Abstract
Hormones of the brain-pituitary-peripheral axis regulate metabolism, gonadal maturation, and growth in vertebrates. In fish, reproduction requires a significant energy investment to metabolically support the production of hundreds of eggs and billions of sperms in females and males, respectively. This study used an LC-MS-based metabolomics approach to investigate seasonally-related changes in metabolic profile and energy allocation patterns in female goldfish liver. We measured basal metabolic profile in female goldfish at three phases of the reproductive cycle, including 1) Maximum growth period in postovulatory regressed phase, 2) mid recrudescence in fish with developing follicles, and 3) late recrudescence when the ovary contains mature ovulatory follicles. We also investigated changes in the liver metabolism following acute treatments with GnRH and GnIH, known to be involved in controlling reproduction and growth in goldfish. Chemometrics combined with pathway-driven bioinformatics revealed significant changes in the basal and GnRH/GnIH-induced hepatic metabolic profile, indicating that metabolic energy allocation is regulated to support gonadal development and growth at different reproductive cycles. Overall, the findings support the hypothesis that hormonal control of reproduction involves accompanying metabolic changes to energetically support gonadotropic and somatotropic activities in goldfish and other oviparous vertebrates.
Highlights
A number of oviparous species, including many fishes, are seasonal breeders and follow cycles of predominantly reproductive and growth phases
Principal Component Analysis (PCA) was conducted on the metabolic data obtained from the Control samples collected from female goldfish at three stages of reproduction
We identified the dominant metabolites in each Partial Least Squared—Discriminant Analysis (PLS-DA) model by selecting the metabolites with Variable Importance in Projection (VIP) score >1 to characterize the phenotypes at the three recrudescence stages investigated (Figure 2)
Summary
A number of oviparous species, including many fishes, are seasonal breeders and follow cycles of predominantly reproductive and growth phases. Vitellogenesis requires a significant metabolic energy allocation (Schneider, 2004; Fernandez-Fernandez et al, 2006; Shahjahan et al, 2014; Ladisa et al, 2021) to support the production of hundreds of mature eggs filled with lipoprotein-filled yolk (Jalabert, 2005) This is critical in oviparous species since embryonic development and early larval stages depend entirely on energy molecules stored in the egg during the maturation (Reading and Sullivan, 2011). We used an LC-MS-based metabolomics approach to investigate the hepatic metabolic profile of adult female goldfish during three stages of the reproductive cycle, including maximum growth period in postovulatory regressed phase, mid recrudescence in fish with developing follicles, and late recrudescence when the ovary contains mature ovulatory follicles. We investigated seasonally related changes in the liver metabolism following acute treatments with GnRH and GnIH, known to be involved in controlling reproduction and growth in goldfish. The present study provides an insight into the metabolic changes accompanying seasonal variation in the reproductive cycle in fish and other seasonally reproducing vertebrates
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