This review looks into the phylogeny of spermatogonial stem cells and describes their basic biological features. We are focusing on species-specific differences of spermatogonial stem cell physiology. We propose revised models for the clonal expansion of spermatogonia and for the potential existence of true stem cells and progenitors in primates but not in rodents. We create a new model for the species-specific arrangements of spermatogenic stages which may depend on the variable clonal expansion patterns. We also provide a brief overview of germ cell transplantation as a powerful tool for basic research and its potential use in a clinical setting.

/pdf/spermatogonial-stem-cells-questions-models-and-perspectives-pvenhx6l25.pdf

Spermatogonial stem cells: questions, models and perspectives

Owing to the close phylogenetic relationship of Platyrrhini (New World monkeys) and Catarrhini (Old World monkeys) to man, nonhuman primates are often used as models for the study of male reproductive physiology and endocrinology. This review aims at providing new data and insights into comparative primate spermatogenesis, dealing specifically with quantitative aspects of germinal epithelial organisation and germ cell production, and with the roles of gonadotrophic hormones in this process. Typically, the seminiferous epithelium is composed of specific germ cell associations (spermatogenic stages). In rodents, prosimians and most Catarrhini, tubular cross sections contain a single spermatogenic stage whereas in Platyrrhini, great apes and man multi-stage tubules are present. Since Platyrrhini represent a more basal type of primate, this spermatogenic feature must have developed convergently. The primate multi-stage tubular arrangement was previously believed to be associated with low spermatogenic efficiency. However, recent studies using new methodological approaches and comparing primate species from all taxa have revealed that multistage organisation is compatible with highly efficient spermatogenesis. In fact, meta-analysis demonstrated that the efficiency of spermatogenesis in several nonhuman primate species is comparable to that of rodents which are considered as species with highly efficient germ cell production. The duration of the spermatogenic process was not related to organisation or efficiency of spermatogenesis. Sertoli cell work load was species-specific but had no impact on germ cell numbers and on the efficiency of spermatogenesis. The gonadotrophic hormones, luteinizing hormone (LH) and follicle stimulating hormone (FSH) are the primary regulators of primate testicular function. Recent studies revealed that in New World monkeys chorionic gonadotrophin (CG)--the primate pregnancy hormone--regulates testosterone production instead of LH. Receptor studies demonstrated a dual action of the closely related hormones LH and CG in primates. It is hypothesised that following the divergence of the Platyrrhini lineage from Catarrhini, the LH/CG system evolved independently with ancestral functions of the LH/CG system retained in the neotropical taxa. In summary, key spermatogenic features are preserved across all primate taxa whereas male reproductive endocrinology features appear substantially different in the neotropical primates compared to other primate lineages.

Primate spermatogenesis: new insights into comparative testicular organisation, spermatogenic efficiency and endocrine control.

Gonadal development in immature, pubertal, young mature, and sexually mature male common dolphins (Delphinus delphis) was assessed for 212 dolphins collected between 1991 and 2003. The sample consisted of animals stranded along the Irish and French coasts, and also bycatch samples from Irish and French observer programs. Through histological analysis of the testes, individuals were categorized into reproductive stages by using characteristics of their gonadal morphology. These stages were immature, pubescent, young mature, and sexually mature. Male common dolphins were 102–233 cm in length and 0–28 years of age. Sexually mature individuals were 195–233 cm in length and 8–28 years of age, and the average age at attainment of sexual maturity was 11.86 years. Combined testes weight for mature male dolphins ranged from 0.45 to 5 kg, which is relatively large considering the overall size of the dolphin. Reproductive seasonality was found to occur, as evidenced by marked seasonal changes in both testes weights and cellular activity in testes outside the mating period; the mating period was estimated to take place during May–September. Moderate sexual dimorphism and large testes suggest sperm competition and a promiscuous mating system, with female common dolphins mating with multiple mates.

https://bioone.org/journals/Journal-of-Mammalogy/volume-86/issue-6/1545-1542(2005)86[1247:MSITMC]2.0.CO;2/MATING-STRATEGY-IN-THE-MALE-COMMON-DOLPHIN-DELPHINUS-DELPHIS/10.1644/1545-1542(2005)86[1247:MSITMC]2.0.CO;2.pdf

Mating strategy in the male common dolphin (delphinus delphis): what gonadal analysis tells us

Vertebrate gonads are the sites of synthesis and binding of many peptides that were initially classified as neuropeptides. These gonadal neuropeptide systems are neither well understood in isolation, nor in their interactions with other neuropeptide systems. Further, our knowledge of the control of these gonadal neuropeptides by peripheral hormones that bind to the gonads, and which themselves are under regulation by true neuropeptide systems from the hypothalamus, is relatively meager. This review discusses the existence of a variety of neuropeptides and their receptors which have been discovered in vertebrate gonads, and the possible way in which such systems could have evolved. We then focus on two key neuropeptides for regulation of the hypothalamo-pituitary-gonadal axis: gonadotropin-releasing hormone (GnRH) and gonadotropin-inhibitory hormone (GnIH). Comparative studies have provided us with a degree of understanding as to how a gonadal GnRH system might have evolved, and they have been responsible for the discovery of GnIH and its gonadal counterpart. We attempt to highlight what is known about these two key gonadal neuropeptides, how their actions differ from their hypothalamic counterparts, and how we might learn from comparative studies of them and other gonadal neuropeptides in terms of pharmacology, reproductive physiology and evolutionary biology.

/pdf/neuropeptides-in-the-gonads-from-evolution-to-pharmacology-pl3fwaf4oj.pdf

Neuropeptides in the gonads: from evolution to pharmacology.

Apoptosis and cell proliferation are two important cellular processes known to be involved in the normal functioning of the testis in nonseasonally breeding mammals, but there is some controversy concerning their roles in the gonads of males from seasonally breeding species. We have studied the processes of apoptosis and cell proliferation in the testes of males of the Iberian mole (Talpa occidentalis), a species showing a strict seasonal reproduction pattern. Both males and females are sexually active during the winter and completely inactive in the summer, with two transitional periods, in the autumn and the spring. Adult males from these four reproductive stages were captured, and their testes were immunohistochemically studied for the presence of apoptotic and proliferation molecular markers as well for other testicular and meiotic cell-specific markers. We found that apoptosis varies in a season-dependent manner in the testes of male moles, affecting mainly late zygotene and pachytene cells during the period of sexual inactivity, but it does not differentially affect the number of Sertoli cells. More interestingly, apoptosis is not responsible for the massive germ-cell depletion occurring during mole testis regression. In addition, a wave of spermatogonial cell proliferation appears to restore the number of spermatogonia lost during the period of testis inactivity. According to current knowledge, data from moles indicate that mammals do not form a homogeneous group regarding the mechanisms by which the cell-content dynamics are regulated in the testes of males from seasonally breeding species.

https://bioone.org/journals/biology-of-reproduction/volume-83/issue-1/biolreprod.109.080135/Role-of-Apoptosis-and-Cell-Proliferation-in-the-Testicular-Dynamics/10.1095/biolreprod.109.080135.pdf

Role of Apoptosis and Cell Proliferation in the Testicular Dynamics of Seasonal Breeding Mammals: A Study in the Iberian Mole, Talpa occidentalis

With a view to elucidate seasonal variations in testicular spermatogenesis, quantitative analysis of spermatogenic cells was carried out in non-human primate species viz. rhesus (Macaca mulatta) and bonnet (M. radiata) monkeys during breeding (October-December) and non-breeding (May-June) seasons. The results revealed significant inhibition of testicular germ cell population during non-breeding compared with the breeding period in both the species. Quantitative determination of Sertoli cell-germ cell ratio showed a marked decrease in the number of type A-spermatogonia, spermatocytes (non-pachytene and pachytene) and spermatids (in steps 1-12 of spermiogenesis) in rhesus monkey during the non-breeding period. Bonnet monkeys exhibited the significant decline in the number of primary spermatocytes and spermatids during the non-breeding phase. In addition, average diameter of round seminiferous tubules and nuclear diameter of Leydig cells also decreased significantly in rhesus monkeys. However, bonnet monkeys did not show any significant change in nuclear diameter/morphology of Leydig cells, testicular tubular diameter and number of type A-spermatogoniae. Sertoli cell number did not show any significant change during both breeding and non-breeding periods in both the species. The results of this study indicate a prominent seasonal variation in testicular spermatogenic/Leydig cells in rhesus monkeys than those observed in bonnet monkeys.

S.R. Chowdhury

Papers

Seasonal changes in the seminiferous epithelium of rhesus and bonnet monkeys