Proteomic analysis of the zone of degeneration at the mitosis-meiosis transition stage in wild-caught male catshark (Scyliorhinus canicula), correlated with an unusually high-water temperature in the English Channel.

In the context of current global change, variations in water temperature are one of the environmental conditions with serious consequences for marine life, including reproductive processes. In the small spotted catshark Scyliorhinus canicula, spermatogenesis occurs in spermatocysts composed of synchronously developing germ cells associated with Sertoli cells, forming a zonal arrangement of the spermatogenic wave. Male catsharks are known to show little to no seasonal variation in spermatogenesis, unlike other sharks that may have a seasonal break at the spermatogonia-primary spermatocyte transition, creating a zone of degeneration (ZD). Unexpectedly, an unusually high number of male catsharks, collected in the eastern English Channel in September 2022, exhibited a ZD. Analysis of bottom water temperatures indicated that the warmest period, from July to September 2022, was higher than the average for previous years. To further explore the biological perturbations associated with the ZD of the testis, a histological description and a comparative proteomic analysis of the ZD with a zone of intact mitosis-meiosis transition were performed. The results showed that only the spermatogonia at stages II to IV were degenerating, as well as their associated Sertoli cells, while the rest of the testicular tissue appeared not impacted. This spermatogonia-specific degeneration was also supported by the proteomic analysis, which showed that only 20% (1565 proteins) of the identified proteins presented a change in abundance. Based on functional annotations, the comparative proteomic analysis revealed cell cycle disruption, impaired DNA damage repair, apoptosis and stimulated lipid metabolism. In addition, follicle-stimulating hormone and luteinizing hormone receptors were upregulated in the ZD. In conclusion, the results showed a correlation between high water temperatures and an arrest of spermatogenesis in S. canicula, with implications for the conservation of elasmobranchs.