Chemical communication in humans

Pheromones, chemical signals within a species, have been identified in many mammal species. These include rabbits, which use a small aldehyde molecule as their mammary pheromone, and mice, shown to have a variety of protein pheromones such as darcin, secreted by males in their urine scent marks, as well as small molecule pheromones. However, identifying pheromones remains challenging, particularly in mammals. Pheromones occur in a background of hundreds of molecules making up a highly variable chemical profile which differs between individuals. This odour ‘fingerprint’ can be learnt and used, perhaps, to avoid kin as mates. Conspecifics may use some molecules in this complex chemical profile as cues to assess physiological state, much as a mosquito uses carbon dioxide emitted by its mammal host as a cue to locate it. As humans are mammals, we may well have pheromones. Sadly, the story of molecules claimed to be ‘putative human pheromones’ is a classic example of bad science carried out by good scientists. The ‘reproducibility crisis’ in psychology may include some human olfactory research including work on ‘human pheromones’. Ways to create better, more reliable science are being mapped by psychology researchers, with an emphasis on enhancing reproducibility and using approaches from open science.

Because of their impact as pests, and now with growing concern for raising the value of the ecosystem services they offer, we resource insect far more than human semiochemistry. Vertebrate and particularly mammal semiochemistry is in many ways more sophisticated and for human certainly more subtle but we can gain insights from our studies to date on insects. Firstly, for capturing human semiochemicals and where we are concerned with semiochemistry relating to the organism itself, rather than to potentially irrelevant passengers, we are wise to keep away from sites of obvious infection. Of course, it could be valuable to know by smell if a neighbour is infected but it is valuable to target human physiology rather than merely another organism’s metabolic products. Where we can, we should go for organs of production and sometimes these can be cultured but overall we need signals to be captured as they are released without too much variable processing. Ideally, we capture the signals from human individuals in a situation ecologically relevant to the signals under study. We know that for insects there can be a novel chemical composition of a pheromone for the species but for a human pheromone the individual may produce its own pheromonal signature. For insects we can enter the olfactory signal recognition system by electrophysiology and directly monitor chromatographically separated components of captured semiochemicals but this is becoming now more feasible for human semiochemistry using overexpressed human molecular recognition genetics and, while we await perfection in this, we can still exploit the insect system. What would be tragically deceptive though would be to believe that we can manipulate human behaviour in the same way we can the insects’ and there the value of insights from insect semiochemistry ends.

All major primate groups bear scent-producing organs used in intraspecific olfactory communication, but none are as diverse, well-developed or specialized as those displayed by strepsirrhines. In this group, odorants derive from urine, feces, saliva, skin and a suite of scent glands distributed across the body. Each source expresses unique, potentially costly, chemical blends or ‘signatures’ that vary by species and often by signaller sex, reproductive state, identity, breeding history, social status, genotype (diversity, relatedness, MHC composition) or transient condition. Female dominance is even reflected by a sex reversal in glandular and chemical complexity. Whereas some compounds may be endogenously produced and modified (eg via hormones), antibiotic administration and microbial analyses also support the fermentation hypothesis of signal production. The main category of scent source relied upon (ie, excretory vs glandular) broadly differentiates nocturnal from diurnal or cathemeral species, likely reflecting different socioecological demands. Variation in delivery (spatial, seasonal, substrate) or mixing (to create composite unimodal or multimodal signals) may alter signal meaning, longevity or intended audience. Conspecifics possess a functional VNO, investigate scents via olfactory and gustatory means, and are highly sensitive to the chemically encoded messages. This group thus provides unique insights into the olfactory communication system of primates.

Loss of olfactory function is largely found with aging. Such a reduction in olfactory function affects quality of life and enhances likelihood of depressive symptoms. Furthermore, it has been shown that reduction in olfactory function is associated with cognitive impairment and several diseases such as Major Depression or neurodegenerative disorders like Parkinson’s disease and Alzheimer’s disease. Still, a certain portion of this population is not aware of the olfactory loss. Systematic, repeated exposure to odours has been shown to be helpful in older people in terms of a significant improvement of olfactory function, improved verbal function, subjective well-being, and in a decrease of depressive symptoms.

What are the roles of olfaction in the early formation of human infants’ cognition about parents and in promoting parents’ recognition of, and attachment to, infants? On the infants’ side, olfaction sets on in utero. Prenatally-acquired odour memories persist postnatally and modulate selective responses in infants. In parallel to this transnatal odour continuity, mothers convey evolved mammary chemosignals that further boost the vital ingestion of colostrum. In the same time, the mammary niche shapes immediate/deferred olfactory cognitions related to social and biotic (food) items. In addition to arousal regulation and orientation, infant perception of mother’s odour engages then visual cognition of her and others, initiating multisensory social intelligence. On the other side, parents appraise infants’ body odours from birth, perhaps before, leading to the rewarding awareness of their individuality. Later, infant odours are involved in many aspects of adaptive responses underlying the economy of mother-infant exchanges of matters (lactation) and commodities (solace, hygienic care). These include attention, discrimination, recognition, monitoring of infant odour changes, with ensuing engagement of empathetic feelings and onset/maintenance of lactational physiology. Olfaction appears thus significant in turning on, sustaining and, in some cases, disturbing the loop of early mother-infant reciprocity effected in emotion and knowledge, and in behaviour and physiology.

Human parent-child bonding and kin recognition are modulated by olfactory stimuli. This modulation seems age depended: while humans are much in favour of their newborns’ body odour, the enthusiasm seemingly decreases when the children get pubertal. Additionally, studies about mate choice suggest, that humans prefer the smell of an opposite sex partner who differs in terms of genetic HLA profile. The group aimed to integrate those concepts by examining preferences of mother for the body odour of the own, HLA-similar and -dissimilar children over the whole period of childhood and adolescence. In a cross-sectional design, a total of 164 mothers were presented to probes of their own and four other children, aged 0 to 18 years. HLA profiling [HLA A, B, C, DR, DP, DQ] was performed for mothers and children and the estrogen and testosterone concentration was determined for all pre- to postpubertal children. Mothers preferred odours of their own offspring compared to other children for all age groups, except during puberty. During this time, body odour identification ability dropped as well. An interaction showed a negative correlation between maternal pleasantness rating and donors testosterone concentration for the own son and a positive correlation for other boys. HLA similarity had no major impact on the maternal assessment of probes. The data suggests that familiarity, and not genetic similarity, drives body odour preference. In the light of clinical studies, the group assumes that infantile body odour preference is a learned mechanism which is driven by positive parenting experiences.

Major histocompatibility complex (MHC) is a key part of adaptive immune system functioning. There is ample of evidence across various vertebrates indicating preferences for odour of MHC-dissimilar and diverse partners. However, the results of human studies are rather mixed. The current meta-analyses found no systematic preference for MHC-dissimilar partners. Further, there was no effect of hormonal contraception as reported in some early studies. In contrast, there was a moderate but systematic preference for MHC heterozygous partners. Although, MHC similarity may have limited effect on mate choice several studies show that it negatively affects sexual satisfaction. Finally, it was shown that couples sharing high number of MHC alleles are frequently having problems to conceive. The main drawback of majority of available data is that they are based on genetically highly heterogenous populations mainly from Europe and Northern America. Future studies should thus focus on MHC-related mate choice in more homogenous small-scale societies controlling for number of potentially confounding factors such as background genetic make-up.

The sense of smell, which has long been underestimated in humans, is now recognised as being particularly sharp in a broad diversity of contexts. One of the main functions of olfaction in numerous species is social communication. In humans, there is evidence that odours – especially those conveyed by the body – are extremely important in interpersonal relationships. However, many aspects of social communication remain to be explored to fully understand this function in humans. This presentation will focus on within- and between-individual variations in production and perception of odours conveyed by the body (endogenous but also exogenous odours). Current knowledge and new data will be presented regarding differences according to sex, culture, intergroup relations, hormonal status and emotional state. In particular, results involving underexplored categories of compounds (acidic fraction of body odour) and little-known odour sources (other than the axilla) will be put forward. Finally, this presentation will discuss how understanding variations can contribute to elucidate the social function of odours, and will point to current methodological challenges in the field. Propositions will be made for possible directions to take in future research.