrogen replacement. Their results provide strong evidence for the role of gonadal steroids on brain steroidogenesis, which happens in a sexual-stage specific manner.Hatef and colleagues (2022a) described the roles of kisspeptin on reproduction in zebra fish(Danio rerio)in their first article. Kisspeptin and its receptors were detected in the zebra fish gonads and food deprivation altered its expression in a sex- and tissue-specific manner. Kisspeptin-10 induced germinal vesicle breakdown (oocyte maturation) and upregulated positive endocrine regulators of reproduction in zebra fish ovarian follicles. The same authors(Hatef et al., 2022b), in their second article, discussed the nutrient regulation of ghrelin (a metabolic hormone with reproductive effects)and its receptors in the gonads of zebra fish. The ghrelinergic system(ghrelin and its receptor) was more abundant in the early phases of zebra fish ovarian follicles and the lowest levels were found in the stage 5( final phase) of follicle development. Three or seven days of food-deprivation caused a significant reduction in ghrelin, ghrelin receptor, and ghrelin acyl transferase/GOAT mRNAs in zebra fish gonads in a sex-specific manner. Fadzli, Jaafar, and Piah (2022) presented the first report on the reproductive aspects of a local species, coastal trevally(Carangoides coeruleopinnatus),a fish used as a major dietary protein source and of high commercial value in Malaysia. The major findings of this research include the observation that there is a heavy shift in the sex ratio towards males, length at first maturity was higher in females and that males reached maturity earlier than females, and that energy was mobilized for reproductive functions during the sexually mature stage.Overall, these primary research articles provided incremental knowledge on our fundamental understanding of endocrine regulation of reproduction in commercially important species, or well characterized model organisms such asDanio rerio.

The review articles in this issue covered a broader spectrum of topics.Tilak, Samuel, and Inbaraj (2022) reviewed the factors determining sex determination and differentiation in teleosts. While providing a comparative discussion of sex determination and differentiation, they focused on recent developments in this topic in a gonochoristic fish,mullet(Mugil cephalus).Both genetic and endocrine determinants of both processes were disused in this review. The article from Kobayashi(2022) introduced the regulation of gonadal maturation in a protogynous fish, grouper(Epinephelus species).This review focused on processes underlying gonadal development and gamete maturation, as well as the role of androgen-producing cells that are important for sex change in grouper. Tenugu and Senthilkumaran (2022) provided an in-depth analysis of morphological and molecular changes in sex reversal in bony fishes. This comprehensive review addressed a repertoire of factors including stressors, steroids, and genetic factors that in fluence sex reversal. Begum, Gnanasree, Anusha, and Senthilkumaran(2022) surveyed germ cell markers in teleosts and its interplay, and the practical applications of germ cell markers in fisheries and in the conservation of species. Murugananthkumar and Sudhakumari (2022)provided a summary on the impact of stress on fish reproduction. This review presented stress within the context of stress hormones from both adrenal cortex and medulla. Meanwhile, Roy and Basak (2022) reviewed the implications of xenoestrogens on sex differentiation and reproduction in teleosts. Their primary goal was to introduce and discuss sources of aquatic xenoestrogens and its impact on gonadal and non-gonadal hormones, and reproductive physiology. Saha, Koner, and Sharma(2022) provided insights on how prevalent hypoxia is in aquatic environments, and how it adversely affects all aspects of gonadal development and reproduction in bony fishes. Ghosh, Biswas, and Maitra (2022)discussed the molecular determinants of egg release during ovulation in teleost fishes. They surveyed several factors including steroids, cytokines, growth factors, leukotrienes and nitric oxide and summarized the potential crosstalk within this system. Miyanishi and Nagano (2022),discussed the emerging and established reproductive technologies in Japanese eel(Anguilla japonica)and chub mackerel(Scomber japonicus),two species of commercial importance in Asia. The focus was on hormones and current methods used to enhance seed production in these two species. Collectively, these nine reviews provided a very nice collection of up-to-date reference materials on important topics on fish reproduction.

The original goal set for this issue was ten articles. However, this was exceeded well in advance of the set deadlines. We deeply appreciate the authors who accepted our invitation and decided to make this special issue as the destination of their excellent work. Our deepest appreciation also goes to the chief editors of the journal for accepting and encouraging this special issue, and to the Elsevier staff in charge of this journal for their tremendous support throughout the process. This work was enabled by the significant contributions of all our reviewers who volunteered their time to improve the quality of the articles presented through their rigorous reviews and rescreening of revised manuscripts.It is our sincere hope that this collection will be of interest to fish reproductive physiologists in general, and that it, especially the reviews,will serve as a reference source to beginners and trainees in this field.

Declaration

Authors have nothing to disclose.

Acknowledgments

The research using fish models in SU’s laboratory is funded through a Discovery Grant (RGPIN-2022-04293) from the Natural Sciences and Engineering Research Council of Canada (NSERC) and through the Centennial Enhancement Chair in Comparative Endocrinology at the University of Saskatchewan. BS is a former DBT-Tata Fellow and a visiting professor to the University of Saskatchewan through the Global Ambassadors (Incoming) program to promote scientific interactions and internationalization. BS’s research is funded through grants from the Council of Scientific and Industrial Research, New Delhi, India, and the Science and Engineering Research Board of Department of Science and Technology, New Delhi, India.