Heterosis is a widespread biological phenomenon in fishes, in which hybrids have superior traits to parents. However, the underlying molecular basis for heterosis remains uncertain. Heterosis in growth and survival rates is apparent in hybrid tilapia (Oreochromis niloticus ♀ × O. aureus ♂). Comparisons of growth and hematological biochemical characteristics and mRNA and miRNA transcriptional analyses were performed in hybrid and parents tilapia stocks to investigate the underlying molecular basis for heterosis. Growth characteristics and hematological glucose and cholesterol parameters were significantly improved in hybrids. Of 3097 differentially expressed genes (DEGs) and 120 differentially expressed miRNAs (DEMs) identified among three stocks (O. niloticus, O. aureus, and hybrids), 1598 DEGs and 62 DEMs were non-additively expressed in hybrids. Both expression level dominance and overdominance patterns occurred for DEGs and DEMs, indicating that dominance and overdominance models are widespread in the transcriptional and post-transcriptional regulation of genes involved in growth, metabolism, immunity, and antioxidant capacity in hybrid tilapia. Moreover, potential negative regulation networks between DEMs and predicted target DEGs revealed that most DEGs from miRNA-mRNA pairs are up-regulated. Dominance and overdominance models in levels of transcriptome and miRNAome facilitate the integration of advantageous parental alleles into hybrids, contributing to heterosis of growth and improved survival. The present study provides new insights into molecular heterosis in hybrid tilapia, advancing our understanding of the complex mechanisms involved in this phenomenon in aquatic animals.

Hybrid tilapia were produced from hybridization of Nile tilapia (Oreochromis niloticus) and blue tilapia (O. aureus). Comparative transcriptome analysis was carried out on the liver of hybrid tilapia and their parents by RNA sequencing. A total of 2319 differentially expressed genes (DEGs) were identified. Trend co-expression analysis showed that non-additive gene expression accounted for 67.1% of all DEGs. Gene Ontology and KEGG enrichment analyses classified the respective DEGs. Gene functional enrichment analysis indicated that most up-regulated genes, such as FASN, ACSL1, ACSL3, ACSL6, ACACA, ELOVL6, G6PD, ENO1, GATM, and ME3, were involved in metabolism, including fatty acid biosynthesis, unsaturated fatty acid biosynthesis, glycolysis, pentose phosphate pathway, amino acid metabolism, pyruvate metabolism, and the tricarboxylic acid cycle. The expression levels of a gene related to ribosomal biosynthesis in eukaryotes, GSH-Px, and those associated with heat shock proteins (HSPs), such as HSPA5 and HSP70, were significantly down-regulated compared with the parent tilapia lineages. The results revealed that the metabolic pathway in hybrid tilapia was up-regulated, with significantly improved fatty acid metabolism and carbon metabolism, whereas ribosome biosynthesis in eukaryotes and basal defense response were significantly down-regulated. These findings provide new insights into our understanding of growth heterosis in hybrid tilapia.

Luteinizing hormone receptor (LHR) and follicle-stimulating hormone receptor (FSHR) belong to the gonadotropic hormone receptors (GtHR), which are highly expressed in fish gonads and participate in the regulation of fish reproductive activities. Fish gonadal development and gamete maturation are not only regulated by their BPG axis but also affected by natural environmental factors (such as temperature, salinity, pH, nutrients, light, etc.). Nile tilapia (Oreochromis niloticus) is a farmed fish with a short reproductive cycle, fast growth, and high economic value. To study the relationship between gonadotropic hormone receptors (GtHR) and the reproductive activity of Nile tilapia, different oxytocin injection experiments and different temperature treatment experiments were set up, and the expression changes of the GtHR gene in the gonads and the concentration changes of the estradiol (E₂) in the female serum and testosterone (T) in the male serum were determined employing a quantitative RT-PCR assay and enzyme-linked immunosorbent assay (ELISA), respectively. After the injection of oxytocin, with the change of E2 in females and T in males, the FSHR showed an expression pattern of first increase, then decrease, and the LHR showed an expression pattern of first increase, then decrease, and finally increase in the gonads, and the expression level of FSHR and LHR in the injection group was significantly higher than that in the control group at multiple time points; in addition, the expression level of FSHR and LHR in the oxytocin-combination injection group was higher than that in the single injection group. During 28 days of treatment at different temperatures, the sex steroid hormones and GtHR genes also showed regular changes, and the relationship between each group was 28 °C > 32 °C > 24 °C at most time points. According to the research results, it is speculated that FSHR and LHR play an important role in the development of Nile tilapia gonads and participate in the reproductive activities of Nile tilapia. By comparing and analyzing the changes in the sex steroid hormones and GtHR genes in each experimental group, it is speculated that different oxytocin injections could affect the expression of FSHR and LHR genes in Nile tilapia, and the combined effect of oxytocin was better than single oxytocin; the optimum temperature for the reproduction of Nile tilapia is between 28–32 °C. This study provides a theoretical basis for further elucidating the physiological functions and molecular mechanisms of FSHR and LHR and also provides a reference for the research of reproductive regulation in Nile tilapia.