Multi-omics insights into phenotypic traits of butter crab (Scylla paramamosain): Ovarian impairment triggers lipid and carotenoid leakage

Butter crabs (BC), a stress-induced physiological phenotype of Scylla paramamosain , command much higher market prices owing to its unique sensory qualities, yet its formation and phenotypic regulation remains limited. Herein, we integrated multi-modal datase among top-grade BC (TBC), special-grade BC (SBC), first-grade BC (FBC), and normal female mud crabs (NFMC) to systematically unravel the cascade of events underlying BC formation. Phenotypically, BC exhibited grade-dependent orange-yellow pigmentation (strongest in TBC) and gonadosomatic index (GSI) reduction (TBC: GSI ≤ 2; NFMC: GSI ≥ 8). Histologically, TBC ovaries showed severe damage—reduced oocyte density, membrane disruption, vacuolization, and the highest apoptotic index (73.67 ± 6.65%), while FBC ovaries were nearly intact. Ovarian antioxidant (CAT, SOD) and immune (ACP, AKP) activities were progressively exhausted with BC grade (TBC < SBC < FBC < NFMC), accompanied by elevated malondialdehyde (MDA) levels (TBC: 6.17 ± 0.32 nmol/mg prot), while hemolymph presented activated antioxidant defense but suppressed immunity. Lipidomic analysis revealed TBC hemolymph had 7-fold higher total lipids than NFMC, with enriched ovarian-derived phospholipids (PC, PE) and carotenoids (β-carotene: 7.04 ± 0.46 μg/mL vs. NFMC: 0.27 ± 0.01 μg/mL). Transcriptomic and targeted gene expression confirmed TBC ovaries had disrupted oocyte meiosis (downregulated gnrhR , cycA ), enhanced apoptosis (upregulated p53 , caspase3 ), and impaired lipid sequestration (downregulated vtgR , lrp ). Correlation analysis indicated vtgR and abca1 expressions were associated with GSI and hemolymph lipid content. Collectively, this study reveals correlative cascades linking stress-related ovarian damage to elevated hemolymph lipids and carotenoids, which are correlated with the typical phenotypic traits of butter crab. This work provides scientific basis for BC quality evaluation and mud crab aquaculture optimization. • An integrated analytical framework deciphers stress-induced butter crab formation in Scylla paramamosain. • Stress-induced ovarian impairment with oxidative damage and apoptosis drives the butter crab phenotype. • Ovarian dysfunction elevates hemolymph lipids (7-fold) and beta-carotene (26-fold) in top-grade butter crabs. • Key genes ( vtgR , abca1 , p53 ) and pathways link molecular shifts to BC's buttery texture and orange-yellow pigment.