Chronic Hypoxia Impairs Gamete Maturation in Atlantic Croaker Induced by Progestins through Nongenomic Mechanisms Resulting in Reduced Reproductive Success

Recent studies have shown that chronic hypoxia exposure impairs reproduction in fish by interfering with endocrine function, although the mechanisms of endocrine disruption remain unclear. The effects of chronic exposure (4 or 10 weeks) to hypoxia (dissolved oxygen, DO: 1.7 mg L-1) on gamete maturation and its endocrine control, as well as the consequences for reproductive success, were investigated in Atlantic croaker (Micropogonias undulatus). Circulating levels of the progestin hormone that induces gamete maturation, 17,20 beta,21-trihydroxy-4-pregnen-3-one (20 beta-S), were significantly decreased in croaker of both sexes chronically exposed to hypoxia and were associated with impairment of oocyte meiotic maturation and sperm motility. Interestingly, expression of the novel membrane receptor mediating these nongenomic 20 beta-S actions, membrane progestin receptor alpha (mPR alpha), was significantly decreased on oocyte and sperm plasma membranes of hypoxia-exposed fish. Hypoxia-induced impairment of gamete maturation was accompanied with a dramatic decline in the percent fertilized eggs in a spawning trial. Moreover, the fertilized eggs from hypoxia-exposed donors displayed decreased hatching success and larval survival. The results suggest that nongenomic progestin signaling controlling the final stages of the reproductive cycle in fish is impaired under hypoxic conditions.