Molecular histology of spermatogenesis in the Japanese macaque monkey (Macaca fuscata).

Non-human primates are our closest relatives and therefore offer valuable comparative models for human evolutionary studies and biomedical research. As such, Japanese macaques (Macaca fuscata) have contributed to the advancement of primatology in both field and laboratory settings. Specifically, Japanese macaques serve as an excellent model for investigating postnatal development and seasonal breeding in primates because of their relatively prolonged juvenile period and distinct seasonal breeding activity in adulthood. Pioneering histological studies have examined the developmental associations between their reproductive states and spermatogenesis by morphological observation. However, a molecular histological atlas of Japanese macaque spermatogenesis is only in its infancy, limiting our understanding of spermatogenesis ontogeny related to their reproductive changes. Here, we performed immunofluorescence analyses of spermatogenesis in Japanese macaque testes to determine the expression of a subset of marker proteins. The present molecular histological analyses readily specified major spermatogonial subtypes as SALL4+ A spermatogonia and Ki67+/C-KIT+ B spermatogonia. The expression of DAZL, SCP1, γH2AX, VASA, and calmegin further showed sequential changes regarding the protein expression profile and chromosomal structures during spermatogenesis in a differentiation stage-specific manner. Accordingly, comparative analyses between subadults and adults identified spermatogenic deficits in differentiation and synchronization in subadult testes. Our findings provide a new diagnostic platform for dissecting spermatogenic status and reproduction in the Japanese macaques.

On the sunny side of (new) life: Effect of sunshine duration on age at first reproduction in Japanese macaques (Macaca fuscata).

To produce offspring early in life is energetically demanding and depends greatly on environmental conditions. In female primates, age at first reproduction (AFR) has been associated with social parameters (e.g., population density and social rank), food availability and meteorological conditions (e.g., photoperiod, rainfall patterns, and temperature). Regarding the latter, less attention has been given to the influence of sunshine. In nonhuman primates, including the northern-most distributed Japanese macaque (Macaca fuscata), sunbathing is an effective thermoregulatory strategy to maintain sufficient energy intake during harsh winter months. Furthermore, the energetic value of sunshine and its role in the synthesis of essential vitamins important for sexual development and overall fertility is well investigated using human and animal models. In the present study, we hypothesized that female's AFR is influenced by the amount of sunshine in a semi-free-ranging, provisioned a group of Japanese macaques. To test this, we gathered data on sunshine duration in the year females theoretically experienced the onset of puberty. This phase of the female life cycle is particularly prone to the effects of environmental conditions. In addition to the investigation of sunshine duration and other meteorological conditions (i.e., rainfall and temperature) we controlled for social parameters (i.e., group size and sex ratio) as potential covariates. We found a clear effect of sunshine duration on female AFR: Females who entered puberty in years with more sunshine reproduced for the first time at significantly younger ages than females who experienced less sunshine during this specific period of their development. Possible mechanisms for how the sunshine influences sexual maturation in Japanese macaques are discussed.

The development and ecology of the Japanese macaque gut microbiome from weaning to early adolescence in association with diet.

Previously we have shown that the Japanese macaque gut microbiome differs not by obesity per se, but rather in association with high-fat diet (HFD) feeding. This held true for both pregnant dams, as well as their 1-year-old offspring, even when weaned onto a control diet. Here we aimed to examine the stability of the gut microbiome over time and in response to maternal and postweaning HFD feeding from 6 months of age, and at 1 and 3 years of age. In both cross-sectional and longitudinal specimens, we performed analysis of the V4 hypervariable region of the 16S rRNA gene on anus swabs collected from pregnant dams and their juveniles at age 6 months to 3 years (n = 55). Extracted microbial DNA was subjected to 16S-amplicon-based metagenomic sequencing on the Illumina MiSeq platform. We initially identified 272 unique bacterial genera, and multidimensional scaling revealed samples to cluster by age and diet exposures. Dirichlet multinomial mixture modeling of microbiota abundances enabled identification of two predominant enterotypes to which samples sorted, characterized primarily by Treponema abundance, or lack thereof. Approximating the time of initial weaning (6 months), the Japanese macaque offspring microbiome underwent a significant state type transition which stabilized from 1 to 3 years of age. However, we also found the low abundance Treponema enterotype to be strongly associated with HFD exposure, be it during gestation/lactation or in the postweaning interval. Examination of taxonomic co-occurrences revealed samples within the low Treponema cluster were relatively permissive (allowing for increased interactions between microbiota) whereas samples within the high Treponema cluster were relatively exclusionary (suggesting decreased interactions amongst microbiota). Taken together, these findings suggest that Treponemes are keystone species in the developing gut microbiome of the gut, and susceptible to HFD feeding in their relative abundance.