Environment-Dependent Heterosis and Transgressive Gene Expression in Reciprocal Hybrids between the Channel Catfish Ictalurus punctatus and the Blue Catfish Ictalurus furcatus

Abstract

The hybrid between female channel catfish (Ictalurus punctatus) and male blue catfish (Ictalurus furcatus) is superior in feed conversion, disease resistance, carcass yield, and harvestability compared to both parental species. However, heterosis and heterobeltiosis only occur in pond culture, and channel catfish grow much faster than the other genetic types in small culture units. This environment-dependent heterosis is intriguing, but the underlying genetic mechanisms are not well understood. In this study, phenotypic characterization and transcriptomic analyses were performed in the channel catfish, blue catfish, and their reciprocal F1s reared in tanks. The results showed that the channel catfish is superior in growth-related morphometrics, presumably due to significantly lower innate immune function, as investigated by reduced lysozyme activity and alternative complement activity. RNA-seq analysis revealed that genes involved in fatty acid metabolism/transport are significantly upregulated in channel catfish compared to blue catfish and hybrids, which also contributes to the growth phenotype. Interestingly, hybrids have a 40–80% elevation in blood glucose than the parental species, which can be explained by a phenomenon called transgressive expression (overexpression/underexpression in F1s than the parental species). A total of 1140 transgressive genes were identified in F1 hybrids, indicating that 8.5% of the transcriptome displayed transgressive expression. Transgressive genes upregulated in F1s are enriched for glycan degradation function, directly related to the increase in blood glucose level. This study is the first to explore molecular mechanisms of environment-dependent heterosis/heterobeltiosis in a vertebrate species and sheds light on the regulation and evolution of heterosis vs. hybrid incompatibility.

Chromosome-level assembly and annotation of the blue catfishIctalurus furcatus, an aquaculture species for hybrid catfish reproduction, epigenetics, and heterosis studies

“…Genes with immune-related functions account for 40% of the known expanded families, including T-cell receptor delta, lectin, complement control proteins, glucocorticoid receptor, chemokine interleukin 8, CD225/Dispanin, and others. This is consistent with our previous findings that the blue catfish had the highest immune activity compared to the channel and hybrid catfish at 10 months of age [ 19 ], and the gene family expansion may contribute to the superior phenotypes of lysozyme and alternative complement activities in blue catfish. Further understanding of the evolution of immune-related genes will provide valuable information for the genetic enhancement of hybrid catfish in pathogenic disease resistance.…”

“…To assess the quality of the blue catfish reference genome assembly, we compared blue catfish transcriptome and DNA methylome data alignment rate to channel catfish reference genome versus this blue catfish assembly. For RNA-seq, adult liver transcriptome data from our previous research were used with NCBI GEO (Gene Expression Omnibus) databases, accession number GSE186603 [ 19 ]. For DNA methylome data, DNA was extracted from 3 cryopreserved blue catfish sperm samples using AllPrep PowerFecal DNA/RNA Kit (Qiagen, Redwood City, CA, USA) following the manufacturer's protocols.…”

“…In channel–blue catfish hybrids, only C × B hybrids demonstrated heterobeltiosis characteristics [ 15 ], and the superior phenotypes were only observed in pond culture but not in smaller culturing units 1 m 3 or less [ 19 ]. The asymmetric and environment-dependent heterosis remains a mystery in the genetics and evolutionary biology field [ 20 ].…”

Transcriptome Analysis Reveals Key Gene Expression Changes in Blue Catfish Sperm in Response to Cryopreservation

“…Evaluation of RNA quality was conducted using the LabChip GX Touch HT (PerkinElmer, Hopkinton, MA, USA). RNA-seq library construction was performed following the procedure described in our previous publication [ 96 ] with 500 ng of total RNA input. The size distributions of cDNA libraries were checked using the TapeStation 4200 D1000 ScreenTape (Agilent Technologies, Santa Clara, CA, USA), and library concentrations were determined by a Qubit 3.0 Fluorometer (Thermo Fisher Scientific, Waltham, MA, USA).…”

Transcriptome and Genome Analyses Applied to Aquaculture Research

“…Interestingly, heterosis for these hybrids only occurs in small culture units (pond culture) but not in tank culture, being therefore environment-dependent. Wang et al [ 20 ] conducted different morphometric, immune, and metabolic measurements and analyzed through RNA-Seq the differences in the liver transcriptome among channel catfish, blue catfish, and their reciprocal F1s reared in tanks. The results showed that the tank environment resulted in a higher growth performance for channel catfish, which could be related to a lower immune function and a higher expression of genes involved in fatty acid metabolism/transport [ 20 ].…”