Do apes smell like humans? The role of skin bacteria and volatiles of primates in mosquito host selection

Abstract

Anthropophilic mosquitoes are effective vectors of human disease because of their biting preferences. To find their host, these mosquitoes are guided by human odours, primarily produced by human skin bacteria. By analysing the skin bacterial and skin volatile profiles of humans, bonobos, chimpanzees, gorillas, lemurs and cows, we investigated whether primates that are more closely related to humans have a skin bacterial community and odour profile that is similar to that of humans. We then investigated whether this affected discrimination between humans and closely related primates by anthropophilic and zoophilic mosquitoes that search for hosts. Humans had a lower skin bacterial diversity than the other animals and their skin bacterial composition was more similar to that in other primates than it was to the skin bacteria of cows. Like the skin bacterial profiles, the volatile profiles of the animal groups were clearly different from each other. The volatile profiles of cows and lemurs were more closely related to the human profiles than expected. Human volatiles were indeed preferred above cow volatiles by anthropophilic mosquitoes and no preference was observed when tested against non-human primate odour, except for bonobo volatiles, which were preferred over human volatiles. Unravelling the differences between mosquito hosts and their effect on host selection is important for a better understanding of cross-species transmission of vector-borne diseases.

Differential attraction in mosquito–human interactions and implications for disease control

“…Mosquitoes also react to combinations of volatiles that may act in synergy or antagonize each other [41], and removal or addition of compounds can affect the attractiveness of the blend [42,43]. While mosquito host selection in nature depends on a variety of factors, anthropophilic mosquito species show strong preferences to human odour above other odours such as cattle in laboratory studies [44] and there are clear interspecific differences in volatile profiles [45]. This suggests that variation in VOCs may play a role in anthropophily; however, further research is required to pinpoint which VOCs contribute the most to host selection.…”

“…Interestingly, there are differences in skin microbiome between humans, other primates and cattle, in terms of both diversity and composition [45,81], and this could potentially influence mosquito preference for particular host species. For instance, although less diverse, the human skin microbiome was found to have a higher abundance of Staphylococcus spp., known to be attractive to Anopheles mosquitoes, compared with other apes and monkeys [45,71].…”

Chemical signatures of human odour generate a unique neural code in the brain ofAedes aegyptimosquitoes

“…Human blends contain an array of common volatile compounds that originate from skin secretions, the skin microbiome, or their interaction 13 . They differ consistently from animal blends in the relative abundance of at least two or three components, but quantitative, cross-species comparisons are rare and almost always focus on a single compound 24,26,27,62,63 . We therefore lack a clear, comprehensive picture of the relative ratios and other chemical features mosquitoes may use to discriminate.…”

“…1a–d). The apparent ease with which they distinguish these stimuli is remarkable since vertebrate odours are complex blends of relatively common compounds that are frequently shared across species 13,25–27 . Females require a multi-component blend for strong attraction 28–30 and may discriminate based on the ratios in which different components are mixed 31,32 .…”

Interdisciplinary challenges for elucidating human olfactory attractiveness

“…In humans and other mammals, the study of chemical communication is much more recent than in other organisms such as plants or insects [64]. In the last two decades, the chemical composition of human scents has received increasing interest in areas such as medical diagnosis [65] and disease prevention [66,67], forensics [59,60], emergency search [68], and more occasionally in the field of cognitive psychology and affective neuroscience (e.g. communication of emotions [69,70]).…”