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

Overview

This 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.

This project forms part of a long-term collaboration between JMS, SK and Dr Barthélémy Ngoubangoye (Centre International de Recherches Médicales, Franceville, CIRMF, Gabon) to study the behavioural ecology of a semi-free ranging colony of mandrills (a large species of primate) under naturalistic conditions. It represents a new collaboration with LK to explore the microbial ecology of the colony and benefits from collaboration with Prof Steve Leigh (University of Boulder, Colorado), an expert in the primate microbiome and Dr Jennifer Pratscher (Heriot-Watt University), an expert in microbiome data analysis.

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.

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Image Captions

Mandrill(s) living at the Centre International de Recherches Médicales, Franceville, Gabon.
Bacterial community mapping (from an unrelated sample)

Methodology

Study subjects: Mandrills are large cercopithecine primates that live in the dense rainforests of Gabon, Equatorial Guinea, Cameroon and the Democratic Republic of Congo. The CIRMF mandrill colony was founded in 1983 and currently comprises ~120 animals in three forested enclosures. The animals can be observed daily and are captured annually for a health check at which point we can obtain biological samples.

Biological samples: The student will use existing skin swab samples (n = 110) collected by SK and JMS, complemented with new samples collected from the CIRMF mandrill colony when the animals are anaesthetised for their annual health check. Training and oversight: BN and JMS.

Behavioural sampling: The student will collect behavioural data on dominance ranks and social behaviour in the CIRMF mandrill colony. Training and oversight: JMS.

Laboratory methods: The student will isolate genomic DNA from biological samples that will be sent for high-throughput sequencing (16s/18S/ITS amplicon sequencing and metagenomics). Specific microbial species of interest can be further investigated by qPCR. Training and oversight: LK

Bioinformatics: The student will analyse sequencing data using online tools such as Qiime2, and cloud-based computing tools of CLIMB MRC. The student will attend external training courses and additional training will be provided by a collaborator, Dr Jennifer Pratscher, at Heriot-Watt University. Oversight: LK

Project Timeline

Year 1

6 months in Durham (Oct-Mar): Initial training needs analysis to refine needs. Detailed literature reviews on relevant topics (microbial ecology, animal communication).
6 months in HW (Apr-Sept): initial laboratory training, extract small number of samples for pilot work and quality checks. Submit PhD progression report and undergo examination at 9 months. Extract all remaining samples and send for amplicon sequencing.
Attend data analysis training course (Training in Introduction to Linux for Genomics).
Present project plans and pilot work at national conferences.

Year 2

6 months of bioinformatic analysis for existing samples to address initial research questions and use findings to design additional sample collection (Oct-Mar). Training in metagenomic analysis. Sample collection in Gabon (April-June). Extraction, sequencing and bioinformatic analysis of new samples (July-Sep). Presentations at national conferences.

Year 3

Continue bioinformatic analysis of new samples (Oct-Dec). Use findings to inform further field, laboratory and bioinformatic analyses. Preparation and submission of manuscripts for publication; presentations at international conferences.

Year 3.5

Revision of manuscripts for publication; writing up dissertation; presentations at international conferences; applications for future posts.

Training
& Skills

The student will develop the following key skills and expertise during the project: teamwork and collaboration in the field and laboratory; ethics and scientific integrity; searching and critically assessing the literature; study design; behavioural sampling; biological sampling and shipping samples internationally; laboratory analysis including sample preparation for sequencing (gDNA extraction and nucleic acid quantification) and PCR/qPCR; data handling and bioinformatic analyses; writing scientific reports; presenting at conferences. Opportunities to teach and engage with non-academic audiences are available. Collaboration with Save Gabon’s Primates includes additional relevant training in primate research, welfare and conservation issues in the field.

References & further reading

Setchell et al. 2011. Odour signals major histocompatibility complex genotype in an Old World monkey. Proc. R. Soc. B.278274–280. http://doi.org/10.1098/rspb.2010.0571

Council et al. 2016. Diversity and evolution of the primate skin microbiome. Proc. R. Soc. B. 283:20152586. https://doi.org/10.1098/rspb.2015.2586.

King et al. 2017. Performing skin microbiome research: A method to the madness. J Invest Dermatol. 137:561–568. https://doi.org/10.1016/j.jid.2016.10.033

Leclaire et al. 2017. Social odours covary with bacterial community in the anal secretions of wild meerkats. Sci Rep. 7:3240. https://doi.org/10.1038/s41598-017-03356-x.

Li et al 2018. Microbiota changes in the musk gland of male forest musk deer during musk maturation. Frontiers in Microbiology, https://doi.org/10.3389/fmicb.2018.03048

Maraci et al. 2018. Olfactory communication via microbiota: What is known in birds? Genes. 9:387. doi: 10.3390/genes9080387

Ross et al 2019. The skin microbiome of vertebrates. Microbiome 7, 79 https://doi.org/10.1186/s40168-019-0694-6.

Theis et al. 2013. Symbiotic bacteria appear to mediate hyena social odors. Proc Natl Acad Sci USA. 110:19832–19837. https://doi.org/10.1073/pnas.1306477110

Whittaker et al. 2019. Experimental evidence that symbiotic bacteria produce chemical cues in a songbird. Journal of Experimental Biology 222, jeb202978. https://doi.org/10.1242/jeb.202978

Further Information

Prof Jo Setchell, joanna.setchell@durham.ac.uk
Dr Leena Kerr, leena.kerr@hw.ac.uk

If fieldwork is not possible due to Covid-19, we can work with existing samples and easily develop alternative research questions.

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