Oxidative stress resistance of the extended longevity phenotype of Drosophila under paraquat exposure is heritable: influence of maternal genotype on the offspring.

Oxidative stress resistance is an important trait that contributes to the long lifespan of Drosophila melanogaster, but its epigenetic inheritance via transgenerational transmission has been poorly studied. In this study, using reciprocal crosses between normal-lifespan (NLS) and long-lifespan (LLS) lines, we investigated the transgenerational inheritance of paraquat-induced oxidative stress resistance across the parental, F1, and F2 generations, assessing survival, locomotor performance, and antioxidant biochemical defenses. The results showed that LLS flies had significantly higher resistance to paraquat than NLS flies, with females being more resistant than males. We also observed a sex-specific maternal effect on female survival, with N♂ × L♀ offspring having significantly lower mortality than L♂ × N♀ offspring in the F1 and F2 generations. Locomotor resilience was found to be the most robust transgenerational maternal effect (in both sexes and generations). Our narrow-sense heritability for negative geotaxis in males provided a measure of differential transgenerational transmission of locomotor resilience through mothers. Among the measured antioxidant defenses, glutathione was the most consistent transgenerational maternal antioxidant trait. N♂ × L♀ offspring had significantly higher glutathione levels than L♂ × N♀ in F1 and F2 generations in both sexes, with positive F2 recombination values, indicating transgenerational amplification of glutathione-based antioxidant capacity. Catalase had near-zero heritability, consistent with its predominantly nuclear regulation. Variance partitioning analysis revealed prominent maternal contributions to ROS, LPO, SOD, and locomotion in the parental generation, which were reduced in subsequent generations. Taken together, these findings indicate that the adaptive stress resistance linked with longevity is heritable in Drosophila in a trait-dependent fashion, predominantly driven by the maternal lineage. Locomotion and glutathione regulation are the most maternally inherited traits, making them the primary subjects of subsequent studies on the cytoplasmic, epigenetic, and mitochondrial pathways that mediate transgenerational stress resistance.