Reflections on the evolution of the regulation of spermatogenesis

We have developed the concept that mechanisms evolved very early for the modulation of spermatogenesis in response to changes in the external environment, and that these ancient control mechanisms were retained during subsequent evolution. In nearly all animals, the regulation of germinal cell development is postulated to be mediated through the control of gonadal somatic cell functions, associated with the creation and maintenance of an optimal milieu within the spermary of seminiferous tubule in which gametogenesis takes place. In primitive organisms, a small number of stages intervenes between environmental stimuli and subsequent alteration of gonadal somatic cell functions. In contrast, in more complex organisms, the number of intervening stages is greatly amplified and modulated via neuroendocrine mechanisms involving receptors, transducers, and various sorts of relays and messengers. The evolution of these neural and endocrine controls appears to have occurred in lock-step with the evolution of increasing layers of complexity of regulators of spermatogenesis. This is not unduly surprising, since the requirement to have functionally fertile male and female partners of the same species together at the same time and place would require considerable integration of behavioral and recognition mechanisms during courtship and mating. The nature of these neural mechanisms is likely to prove no less complex than that of mechanisms in the gonad required for successful gamatogenesis. The neuroendocrine regulation of spermatogenesis in starfish and in chordates is postulated to act in a manner completely homologous to the ways in which external environmental stimuli influence spermatogenesis in more primitive organisms. In both sets of cases, the gonadal somatic cells (nurse cells) are the ultimate targets which mediate the effective turning on or turning off of spermatogenesis. The hormone-responsive nurse cells are postulated to achieve this simply by creating a microenvironment in the vicinity of germinal cells which permits the expression of program required for development, or by failing to do so. In mammals, Sertoli cells and peritubular cells, only when optimally stimulated by hormones and paracine factors, are thought to form a functional unit which provides this necessary microenvironment. In less complex organisms, other nurse cell arrangements exist to nourish the syncytia of developing germ cells with the mixture of nutrients, salts, etc. required for a gametogenesis to take place in a protected milieu.