<p>The gut microbiota is closely associated with seasonal reproductive activity in nonprimate mammals such as muskrats (<i>Ondatra zibethicus</i>) and Daurian ground squirrels (<i>Spermophilus dauricus</i>). Gut microbial dynamics are also correlated with season in male black howler monkeys (<i>Alouatta pigra</i>) and Japanese macaques (<i>Macaca fuscata</i>). However, whether the gut microbiota correlates with mating behavior is unclear. We integrated behavioral (frequency of mating and aggression), physiological (fecal testosterone), and metagenomic (gut microbial community composition and diversity) data to explore the association between gut microbiome and seasonal reproductive activity in wild male Tibetan macaques (<i>Macaca thibetana</i>). We studied ten adult male individuals, and analyzed 26 fecal samples collected during the mating season and 15 collected during the nonmating season. We found no significant differences in alpha diversity (Sobs and Shannon indices) between the two seasons. Nevertheless, PCoA based on Bray–Curtis distances detected significant seasonal differences in gut bacterial community composition and RDA identified mating and aggressive frequencies as the key drivers of community variation. We found a significant negative correlation between gut bacterial richness and mating frequency, while the frequency of both mating and aggression predicted the differentiation of gut microbiome communities between the mating and nonmating seasons. The relative abundances of dominant microbial taxa showed marked seasonal divergence: Actinomycetota and its affiliated <i>Bifidobacterium</i> were significantly enriched during the mating season and positively correlated with mating frequency, whereas <i>Clostridium</i> and <i>Candidatus limimonas</i> showed the opposite abundance patterns. Furthermore, functional genes related to energy accumulation and reproductive activities were enriched in the gut microbiome during the mating season, while we detected enrichment of genes related to basic metabolism in the nonmating season. This study suggests a close link between gut microbiota and mating frequency in terms of community composition, structure, and function, providing valuable insights for further investigation into the reproductive regulation mechanisms of wild primates.</p>

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Exploring the Associations Between the Gut Microbiome and Mating Behavior in Free-ranging Male Tibetan Macaques (Macaca thibetana)

  • Fan Zhang,
  • Chuanpeng Bao,
  • Dongxin Yang,
  • Yue Ling,
  • Ximeng Zhu,
  • Yanan Wu,
  • Yuhao Chen,
  • Xiaojuan Xu,
  • Binghua Sun

摘要

The gut microbiota is closely associated with seasonal reproductive activity in nonprimate mammals such as muskrats (Ondatra zibethicus) and Daurian ground squirrels (Spermophilus dauricus). Gut microbial dynamics are also correlated with season in male black howler monkeys (Alouatta pigra) and Japanese macaques (Macaca fuscata). However, whether the gut microbiota correlates with mating behavior is unclear. We integrated behavioral (frequency of mating and aggression), physiological (fecal testosterone), and metagenomic (gut microbial community composition and diversity) data to explore the association between gut microbiome and seasonal reproductive activity in wild male Tibetan macaques (Macaca thibetana). We studied ten adult male individuals, and analyzed 26 fecal samples collected during the mating season and 15 collected during the nonmating season. We found no significant differences in alpha diversity (Sobs and Shannon indices) between the two seasons. Nevertheless, PCoA based on Bray–Curtis distances detected significant seasonal differences in gut bacterial community composition and RDA identified mating and aggressive frequencies as the key drivers of community variation. We found a significant negative correlation between gut bacterial richness and mating frequency, while the frequency of both mating and aggression predicted the differentiation of gut microbiome communities between the mating and nonmating seasons. The relative abundances of dominant microbial taxa showed marked seasonal divergence: Actinomycetota and its affiliated Bifidobacterium were significantly enriched during the mating season and positively correlated with mating frequency, whereas Clostridium and Candidatus limimonas showed the opposite abundance patterns. Furthermore, functional genes related to energy accumulation and reproductive activities were enriched in the gut microbiome during the mating season, while we detected enrichment of genes related to basic metabolism in the nonmating season. This study suggests a close link between gut microbiota and mating frequency in terms of community composition, structure, and function, providing valuable insights for further investigation into the reproductive regulation mechanisms of wild primates.