Seasonal rank changes for adolescent and subadult natal males in a free-ranging group of rhesus monkeys

Changes in dominance rank for adolescent and subadult natal males in a semi-free-ranging rhesus macaque group were seasonal. Three 4-year-old natal males of the highest-ranking matriline occupied high ranks in the adult male dominance hierarchy during the premating period. In the mating season they dropped in rank, and this decrement was related to a concomitant drop in their alliances. After the mating season, these males rose in rank along with their two 3-year-old kin to occupy ranks 2–5 and 7–8 in the adult male dominance hierarchy. Three-year-old natal males of matrilines lower ranking than first did not become integrated into the hierarchy at this time.     

Seasonal variations in daily sperm production rate of rhesus and bonnet monkeys

Daily sperm production (DSP) rate was estimated in adult male rhesus and bonnet monkeys to evaluate seasonal changes in the gametogenic activity of the testes. Three monkeys of each species were castrated during breeding and non-breeding seasons and DSP rate was estimated by enumerating the homogenization-resistant spermatid nuclei of steps 13 and 14. Results indicated a significant reduction in the DSP rate per testis during the non-breeding season in two species, along with a marked decline in the testis weight. However, the gametogenic capacity of seminiferous tubules did not appear to be markedly affected during non-breeding season, as the DSP rate per gram parenchyma of testis was only marginally reduced. The seasonal changes in DSP were much more pronounced in the rhesus than in the bonnet monkey. The feasibility of circanual rhythm in DSP of sub-human primates to form a baseline for the study of reproductive function in male is discussed.     

Seasonal breeding in rhesus monkeys: Influence of the behavioral environment

The accepted model of breeding seasonality in rhesus monkeys states that females become reproductively active in response to an environmental cue and that males become sexually active in response to ovulating females. This model must be modified to include direct responses of the male to the physical environment, endocrine responses of males to sexual activity, and responses of the female to the sexual activation of fellow group members. The complex set of social stimuli that influences the breeding readiness of both sexes may serve to delimit more precisely the annual periods of conception and birth than would be the case if each individual responded only to the changing physical environment.     

Seasonal changes in reproductive behavior in two ovariectomized female rhesus monkeys treated year-round with estradiol

Two ovariectomized female rhesus monkeys treated year-round with estradiol-filled capsules were used in hour-long behavioral tests with male rhesus monkeys both in and out of the normal breeding season. The study was designed primarily to test male hormonal responses to copulatory behavior and it was expected that behavior of the females would be essentially the same under both seasonal conditions. Several behaviors of the female, however, were found to fluctuate on a seasonal basis, namely (1) proximity to the male, (2) grooming of the male, (3) sexual presentations, and (4) threatening away (a form of sexual invitation). All of these behaviors, except proximity, were found to be positively correlated with the male partner's testosterone levels before and after the behavior test in the only test condition in which most males ejaculated. The preliminary suggestion is made that these females responded to some cue, either from the environment or from the males, that caused a change in their behavior between breeding and nonbreeding seasons despite the constant hormonal environment provided by the estradiol capsules. Since the same behaviors which were sensitive to seasonal effects were positively correlated with male testosterone levels, it is possible that the male's hormonal status affects affects female behavior.     

An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: a biochemical and molecular perspective

During spermatogenesis in adult rat testes, fully developed spermatids (i.e. spermatozoa) at the luminal edge of the seminiferous epithelium undergo “spermiation” at stage VIII of the seminiferous epithelial cycle. This is manifested by the disruption of the apical ectoplasmic specialization (apical ES) so that spermatozoa can enter the tubule lumen and to complete their maturation in the epididymis. At the same time, the blood–testis barrier (BTB) located near the basement membrane undergoes extensive restructuring to allow transit of preleptotene spermatocytes so that post-meiotic germ cells complete their development behind the BTB. While spermiation and BTB restructuring take place concurrently at opposite ends of the Sertoli cell epithelium, the biochemical mechanism(s) by which they are coordinated were not known until recently. Studies have shown that fragments of laminin chains are generated from the laminin/integrin protein complex at the apical ES via the action of MMP-2 (matrix metalloprotease-2) at spermiation. These peptides serve as the local autocrine factors to destabilize the BTB. These laminin peptides also exert their effects on hemidesmosome which, in turn, further potentiates BTB restructuring. Thus, a novel apical ES-BTB-hemidesmosome regulatory loop is operating in the seminiferous epithelium to coordinate these two crucial cellular events of spermatogenesis. This functional loop is further assisted by the Par3/Par6-based polarity protein complex in coordination with cytokines and testosterone at the BTB. Herein, we provide a critical review based on the latest findings in the field regarding the regulation of these cellular events. These recent findings also open up a new window for investigators studying blood–tissue barriers.     

Morphological pattern of response after administration of procarbazine: Alteration of specific cell associations during the cycle of the seminiferous epithelium of the rat

Procarbazine, an anti-cancer agent, administered intraperitoneally to adult, male rats induced a characteristic morphological pattern of response in the seminiferous epithelium. Seminiferous tubules of rats receiving 100 mg/kg procarbazine and higher dosages displayed spermatids which were less mature than those normally found within seminiferous tubules which show a particular cell association. Early spermatids in steps 1–7 of spermiogenesis appeared arrested in their development and were present in cell associations which had advanced normally. The most probable cause of this apparent germ cell arrest was a retardation of acrosomal development since procarbazine is known to affect RNA and consequently protein synthesis. Other features which indicated defective RNA synthesis were the presence of abnormal spermatid nucleoli and abnormally configured chromatoid bodies. This study demonstrates, in contrast to what is indicated by present dogma, that apparent and temporary germ cell arrest may occur under certain deleterious conditions. It also illustrates that particular cell types within a cell association may be out of synchrony with the remainder of the cells in a cell association.     

Postnatal somatic cell proliferation and seminiferous tubule maturation in pigs: A non-random event

Although seminiferous tubule maturation in horses begins in the central area of the testis, this process is thought to occur randomly throughout the testis in most mammals. Studies in our laboratory revealed that the establishment of spermatogenesis may not be a synchronous event in the testicular parenchyma of pigs. The objectives of the present study were to evaluate the pattern of seminiferous cord/tubule maturation and the morphological and functional characteristics of testicular somatic cells during postnatal development in three regions of the pig testis: a) near the tunica albuginea (TA); b) in the transitional area between the seminiferous tubules and mediastinum (TR); and c) in the intermediate area (ID) between the TA and TR. Based on the diameter of seminiferous cords/tubules, nucleus size of Sertoli cells and fluid secretion, mainly at 90 and 120 d of age, seminiferous tubule maturation was more advanced in the ID and TR. The mitotic activity of Sertoli cells was higher (P < 0.05) in the TR than the ID and TA at 7 and 120 d. Except for the mitotic index of the Leydig cells, which was lower (P < 0.05) in the ID at 7, 30, and 180 d than in the TA and TR, other Leydig cell ebd points, e.g., individual cell size, nuclear volume, and cytoplasmic volume, were consistently higher (P < 0.05) in the ID, suggesting that steroidogenesis was more active in this region during the period investigated. Overall, we inferred that Leydig cells in the ID may play a pivotal role in postnatal testis development in pigs and this type of cell is likely related to asynchronous testicular parenchyma development, with the transitional area providing the primary zone for growth of seminiferous tubules.     

Self-agency in rhesus monkeys

Rhesus monkeys (Macaca mulatta) have shown the ability to monitor their own mental states, but fail the mirror self-recognition test. In humans, the sense of self-agency is closely related to self-awareness, and results from monitoring the relationship between intentional, sensorimotor and perceptual information. Humans and rhesus monkeys were trained to move a computer icon with a joystick while a distractor icon partially matched their movements. Both humans and monkeys were able to monitor and identify the icon they were controlling, suggesting they have some understanding of self-agency.     

Pubertal orchestration of hormones and testis in primates

The term “Puberty”, socially known as “Adolescence” is the transitional period from juvenile life to adulthood with functional maturation of gonads and genital organs. In this process, some remarkable developmental changes occur in morphology, physiology, and behavior leading to reproductive competence. Despite sufficient levels of gonadotropins (luteinizing hormone [LH] and follicle‐stimulating hormone [FSH]), robust spermatogenesis is not initiated during infancy in primates due to the immaturity of testicular Sertoli cells. Recent studies suggest that developmental competence augmenting functional activities of receptors for androgen and FSH is acquired by Sertoli cells somewhere during the prolonged hypo‐gonadotropic juvenile period. This juvenile phase is terminated with the re‐awakening of hypothalamic Kisspeptin/Neurokinin B/Dynorphin neurons which induce the release of the gonadotropin‐releasing hormone leading to reactivation of the hypothalamo‐pituitary‐testicular axis at puberty. During this period of pubertal development, FSH and LH facilitate further maturation of testicular cells (Sertoli cells and Leydig cells) triggering robust differentiation of the spermatogonial cells, ensuing the spermatogenic onset. This review aims to precisely address the evolving concepts of the pubertal regulation of hormone production with the corresponding cooperation of testicular cells for the initiation of robust spermatogenesis, which can be truly called “testicular puberty.”     

Circadian and circannual changes in the testicular function of adult rhesus monkeys

The endocrine and gametogenic status of the testes were studied in 9 healthy adult rhesus monkeys of proven fertility throughout a one-year period. Testosterone levels were estimated by radioimmunoassay in blood samples collected at 4 h intervals over a 24 h period once a month. Semen samples and testicular biopsies were also examined once a month. A well-defined circandian rhythm was evident in serum levels of testosterone. The rhythmicity was less pronounced in February and September. The 24 h mean levels of serum testosterone were high between the months of August to March and low in the months of May to July. All animals did not uniformly respond to electro-ejaculation in April and May. Semen volume and total number of spermatozoa were maximal between September and March and least from April to August. Testicular biopsies indicated that all stages of spermatogenesis were evident between September and March and the spermatogenic activity was less evident between April and August. The contents of Sertoli cells showed a seasonal cyclicity; they were laden with lipid droplets during April to August when spermatogenesis was quiescent and vacuolated during September to March when spermatogenesis was active. These studies indicate that the testing of contraceptive drugs needs to be restricted to months of September to March in male rhesus monkeys otherwise, it is possible that the naturally occurring reproductive quiscence may be attributed to the effect of the drug being tested. The data accrued from the present studies also provide quantitative information on circulating levels of testosterone which could be used as a reference background while evaluating the contraceptive drug-effects in male rhesus monkeys.     

Annual changes in germinal epithelium determine male reproductive classes of the cobia

Five reproductive classes of cobia Rachycentron canadum , caught along the Gulf of Mexico and the south-east Atlantic coast of the U.S.A., are described during the annual reproductive cycle. These are based upon changes in the testicular germinal epithelium and the stages of germ cells that are present: early maturation, mid maturation, late maturation, regression and regressed. During early maturation, the germinal epithelium is continuous from the testicular ducts to the periphery of the testis and active spermatogenesis occurs throughout the testis. In mid maturation, the germinal epithelium near the ducts becomes discontinuous, but it remains continuous distally. In late maturation, a discontinuous germinal epithelium extends all along the lobules to the testicular periphery; lobules are swollen with sperm and there is minimal spermatogenesis. The regression class is characterized by a discontinuous epithelium throughout the testis, sperm storage and widely scattered spermatocysts. Spermatogonial proliferation also occurs along the lobule walls and at the periphery of the testis. In regressed testes, spermatogonia exist only in a continuous or discontinuous germinal epithelium, although residual sperm are nearly always present in the lobules and ducts. The presence or absence of sperm is not an accurate indicator of reproductive classes. At the periphery of the testis in the regression and regressed classes, the distal portions of lobules elongate as cords of cells containing spermatogonia and Sertoli cells. All reproductive classes can be identified in paraffin sections, although plastic sections provide better resolution. Using maturation classes defined by changes in the germinal epithelium to describe testicular development and spermatogenesis gives a more accurate picture than does using the traditional terminology.     

Seasonal changes in epididymis and the effects of FSH and testosterone in the spiny-tailed lizard,Uromastix hardwicki

Seasonal changes in epididymal weight and histology were studied in relation to testicular function in the adult spiny-tailed lizard, Uromastix hardwicki, over a period of 1 year. The eipdidymal weights, tubular diameter, and epithelial height increased in March, reaching a peak in April. This peak coincided with sperm maturation, elevated plasma testosterone levels, and release of sperm into the epididymis. The epididymal weights decreased in May following a sudden regression of the testis early in the month. The epididymal weights decreased further during June and remained low until February. The diameter of the duct and the height of the epithelial cells also decreased in May and the epididymal epithelium maintained a low histological profile from June to February. The fall testicular recrudescence was not accompanied by a change either in the weight or the histological structure of the epididymis. Administration of oFSH (0.1 mg) daily for 7 days during the sexually quiescent period induced a significant increase in the weight of the epididymis and epithelial height of the duct. Administration of testosterone alone, (2.0 mg) daily for the same period and under identical conditions, did not induce a change in the weight of epididymis or its histology. A possible permissive role of gonadotrophin in the hormonal regulation of the lizard epididymis has been suggested.     

Associated endocrine,physiological and behavioral changes in rhesus monkeys after intravenous corticotropin-releasing factor administration

The intravenous (IV) administration of synthetic ovine corticotropin-releasing factor (CRF) (10 and 125 μg/kg) to chair restrained rhesus monkeys stimulated the pituitary-adrenal axis. At these doses, increases in plasma concentrations of adrenocorticotropic hormone (ACTH) and cortisol were associated with blood pressure decreases and behavioral effects. These data demonstrate that synthetic ovine CRF (10 and 125 μg/kg) administered IV to the rhesus monkey results in associated endocrine, physiological, and behavioral changes.     

Seminal parameters in rhesus monkeys under physiological conditions and in studies for male fertility control using FSH antibodies or LH-RH-agonists

To characterize the male rhesus monkey as a nonhuman primate model for human testicular functions, parameters of exocrine and endocrine testicular function were monitored in 16 adult male-rhesus monkeys for 1 and 5 years respectively. Testicular volumes in-season (October–January) were twice as great as in out-of-season animals (March–June). Ejaculations, both spontaneous and electrostimulated, ceased out-of-season. In 37 ejaculates obtained by electrostimulation in-season, sperm counts ranged from 110–1,100 million/ejaculate, 65% of sperm were motile and 60% were normally formed. Testicular histology showed regression of spermatogenesis out-of-season, with the diameter of the tubules being only one third of that in-season. Circannual changes in exocrine testicular function were accompanied by parallel fluctuations in pituitary and endocrine testicular functions, as evidenced by basal hormone levels and the production rate of testosterone, as well as the response to LH-RH throughout the year. As FSH is required for spermatogenesis in rhesus monkeys, we initiated a study on the long-term effects of active immunization against FSH as a possible means of fertility control. After the first 2 years of observation we can conclude that the production of specific antibodies to FSH results in suppression of spermatogenesis (oligospermia and occasional azoospermia) without affecting endocrine function. The lack of adverse side effects may encourage further investigations on this approach to fertility control. LH-RH-agonists exert degenerative effects on testicular function in rats via a down regulation of the pituitary and testis. A 12 week treatment of four adult monkeys in-season with Hoe 766 (Hoechst; 4μg/day for eight weeks, 20μg/day for 4 weeks sc) did not reveal any change in sperm counts or motility, although some pituitary desensitization was evident. It remains to be investigated whether even higher doses may result in a suppression of spermatogenesis.     

The technique of kidney transplantation in rhesus monkeys

The technique of kidney transplantation in rhesus monkeys is described in detail. The rate of successful transplantations can be increased to 90-100% if several technical aspects are considered. These include adequate perfusion of the organ to be preserved, measures to prevent a sharp decrease in body temperature, doing the arterial anastomosis with interrupted sutures and prevention of low blood pressure after revascularization.     

Water metabolic parameter changes in rhesus monkeys during exposure to prolonged restriction of motor activity

The objective of this investigation was to determine the effect of prolonged restriction of motor activity (hypokinesia [HK]) on several parameters of water metabolism in primates. The studies were performed on 12 rhesus monkeys aged 4–5 yr (5.10–6.85 kg) during the hypokinetic period of 90 d and during the prehypokinetic period of 30 d. They were divided into two equal groups: the first group was placed under ordinary vivarium conditions (vivarium control animals) and the second group was subjected to 90 d of HK (hypokinetic animals). For the simulation of the hypokinetic effect, the primates were immobilized on their abdomens in special tables. The legs of the monkeys were immobilized with hip and knee joints extended. The primates retained freedom of movement at elbow, wrist, and ankle. During the preexperimental period of 30 d and during the experimental period of 90 d, the following variables were determined: body weight, total body fluid content, specific total body fluid, mean fluid consumed and eliminated in urine, specific plasma resistance, hematocrit level, and plasma concentrations of sodium (Na) and potassium (K). In the hypokinetic primates, body weight decreased significantly when compared to the controls. Mean fluid intake, total body fluid, and specific total body fluid decreased, whereas mean daily fluid loss and specific mean daily fluid elimination increased significantly. Specific plasma resistance, hematocrit level, and plasma electrolyte concentrations increased significantly when compared to the control primates. It was concluded that prolonged restriction of motor activity induces significant changes in water metabolic parameters of primates leading in decreased total water content of the body.     

Seasonal changes in spermatogenic cell degeneration in the seminiferous epithelium of adult Japanese macaques (Macaca fuscata fuscata)

The degenerating pattern of spermatogenic cells in the seminiferous tubule of Japanese macaques was studied to clarify a relationship between seasonal changes of reproductive performances and cytological findings in the Japanese macaque. For light microscopy, testis samples were obtained from five adult animals by biopsy in April (nonmating season) and October (mating season). For electron microscopy, specimens from four additional macaques were used. Degenerating cells were found in all steps of spermatogenesis. In stages I to V of the cycle of the seminiferous epithelium, morphologically atypical pachytene spermatocytes were observed in 14.7 and 10.0% of the cells in the nonmating and mating seasons, respectively, although the difference in percentage was not significant. Mature spermatids with atypical features in those stages occupied 59.6% of the cells in the nonmating season, which significantly decreased to 34.1% in the mating season. These results imply that the seasonal change of sperm production is related, at least in part, to the process of degeneration of the spermatogenic cells in this species.