A Window of Vulnerability: Chronic Environmental Stress Does Not Impair Reproduction in the Swordfish Xiphias gladius

SIMPLE SUMMARY: The Mediterranean swordfish (Xiphias gladius) stock was affected in last decades from overfish. The evaluation of the cross-talk among metabolism, stress response, immune system and reproduction in immature and mature females could be of great importance. For these reasons, in the present study, by transcriptomic and histological analysis, a deeper insight into the cross-talk among reproduction, metabolism and response to environmental cues across different stages of sexual maturation was provided by the livers of female swordfish. We show that mature females are able to properly reproduce, since they invest a lot of energy in reproduction; however, their detoxification capacity and immune system are compromised as evidenced by transcriptomic and histological approaches. These results suggest that during the reproductive season, mature females may be more susceptible to environmental stress and pollutants than immature ones. ABSTRACT: Xiphias gladius is an important fishing resource. The Mediterranean stock is affected by overfishing and is declining. In this light, the aim of this study was to evaluate the cross-talk among metabolism, stress response, immune system and reproduction in immature and mature females, coupling histological and transcriptomic approaches. The transcriptome of livers from 3 immature and 3 mature females was analyzed using the Artificial Intelligence RNA-Seq. For the histological analysis, ovary and liver samples were collected from 50 specimens caught during the reproductive season in the Mediterranean Sea. A total of 750 genes were differentially expressed between the livers. The gene ontologtabey analysis showed 91 upregulated and 161 downregulated biological process GO terms. Instead, the KEGG enrichment analysis revealed 15 enriched pathways. Furthermore, the binding occurring between estrogen receptors and aryl hydrocarbon receptor nuclear translocator, upregulated in mature females, could be liable for the inhibition of detoxification pathway. Indeed, at the histological level, mature females showed a higher density and number of melanomacrophage centers, biomarkers of stress. The present findings reveal the cross-talk among response to environmental stressors, metabolism and reproduction, highlighting that mature females invest a lot of energy in reproduction instead of immune response and detoxification.