Dosage-Associated Maternal Dominance and Tissue-Specific Paternal Expression in a Triploid Hybrid Between Grass Carp and Yellowcheek

Allopolyploidy can generate rapid phenotypic change, yet its early transcriptomic consequences in a newly generated triploid hybrid remain poorly understood in animals. Here, we establish a sterile triploid hybrid between grass carp (Ctenopharyngodon idella) and yellowcheek (Elopichthys bambusa), designated CCE, using an optimized hydrostatic pressure protocol that achieved 100% triploidy with high embryonic viability. Whole-genome resequencing supported an approximately 2:1 maternal-to-paternal genomic dosage. Transcriptomes from seven tissues revealed that maternal expression-level dominance (ELD-Ci) was the predominant expression-inheritance pattern (63.7–84.2%), consistent with a passive, dosage-dependent mode of regulation. Paternal expression-level dominance (ELD-Eb) was detected in all tissues but with marked tissue specificity: most ELD-Eb genes in the liver and muscle showed expression levels similar to those of the paternal yellowcheek parent before hybridization (96.2% and 72.8%, respectively), whereas the brain and hypothalamus contained more ELD-Eb genes not directly explained by parental differences. Finally, in the gut, CCE had shorter villi than both parents, a thicker muscularis layer than both parents, and fewer goblet cells than Eb. Genes related to digestion, absorption, and nutrient transport were more highly expressed in Eb and retained an Eb-like expression pattern in CCE. By contrast, several smooth muscle-related genes, including myh14 and smtnl1, showed non-additive upregulation beyond the parental range, in parallel with the thickened muscularis layer. Together, these findings provide new insights into how parental genome dosage and tissue-specific regulation shape gene expression divergence in newly formed animal allopolyploids.