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

这个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。动物体内和体表上有多种多样的微生物群（包括细菌、真菌、古生菌、原生动物和病毒）。其中一些微生物是致病的，但许多微生物对宿主有益，在动物生活中起着至关重要的作用。例如，发酵假说认为，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。嗅觉谱甚至可以编码有关基因型的信息，例如，拥有赋予抗病能力的有益基因，如主要组织相容性复合体（MHC）。气味线索通常被假设为支撑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）和亲缘选择（遗传关系在社会行为中的作用）。此外，社会关系可以调节微生物群的获取和共享，影响亲属和非亲属的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，我们对动物自然栖息地微生物组的了解大多是基于粪便样本，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群（和皮肤）不同于其他哺乳动物，这可能是由于文化习俗，包括生活在人造环境中，穿衣服，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来描述生活在自然条件下的山猴（旧大陆的一种大型猴子）皮肤上的微生物群落，并测试发酵假说的预测，即：(i)微生物群落包括可能产生气味分子作为代谢副产物的分类群。（ii）微生物群落的组成可预见地随着宿主的特定特征（主体身份、年龄和成熟阶段、性别、优势等级、生殖状态）、亲缘关系（例如母亲/后代）和其他社会关系（通过对菌落的行为观察来测量）而有所不同。我们还将测试微生物群落随时间、季节、群体之间以及身体不同部位的变化。对于这项研究来说，山魈是一个特别有趣的物种，因为它们是为数不多的拥有气味腺的灵长类动物（旧大陆的猴子和猿，包括人类）之一。胸骨腺分泌物挥发性特征的差异与宿主的特定特征（年龄、性别、优势等级）和MHC基因型有关，这表明气味可能促进该物种的性选择和亲缘选择。此外，山魈的行为表明，尽管它们的交配系统是一夫多妻制的，但它们可以识别父系亲属，这表明气味可能是识别亲属的基础。该项目将有助于我们对哺乳动物微生物组，特别是灵长类动物皮肤微生物组的理解。潜在的未来工作包括将微生物群落组成与气味腺分泌物的挥发性特征和宿主基因型联系起来。

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.