Heterosis, or hybrid vigor, is a cornerstone of modern aquaculture; however, the molecular mechanisms underlying this phenomenon, particularly during the critical early developmental stages, remain poorly understood. Hybrid snakehead (Channa maculata ♀ × C. argus ♂) displays marked growth superiority over its parents, making it an ideal model for dissecting the genetic basis of heterosis. In this study, we aimed to identify key regulatory genes and molecular pathways driving the early growth advantage in hybrid snakehead through comparative transcriptomic analysis against its maternal parent, C. maculata. Specifically, we constructed 12 cDNA libraries from whole-body samples at 13 days post-hatching (dph) and muscle tissues at 43 dph for both hybrid and parental groups. High-throughput RNA sequencing yielded approximately 500 million high-quality clean reads, with Q30 percentages consistently above 93.76% and mapping rates to the C. maculata reference genome (GCA_020496755.1) ranging from 68.73% to 95.90%, thereby confirming dataset reliability. Principal component analysis revealed distinct transcriptional profiles between hybrid and parental groups at both developmental stages, with the first principal component (PC1) accounting for 54.70% (13 dph) and 88.80% (43 dph) of total variance, indicating significant, stage-specific transcriptional reprogramming in the hybrid. Differential expression analysis, using a threshold of |log2 (Fold Change)|≥1 and false discovery rate<0.05, identified 721 differentially expressed genes (DEGs; 427 up- and 294 down-regulated) at 13 dph and 385 DEGs (168 up- and 217 down-regulated) at 43 dph in hybrid group. Venn analysis revealed 23 core DEGs shared between both stages, suggesting their sustained importance in growth regulation. Gene ontology enrichment analysis highlighted a dynamic shift in biological functions: at 13 dph, DEGs were predominantly enriched in foundational processes—such as "metabolic process," "cellular process, " "binding," and "catalytic activity" —suggesting an early metabolic priming for rapid growth in hybrid group; at 43 dph, the functional landscape significantly shifted towards "developmental process", "multicellular organismal process", and "transporter activity", reflecting a transition to active tissue construction and morphological development. Kyoto Encyclopedia of Genes and Genomes pathway analysis further emphasized the enrichment of pathways associated with neuro-regulation, feeding behavior, muscle development, and energy metabolism. Ten core candidate genes, including npy, slc25a5, ugp2, obscn, ache, coro1ca, tuba, lmod2, nr4a1, and trim33, were selected, and their expression patterns were successfully validated via qPCR. Notably, the consistent upregulation of neuropeptide Y (npy), a potent appetite stimulator, suggests enhanced feeding motivation. Moreover, the upregulation of genes involved in energy metabolism, such as UDP-glucose pyrophosphorylase 2 (ugp2) and solute carrier family 25 member 5 (slc25a5), indicates an optimized energy supply chain for fueling growth. Concurrently, the downregulation of growth inhibitors—such as tripartite motif-containing 33 (trim33)—may relieve myogenic inhibition. Furthermore, genes crucial for muscle structure and remodeling, including leiomodin-2 (lmod2) and coronin-1A (coro1ca), showed differential expression, underscoring active muscle development. In conclusion, our findings demonstrate that early growth heterosis in hybrid snakehead is not governed by a single master gene but constitutes a complex trait orchestrated by the synergistic action of multiple genes across diverse biological pathways. We propose a model where enhanced neuroendocrine-driven feeding motivation, highly efficient energy metabolism, and accelerated muscle development collectively underpin growth superiority in hybrid group. Our findings provide novel insights into the molecular basis of fish heterosis and establish a scientific basis for marker-assisted selection, genetic improvement, and sustainable aquaculture of snakehead.
| 科 Family | 属数 Number of genus | 种数 Number of species | 占总种数比例 Percentage of total species (%) | 属 Genus | 种数 Number of species | 占总种数比例 Percentage of total species (%) |
|---|---|---|---|---|---|---|
| 鹅膏菌科Amanitaceae | 2 | 11 | 5.26 | 鹅膏菌属 Amanita | 10 | 4.78 |
| 小菇科 Mycenaceae | 2 | 12 | 5.74 | 丝盖伞属 Inocybe | 5 | 2.39 |
| 多孔菌科 Polyporaceae | 8 | 14 | 6.70 | 蜡蘑属 Laccaria | 5 | 2.39 |
| 红菇科 Russulaceae | 3 | 23 | 11.00 | 小皮伞属 Marasmius | 6 | 2.87 |
| 小菇属 Mycena | 11 | 5.26 | ||||
| 光柄菇属 Pluteus | 5 | 2.39 | ||||
| 红菇属 Russula | 17 | 8.13 | ||||
| 栓菌属 Trametes | 5 | 2.39 |