Relationships between reproductive steroids, glandular microbiota, and volatile chemical signals in naturally cycling versus hormonally contracepted female lemurs

Olfactory communication directs socio-reproductive interaction in animals, but underlying mechanisms remain unclear. Endocrine action and microbial fermentation both influence the manufacture, composition, and expression of vertebrate chemosignals, involving volatile organic compounds (VOCs); however, there has been no integrative investigation of a putative tripart relationship between reproductive hormones, microbes, and VOCs. Our longitudinal experimental study of normative and contracepted females characterizes pairwise and tripart relationships in two scent-marking primates: ring-tailed lemurs ( Lemur catta ) and Coquerel’s sifakas ( Propithicus coquereli ). We used (1) serum enzyme immunoassays to quantify progesterone (P 4 ), estradiol (E 2 ), and the synthetic progestogen, medroxyprogesterone acetate (MPA), (2) Illumina sequencing of the bacterial 16 S rRNA gene to identify microbiota in genital (labial) secretions, and (3) gas chromatography-mass spectrometry to characterize labial VOCs. Despite species differences in hormone concentrations, contraception expectedly muted natural variation in the E 2 /P 4 ratio and introduced initially supraphysiological MPA concentrations. Normative and induced hormonal variation was reflected in the microbial and/or chemical composition of labial secretions; however, predictive power varied by species, potentially reflecting socioecological variation or differences in glandular specialization. These results highlight the importance of cyclical endocrine variation in female reproductive signaling and the overriding effects on VOC manufacture of a disturbed glandular microbiome during contraception.