Integration of mRNA and miRNA Profiling Reveals Heterosis in Oreochromis niloticus × O. aureus Hybrid Tilapia

SIMPLE SUMMARY: Hybrid tilapia (Oreochromis niloticus ♀ × O. aureus ♂) are commercially important in China. Because cultured hybrids have superior growth and survival rate relative to the parental stocks, parent species potentially represent model taxa to analyze the molecular mechanisms of hybrid vigor. Comparisons of the growth and hematologic biochemical characters and transcriptional analyses of mRNA and miRNA, approximately 21-nt-long noncoding RNAs that negatively regulate gene expression at the post transcriptional level, were performed in hybrid and parental tilapia stocks to investigate the underlying molecular basis for heterosis. The present study indicated that dominance and overdominance models are widespread in transcriptional and post-transcriptional regulation of genes involved in growth, metabolism, immunity, and antioxidant capacity in hybrid tilapia, thus providing new insights into molecular heterosis in hybrid tilapia and advancing our understanding of the complex mechanisms involved in this phenomenon in aquatic animals. ABSTRACT: 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.