Mandrills and microbes: The role of the skin microbiome in primate communication

该项目结合了微生物和行为生态学来研究动物行为中的关键问题，包括动物如何识别亲属，如何识别潜在的配偶以及社会性的成本和收益。动物的身体上和体内有大量的微生物（包括细菌、真菌、古细菌、原生动物和病毒）。其中一些微生物是致病的，但许多微生物对其宿主有益，并在动物生活中起着至关重要的作用。例如，发酵假说表明，动物气味腺中的微生物群消化动物分泌物，产生气味线索，编码有关其宿主的丰富信息，如个体身份，年龄，性别，生殖状况，健康，饮食，支配地位，亲属关系和社会关系。嗅觉特征甚至可以编码基因型的信息，例如，拥有赋予抗病性的有益基因，如主要组织相容性复合体（MHC）。气味线索通常被假设为支持进化理论的两个关键方面：性选择（通过配偶选择和生殖竞争）和亲属选择（遗传相关性在社会行为中的作用）。此外，社会关系可以调解微生物群的获取和共享，影响亲属和非亲属社会行为的成本和收益。微生物生态学的进步彻底改变了我们对微生物组的理解。然而，我们对自然栖息地动物微生物组的大部分了解都是基于粪便样本，这些样本相对容易收集，而我们对皮肤微生物组的了解要少得多。此外，我们所知道的大部分都是针对人类的，我们知道人类的微生物组（和皮肤）与其他哺乳动物不同，可能是由于文化习俗，包括生活在一个建筑环境中，穿着衣服，使用肥皂。该项目结合了行为观察，生物采样，高通量测序，和生物信息学的方法来研究山鸡皮肤上的微生物群落（一种大型的旧大陆猴子）生活在自然主义的条件下，并测试发酵假说的预测，即：（i）微生物群落包括可能产生作为代谢副产品的气味分子的分类群。(ii)微生物群落的组成可预测地随着宿主特异性特征（受试者身份、年龄和成熟阶段、性别、优势等级、生殖状态）、相关性（例如，母亲/后代）和其他社会关系，通过对殖民地的行为观察来测量。我们还将测试微生物群落随时间、季节、群体之间以及身体部位之间的变化。山海关是这项研究中特别有趣的物种，因为它们是极少数拥有气味腺的卡他延灵长类动物（旧大陆猴和猿，包括人类）之一。从这个胸骨腺的分泌物的挥发性配置文件的差异与主机的特定特征（年龄，性别，优势等级），和MHC基因型，这表明气味可能有助于在这个物种的性和亲属选择。此外，山鸡的行为表明，尽管它们有一夫多妻制的交配系统，但它们可以识别父系亲属，这表明气味可能是亲属识别的基础。该项目将有助于我们了解哺乳动物的微生物组，特别是灵长类动物的皮肤微生物组。未来的工作潜力包括相关的微生物群落组成的气味腺分泌物的挥发性配置文件，和主机的基因型。

SummaryThis project combines microbial and behavioural ecology to examine key questions in animal behaviour, including how animals recognise kin, how they identify potential mates, and the costs and benefits of sociality. Animals host a huge diversity of microbiota (including bacteria, fungi, archaea, protozoa and viruses) on and in their bodies. Some of these microbes are pathogenic, but many are beneficial to their hosts and play crucial roles in animal lives. For example, the fermentation hypothesis suggests that microbiota in animal scent glands digest animal secretions, producing odour cues that encode rich information about their host, such as individual identity, age, sex, reproductive status, health, diet, dominance, kin relationships and social relationships. Olfactory profiles may even encode information about genotype, for example, possession of beneficial genes that confer disease resistance, such as the major histocompatibility complex (MHC). Odour cues are commonly hypothesised to underpin two key aspects of evolutionary theory: sexual selection (via mate choice and reproductive competition) and kin selection (the role of genetic relatedness in social behaviour). Moreover, social relationships can mediate the acquisition and sharing of microbiota, influencing the costs and benefits of social behaviour with kin and non-kin. Advances in microbial ecology have revolutionised our understanding of the microbiome. However, most of our knowledge of the microbiome in animals in their natural habitat is based on faecal samples, which are relatively easy to collect, and we know far less about the skin microbiome. Moreover, much of what we do know is for humans, and we know that the human microbiome (and skin) differs to that of other mammals, probably due to cultural practices including living in a built environment, wearing clothes, and use of soap.This project combines behavioural observations, biological sampling, high-throughput sequencing, and bioinformatics to characterise the microbial communities on the skin of mandrills (a large species of Old World monkey) living under naturalistic conditions, and to test predictions of the fermentation hypothesis, that: (i) The microbial community includes taxa likely to produce odorant molecules as metabolic by-products.(ii) The composition of the microbial community differs predictably with host-specific characteristics (subject identity, age and maturational stage, sex, dominance rank, reproductive status), relatedness (e.g., mother/offspring), and other social relationships, measured via behavioural observation of the colony. We will also test variation in the microbial community over time, with season, between groups, and between sites on the body.Mandrills are a particularly intriguing species for this study because they are one of very few catarrhine primates (Old World monkeys and apes, including humans) to possess a scent gland. Differences in the volatile profile of secretions from this sternal gland are linked to host-specific characteristics (age, sex, dominance rank), and to MHC genotype, suggesting that odour may facilitate sexual and kin selection in this species. Moreover, mandrill behaviour suggests that they can recognise paternal kin, despite their polygynandrous mating system, suggesting that odour may underlie kin recognition.The project will contribute to our understanding of mammalian microbiomes, particularly the primate skin microbiome. Potential for future work includes relating the microbial community composition to volatile profiles of odour gland secretions, and to host genotype.