Genotype-Dependent Transcriptome Divergence Associated With Variation at vgll3 in Juvenile Gilthead Seabream (Sparus...

Early developmental processes significantly influence growth and maturation patterns, aquaculture traits that are critical for physiological adaptation and productivity. The vestigial-like family member 3 gene (vgll3) plays a key role in growth and maturation across diverse taxa, including mammals and teleost fishes. A single-nucleotide polymorphism in vgll3 (SNP_vgll3) shows evidence of selection under aquaculture conditions in gilthead seabream (Sparus aurata), as demonstrated by previous genome scan and targeted transcriptomic (qPCR) analyses. This study investigated how different SNP_vgll3 genotypes (AA, AG and GG) affect gene expression in juvenile gilthead seabream. Genotype-dependent regulatory signatures were identified, as the transcriptome profiles (over 240 quantified transcripts) of the farming-associated GG genotype, which also showed significantly lower vgll3 expression according to qPCR, differed markedly from those of individuals with the AA genotype. Reduced vgll3 expression has been associated with improved body condition and altered maturation timing in other teleost species. Consistent with these findings, our transcriptomic analysis identified differential expression of additional genes involved in growth regulation, developmental processes, and sexual maturation. Specifically, genes such as amh, cacng1b, casq2, tnnc2 and igfn1.1, which are known to play roles in puberty onset and muscle physiology in teleosts, were significantly associated with vgll3 genotype differences in gilthead seabream. Overall, our findings support a conserved role of vgll3 in pathways related to somatic growth and reproductive maturation, though its precise mechanistic function remains to be established. This pronounced genotype-specific transcriptomic divergence, well-documented in humans and plants but still underexplored in non-model species such as fish, raises important questions regarding the underlying evolutionary and developmental mechanisms. Future studies integrating phenotypic variation, tissue-specific expression, and multiple developmental stages will be essential to further resolve the basis of genotype-dependent regulatory effects.