In F1 hybrids, phenotypic values are expected to be near the parental means under additive effects or close to one parent under dominance. However, F1 traits can fall outside the parental range, and outbreeding depression occurs when inferior fitness is observed in hybrids. Another possible outcome is heterosis, a phenomenon in which interspecific hybrid F1s exhibit improved fitness than both parental species/strains. As an application of heterosis, hybrids between channel catfish females (Ictalurus punctatus) and blue catfish males (Ictalurus furcatus) are superior in feed conversion efficiency, carcass yield, and harvestability, which account for over 50% of the US catfish production. Interspecific hybridization facilitates the combination of genetic material from different species and has proven to be an effective strategy for enhancing phenotypic variability and achieving genetic improvement in catfish. However, deleterious epistatic effects can occur, manifesting as hybrid breakdown in F2 populations. Therefore, to maintain the enhanced production traits in hybrids, it is necessary to rear hybrid F1 fry for each growth cycle. To fully leverage heterosis and develop catfish breeds with stable superior phenotypes, there is a critical need to elucidate the underlying molecular mechanisms of heterosis.
In this study, we performed catfish culture experiments of parental species (blue catfish and channel catfish) and their reciprocal hybrids in both tank/aquarium and earthen pond environments. By longitudinally quantifying fitness parameters such as growth and survival, we confirmed a previously observed phenomenon, which we have formally defined as environment-dependent heterosis. In ponds, hybrids outgrow both parents due to an extra rapid growth phase of (2~4 months) in year 2. This bimodal growth pattern is unique to F1 hybrids in pond culture environment only. In sharp contrast, the same genetic types cultured in tanks display outbreeding depression, where hybrids perform poorly, while channel catfish demonstrates superiority in growth. Throughout this 29-month experiment, we collected 14 tissues samples per fish at the following ages: 3 weeks, 10.8 months, 18.6 months, 21.8 months, 23.5 months, 25 months, and 28.4 months. RNA-seq and DNA methylome sequencing experiments were conducted using selected tissue samples from all four genetic types (blue, channel, reciprocal hybrids) cultured in tank and pond environments. A set of genes in pond-cultured F1 hybrids were identified as upregulated during the critical fast-growing window in the second year, serving as biomarkers and candidate causal genes for environment-dependent heterosis. Additionally, transgressive genes, cis- and trans-regulatory effects, as well as epigenetic differences, were observed when comparing pond vs. tank culture conditions. Our research has pinpointed key genes that may contribute to the superior phenotypes in F1 hybrids, which serve as targets for genetic enhancement through genome editing. Compared to interspecific hybridization, which combines the entire haploid genomes of two species and results in the indiscriminate mixing of all genes, the precise and stable introduction of beneficial traits via genome editing of specific genes holds significant potential for genetic enhancement to improve catfish production.