Microsmatic primates revisited: Determining the importance of olfaction in primate communication
The EU-funded project Microsmatic primates revisited: Determining the importance of olfaction in primate communication (PrimOlf) is based at Durham University, and carried out in cooperation with the Primate Centre, CNRS (France), and the Rosalind Franklin Science Centre, University of Wolverhampton.This is the first detailed study of olfaction in sexual communication in Old World primates, and the first to integrate information concerning all the potential signals that females exhibit.
This research project was hosted by the Anthropology Department of Durham University. Dr Stefano Vaglio was the fellow experienced researcher and Prof Jo Setchell was the scientist in charge of the supervision of the project.
The data collection activity involved four research assistants: Rosanna Consiglio (Canada), Kerstin Stucky (Germany), Ayong Julia Kim (USA) and Patrick Neilands (UK). The data analysis involved four research interns: Sarah Howard (Durham University), Maria Rodriguez Villanueva (Universidad Autónoma de Madrid), Louise Ducroix (Universite` Paris Nord) and Lauren Woodland (Durham University). The data analysis involved also two research interns: Camilla Barker (Durham UNiversity) and Kirsten Abbott (University of Wolverhampton).
This research was supported by a Marie Curie Intra European Fellowship within the 7th European Community Framework Programme (Grant Agreement Number: PIEF-GA-2012-327083), the Anthropology Department's 2015 Research Fund (Durham University), the academic spin-off company CarbonSinkGroup srl (Florence University) and the Faculty of Science and Engineering's 2016 Annual Funding Competition (University of Wolverhampton).
Primates are traditionally considered to be microsmatic, with decreased reliance on olfactory senses in comparison to other sensory modalities such as vision. This is particularly the case for Old World monkeys and apes (catarrhines). However, some catarrhines possess scent-glands, suggesting that they do communicate via odour. The major histocompatibility complex (MHC) is an extraordinarily diverse cluster of genes that play a key role in the immune system. MHC gene products are also found in various body secretions, leading to the suggestion that MHC genotypes are linked to unique individual odourtypes that animals use to assess the suitability of other individuals as potential mates or social partners.
Previously (Setchell et al. 2010; 2011) we investigated the volatile components of mandrill odour and the relationship between chemical odour profiles and genotype in a semi-free-ranging population of mandrills (Mandrillus sphinx) in Gabon. We compared odour profiles with features of the signaler using principle components and discriminant function analysis and found that volatile profiles convey both variable (age, dominance rank in males) and fixed (sex, possibly individual identity) information about the signaler. An odour profile that signals sex, age and rank, combined with increased motivation to scent-mark and increased production of secretion in high-ranking males leads to a potent signal of the presence of a dominant, adult male with high testosterone levels in the dense rain-forest. This may be particularly relevant in the dense Central African rain forest. Moreover, odour profiles were not linked to the possession of particular MHC supertypes. Sex influenced some measures of odour diversity and dominance rank influenced some measures of odour diversity in males, but not in females. Odour similarity was strongly related to similarity at the MHC. These previous results suggest that odour provides both a cue of individual genetic quality and information against which the receiver can compare its own genotype to assess genetic similarity. These findings highlight the importance of selecting a reproductive partner with compatible genes, emphasise the importance of olfactory cues in primate reproduction, and, due to the similarity to those found in other mammals and in primates that are more distantly related to humans, suggests a broader role for odour in primate communication and mate choice than is currently recognised.
Female primates signal impending ovulation with a suite of sexual signals. Increasing numbers of studies are investigating the function of these signals and in particular the relationships among female signals, the timing of the fertile period, and male sexual behaviour. However, these studies have focused on visual, and to a lesser extent, acoustic signals, neglecting olfactory signals. Moreover, despite good theoretical reasons to expect that different modes of signalling communicate different information, to different male audiences, most studies to date have studied only one or two modes of signalling.
We aim to investigate the information content of female olfactory signals in captive baboons (Papio anubis), and relate these to the female sexual cycle and the fertile period (determined using progesterone and oestrogen levels, measured in saliva, as well as the cytological evaluation of vaginal swabs), other female sexual signals (acoustic, behavioural and visual), and male behaviour.
The project will contribute to: our understanding of (i) olfactory communication in primates that, like humans, have traditionally been considered as “microsmatic”,(ii) the information that females provide to different males concerning their fertility, and(iii) the role of multiple signals in mate choice; the development of a model with potential practical consequences for humans.
We studied 15 baboons (three adult males and 12 adult females) living in four social groups housed at the CNRS Primate Centre, Rousset-sur-Arc (France).
First, we trained these females, both to lick a synthetic swab (saliva sampling) and to present their sexual swelling allowing the vaginal secretions collection (odour sampling), for 10 weeks by using the positive reinforcement training technique. This training made possible to conduct both odour and hormone sampling and take high quality images of sexual swellings every day for each female. Then, we collected daily behavioural data for each female using 30-minute focal samples and we carried out behavioural, odour and hormone sampling on the same animals for four months.
We measured oestrogen and progesterone levels in saliva at the Durham Endocrinology and Ecology Laboratory using established enzyme-immuno assays (EIA). We implemented the preparation and staining of vaginal smear slides at the CNRS Molecular Biology Laboratory using commercially available kits (RAL Diagnostics), then we carried out the cytological evaluation of slides at the Durham Biosciences Department. We used state-of-the-art digital imaging at the Durham Anthropology Department to quantify swelling size, shape and colour daily for females sampled for odour and behaviour.
We carried out the chemical investigations at the Wolverhampton GC-MS Laboratory, analysing volatile compounds by using solid-phase microextraction (SPME) and gas chromatography-mass spectrometry (GC-MS).
Photos Credits: Romain Lacoste, Fraçois Druelle, and research assistants (in particular, Rosanna Consiglio).
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