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Sibling sex, but not androgens, shapes phenotypes in perinatal common marmosets (Callithrix jacchus).

ABSTRACT: When offspring share a womb, interactions among fetuses can impart lasting impressions on phenotypic outcomes. Such intrauterine interactions often are mediated by sex steroids (estrogens and androgens) produced by the developing fetuses. In many mammals, intrauterine interactions between brothers and sisters lead to masculinization of females, which can induce fitness consequences. Many litter-bearing primates, though, seem to escape androgen-mediated litter effects, begging why? Here, we investigated how the sex composition (i.e., same- or mixed-sex) of litters influences perinatal outcomes in the common marmoset monkey (Callithrix jacchus), using a combination of physiological, morphological, and behavioural assays. We hypothesized that androgens from male fetuses would mediate developmental differences across litter types. We found that newborns (24-36?hours old) from same- and mixed-sex litters were indistinguishable by urinary androgen profiles, birth weights, morphometrics, and behaviour. However, monkeys born into same- and mixed-sex litters exhibited subtle morphological and neurobehavioral differences later in the perinatal period, independent of their androgen profiles. Our findings suggest that while androgens from male fetuses likely do not organize their siblings' phenotypes, perinatal stimuli may initiate divergent developmental trajectories among siblings, which, in turn, promotes inter-individual variability within families.

SUBMITTER: Frye BM

PROVIDER: S-EPMC6355804 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Sibling sex, but not androgens, shapes phenotypes in perinatal common marmosets (Callithrix jacchus).

Frye Brett M BM Rapaport Lisa G LG Melber Talia T Sears Michael W MW Tardif Suzette D SD

Scientific reports 20190131 1

When offspring share a womb, interactions among fetuses can impart lasting impressions on phenotypic outcomes. Such intrauterine interactions often are mediated by sex steroids (estrogens and androgens) produced by the developing fetuses. In many mammals, intrauterine interactions between brothers and sisters lead to masculinization of females, which can induce fitness consequences. Many litter-bearing primates, though, seem to escape androgen-mediated litter effects, begging why? Here, we inves ...[more]

PMID: 30705381

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Project description:IntroductionThe common marmoset (Callithrix jacchus), a small New World monkey, has been widely used as a biological model in neuroscience to elucidate neural circuits involved in cognition and to understand brain dysfunction in neuropsychiatric disorders. In this regard, the availability of gene expression data derived from next-generation sequencing (NGS) technologies represents an opportunity for a molecular contextualization. Sexual dimorphism account for differences in diseases prevalence and prognosis. Here, we explore sex differences on frontal cortex of gene expression in common marmoset's adults.MethodsGene expression profiles in six different tissues (cerebellum, frontal cortex, liver, heart, and kidney) were analyzed in male and female marmosets. To emphasize the translational value of this species for behavioral studies, we focused on sex-biased gene expression from the frontal cortex of male and female in common marmosets and compared to humans (Homo sapiens).ResultsIn this study, we found that frontal cortex genes whose expression is male-biased are conserved between marmosets and humans and enriched with "house-keeping" functions. On the other hand, female-biased genes are more related to neural plasticity functions involved in remodeling of synaptic circuits, stress cascades, and visual behavior. Additionally, we developed and made available an application-the CajaDB-to provide a friendly interface for genomic, expression, and alternative splicing data of marmosets together with a series of functionalities that allow the exploration of these data. CajaDB is available at cajadb.neuro.ufrn.br.ConclusionThe data point to differences in gene expression of male and female common marmosets in all tissues analyzed. In frontal cortex, female-biased expression in synaptic plasticity, stress, and visual processing might be linked to biological and behavioral mechanisms of this sex. Due to the limited sample size, the data here analyzed are for exploratory purposes.

Project description:Social behavior can alter the microbiome composition via transmission among social partners, but there have been few controlled experimental studies of gut microbiome transmission among social partners in primates. We collected longitudinal fecal samples from eight unrelated male-female pairs of marmoset monkeys prior to pairing and for 8 weeks following pairing. We then sequenced 16S rRNA to characterize the changes in the gut microbiome that resulted from the pairing. Marmoset pairs had a higher similarity in gut microbiome communities after pairing than before pairing. We discovered sex differences in the degrees of change in gut microbiome communities following pairing. Specifically, the gut microbiome communities in males exhibited greater dissimilarity from the prepairing stage (baseline) than the gut microbiome communities in females. Conversely, females showed a gradual stabilization in the rate of the gut microbiome community turnover. Importantly, we found that the male fecal samples harbored more female-source gut microbes after pairing, especially early in pairing (paired test, P?<?0.05), possibly linked to sex bias in the frequencies of social behavior. From this controlled study, we report for the first time that pair-living primates undergo significant changes in gut microbiome during pairing and that females transmit more microbes to their partners than males do. The potential biases influencing which microbes are transmitted on the basis of sex and whether they are due to sex biases in other behavioral or physiological features need to be widely investigated in other nonhuman primates and humans in the future.IMPORTANCE In this controlled study, we collected longitudinal fecal samples from 16 male and female marmoset monkeys for 2 weeks prior to and for 8 weeks after pairing in male-female dyads. We report for the first time that marmoset monkeys undergo significant changes to the gut microbiome following pairing and that these changes are sex-biased; i.e., females transmit more microbes to their social partners than males do. Marmosets exhibit pair bonding behavior such as spatial proximity, physical contact, and grooming, and sex biases in these behavioral patterns may contribute to the observed sex bias in social transmission of gut microbiomes.

Project description:Gastrointestinal diseases are the most frequently reported clinical problems in captive common marmosets (Callithrix jacchus), often affecting the health and welfare of the animal and ultimately their use as a research subject. The microbiome has been shown to be intimately connected to diet and gastrointestinal health. Here, we use shotgun metagenomics and untargeted metabolomics in fecal samples of common marmosets collected before, during, and after a dietary transition from a biscuit to a gel diet. The overall health of marmosets, measured as weight recovery and reproductive outcome, improved after the diet transition. Moreover, each marmoset pair had significant shifts in the microbiome and metabolome after the diet transition. In general, we saw a decrease in Escherichia coli and Prevotella species and an increase in Bifidobacterium species. Untargeted metabolic profiles indicated that polyamine levels, specifically cadaverine and putrescine, were high after diet transition, suggesting either an increase in excretion or a decrease in intestinal reabsorption at the intestinal level. In conclusion, our data suggest that Bifidobacterium species could potentially be useful as probiotic supplements to the laboratory marmoset diet. Future studies with a larger sample size will be beneficial to show that this is consistent with the diet change.ImportanceAppropriate diet and health of the common marmoset in captivity are essential both for the welfare of the animal and to improve experimental outcomes. Our study shows that a gel diet compared to a biscuit diet improves the health of a marmoset colony, is linked to increases in Bifidobacterium species, and increases the removal of molecules associated with disease. The diet transition had an influence on the molecular changes at both the pair and time point group levels, but only at the pair level for the microbial changes. It appears to be more important which genes and functions present changed rather than specific microbes. Further studies are needed to identify specific components that should be considered when choosing an appropriate diet and additional supplementary foods, as well as to validate the benefits of providing probiotics. Probiotics containing Bifidobacterium species appear to be useful as probiotic supplements to the laboratory marmoset diet, but additional work is needed to validate these findings.

Dataset Information

Sibling sex, but not androgens, shapes phenotypes in perinatal common marmosets (Callithrix jacchus).

Publications

Sibling sex, but not androgens, shapes phenotypes in perinatal common marmosets (Callithrix jacchus).

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