Spermatogenic columns, somatic cells, and the microenvironment of germinal cells in the testes of asteroids

Sixty-seven specimens of the common North Atlantic asteroid, Asterias vulgaris, were collected at seasonal intervals over a 2-year period and their testes observed with both light and electron microscopy. In the germinal epithelium, a predictable series of interactions between versatile somatic cells and germinal cells is repeated annually in relation to sequential events in spermatogenesis. For example, massive proliferation and differentiation of spermatogenic cells depend on the elaboration of thousands of spermatogenic columns, which are distinct cellular subdivisions of the germinal epithelium. Each fully developed column is composed of at least one somatic cell surrounded by ≈︁ 400 germinal cells. Such columns form only after intensive spermatogonial mitosis begins in the germinal epithelium. Single annual periods of spermatogenic proliferation and differentiation are initiated from 1 to 3 months out of phase in different individuals and overlap incompletely. Therefore, it is possible to observe testes that are entirely in the proliferative phase, entirely in the differentiative phase, or in both phases simultaneously. Detailed ultrastructural observations and preliminary autoradiographic data demonstrate that columns maintain their height for a variable period of time as germinal cells are generated near their bases, pass along their lengths, and differentiate near their tips; therefore, simultaneous proliferation and differentiation of more than one generation of germinal cells occur in the same column. Finally, formation of primary spermatocytes ceases basally, (terminating proliferation), and remaining columns degrade completely as germinal cells composing them differentiate or are phagocytized (terminating differentiation and spermatogenesis); resulting spermatozoa ultimately accumulate in the expandable lumen. It is proposed that spermatogenic columns provide the structural basis for organization of the microenvironment of small groups of spermatogenic cells (≈︁ 400 at a time) during proliferation and differentiation. Preliminary evidence from A. vulgaris and other species also suggests that somatic cells are temporally pluripotent and are variously involved in the formation, structure, and activities of columns, in extensive phagocytosis, and probably in contributing intrinsic (e.g., 1-methyl adenine and steroids) and mediating extrinsic (e.g., gamete shedding substance and nutrients) microenvironmental factors influential during spermatogenesis in asteroids. The prodigious spermatogenic capabilities of asteroids apparently depend on the generation of spermatogenic columns, on the progressive interaction of germinal and somatic cells before, during, and after columns form, and on the predictable effects of microenvironmental factors received and interpreted at the structural level of the spermatogenic column.