The epigonal organ and mature pole of the testis in the recreationally fished blue shark (Prionace glauca): Histochemico-functional correlates

The exact role of the immune system in normal spermatogenesis is poorly understood. The attachment, however, of the lymphomyeloid epigonal organ specifically to the testis's mature pole in many shark species is a curious finding. Unlike the histology of the lymphomyeloid tissues of many other elasmobranchs, the epigonal organ leukocytes of wild-caught blue shark (Prionace glauca), besides exhibiting extensive nuclear heterogeneity, contain some of the largest known granules ever seen in vertebrate white blood cells. It was previously shown that the blue shark epigonal organ remains unremarkable and functionally unchanged despite cestode parasites embedded into its surface, suggesting that it might have other functions in addition to microbial defense. We show here that Prionace epigonal leukocytes shed their granule-laden cytoplasm into the cyst resorption zone (RZ) of the testis, i.e. the region separating the spermatogenic tissue from the epigonal organ, as they begin to migrate into the RZ. Using the immunoreactivity of the conserved transcription factor (proliferating cell nuclear antigen) as marker, it is shown that the granule-lacking leukocytes exclusively infiltrated spermatozoal cysts leftover after the wave of wide-spread multinuclear cell death in summer-breeding males in a seasonally dependent manner. By contrast, Prionace caught 2months later showed fully recovered testes containing numerous completely intact spermatozoal cysts. Conversely, degenerating immature spermatids were gradually phagocytized by their accompanying Sertoli cells, and leukocytes did not infiltrate such cysts. The autoimmune response described here resembles in every aspect the testicular autoimmune response induced experimentally in a teleost fish. These observations suggest functional adaptation of shark leukocytes in response to specific changes in the testicular microenvironment.