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.

Metabolic capacity is intrinsic to growth performance. To investigate superior growth performance in Nile tilapia, three full-sib families were bred and compared at the biochemical and transcriptome levels to determine metabolic mechanisms involved in significant growth differences between individuals under the same culture environment and feeding regime. Biochemical analysis showed that individuals in the higher growth group had significantly higher total protein, total triglyceride, total cholesterol, and high- and low-density lipoproteins, but significantly lower glucose, as compared with individuals in the lower growth group. Comparative transcriptome analysis showed 536 differentially expressed genes (DEGs) were upregulated, and 622 DEGs were downregulated. These genes were significantly enriched in three key pathways: the tricarboxylic acid cycle (TCA cycle), fatty acid biosynthesis and metabolism, and cholesterol biosynthesis and metabolism. Conjoint analysis of these key pathways and the biochemical parameters suggests that Nile tilapia with superior growth performance have higher ability to consume energy substrates (e.g., glucose), as well as higher ability to biosynthesize fatty acids and cholesterol. Additionally, the fatty acids biosynthesized by the superior growth performance individuals were less active in the catabolic pathway overall, but were more active in the anabolic pathway, and might be used for triglyceride biosynthesis to store excess energy in the form of fat. Furthermore, the tilapia with superior growth performance had lower ability to convert cholesterol into bile acids, but higher ability to convert it into sterols. We discuss the molecular mechanisms of the three key metabolic pathways, map the pathways, and note key factors that may impact the growth of Nile tilapia. The results provide an important guide for the artificial selection and quality enhancement of superior growth performance in tilapia.