Variation and Interaction of Distinct Subgenomes Contribute to Growth Diversity in Intergeneric Hybrid Fish

Intergeneric hybridization greatly reshapes regulatory interactions among allelic and non-allelic genes. However, their effects on growth diversity remain poorly understood in animals. In this study, we conducted whole-genome sequencing and RNA sequencing analyses in diverse hybrid varieties resulting from the intergeneric hybridization of goldfish (Carassius auratus red var.) and common carp (Cyprinus carpio). These hybrid individuals were characterized by distinct mitochondrial genomes and copy number variations. Through a weighted gene correlation network analysis, we identified 3693 genes as candidate growth-regulating genes. Among them, the expression of 3672 genes in subgenome R (originating from goldfish) displayed negative correlations with body weight, whereas 20 genes in subgenome C (originating from common carp) exhibited positive correlations. Notably, we observed intriguing expression patterns of solute carrier family 2 member 12 (slc2a12) in subgenome C, showing opposite correlations with body weight that changed with water temperatures, suggesting differential interactions between feeding activity and weight gain in response to seasonal changes for hybrid animals. In 40.30% of alleles, we observed dominant trans-regulatory effects in the regulatory interactions between distinct alleles from subgenomes R and C. Integrating analyses of allele-specific expression and DNA methylation data revealed that DNA methylation on both subgenomes shaped the relative contribution of allelic expression to the growth rate. These findings provide novel insights into the interactions of distinct subgenomes that underlie heterosis in growth traits and contribute to a better understanding of multiple allelic traits in animals.