Making “Scents” of the Baboon Vaginal Microbiome

Research on the evolutionary role microbiomes play in their animal hosts has received a great deal of attention over the past few decades. Most of this work has focused on the complex and mutually beneficial relationships between the gut microbiome and animal host. To better understand how these relationships affect animal fitness, research must expand beyond the gut, such as to the reproductive microbiome. The microbial communities in the reproductive tract of animals can play a significant role in host fitness by mediating fertility and pregnancy outcomes and may even play a role in communicating social and reproductive information about their hosts by metabolizing compounds used by the host to communicate olfactorily. This hypothesis was first posited in the 70s as the ‘fermentation hypothesis', yet to date few studies have tested its applicability. To address this gap, my PhD leveraged longitudinal and cross-sectional data on captive and wild primate vaginal odor and microbiomes. I used a solvent-less extraction thermal desorption technique and performed 16S rRNA sequencing to measure the chemical profiles and bacterial compositions of captive and wild primate vaginas, respectively. I then tested whether the chemical composition of vaginal odors and the microbiome were connected, whether they both varied over the ovarian cycle, and whether odors conveyed information about the hosts’ reproductive state by performing behavioral bioassays to measure the response of captive primates to fertile and non-fertile odors.
I found that the vaginal odor and microbiome were correlated and co-varied over the ovarian cycle in the wild, but not in captivity. I then showed that captive primates differentiated between fertile and non-fertile odors. Additionally, I found that the vaginal odor and microbiome were individually unique in our longitudinal dataset, and that captive primates differentiated between the odors of individual females. My work tentatively confirms that the fermentation hypothesis can be applied to primate communication, while demonstrating that captivity may disrupt the ability of females to convey information relative to fitness. This work also demonstrates the importance of using longitudinal datasets, as individual chemical profiles and microbiomes were highly personalized, which must be accounted for when testing whether host-associated microbiomes affect animal fitness. Overall, my work demonstrates the need to expand beyond the gut to additional bodysites to better understand the fitness consequences of host-associated microbiomes.

近年来，关于微生物群在动物宿主进化中所扮演角色的研究备受关注。其中大部分研究聚焦于肠道微生物群与动物宿主之间复杂且互惠互利的关系。为了更深入地理解这些关系如何影响动物的健康状态，研究必须超越肠道，例如拓展至生殖微生物群。动物生殖道中的微生物群落可以通过调节生育力和妊娠结果在宿主健康中发挥重要作用，甚至可能通过代谢宿主用于嗅觉交流的化合物，在传递关于宿主社会和生殖信息方面发挥作用。这一假说最早在20世纪70年代提出，被称为‘发酵假说’，然而截至目前，对其适用性的研究寥寥无几。为了填补这一研究空白，我的博士论文利用了关于圈养和野生灵长类动物阴道气味和微生物群的纵向和横断面数据。我采用了无溶剂提取热脱附技术，并进行了16S rRNA测序，分别测量了圈养和野生灵长类动物阴道的化学特征和细菌组成。随后，我通过行为生物实验，测量圈养灵长类动物对生育和非生育气味的反应，以检验阴道气味的化学组成和微生物群是否相关，它们是否在卵巢周期中发生变化，以及气味是否能够传达关于宿主生殖状态的信息。研究发现，野生灵长类动物的阴道气味和微生物群在卵巢周期中呈现相关性且协同变化，但在圈养状态下则不然。接着，我展示了圈养灵长类动物能够区分生育和非生育气味。此外，我还发现，在我们的纵向数据集中，阴道气味和微生物群各自具有独特性，圈养灵长类动物能够区分不同雌性个体的气味。我的研究初步证实了发酵假说可以应用于灵长类动物的交流，同时表明圈养可能会破坏雌性传达与健康相关信息的能力。这项工作还展示了使用纵向数据集的重要性，因为个体的化学特征和微生物群高度个性化，这在测试宿主相关微生物群是否影响动物健康时必须予以考虑。总体而言，我的研究凸显了超越肠道，拓展至其他身体部位的重要性，以更好地理解宿主相关微生物群的健身后果。