Variability in human attractiveness to mosquitoes

Abstract

Blood-feeding mosquitoes locate humans spatially by detecting a combination of human-derived chemical signals, including carbon dioxide, lactic acid, and other volatile organic compounds. Mosquitoes use these signals to differentiate humans from other animals. Spatial abiotic factors (e.g. humidity, heat) are also used by mosquitoes to find a host. Mosquitoes cause discomfort and harm to humans, being vectors of many pathogens. However, not all humans suffer from mosquito bites with the same frequency or intensity. Some individuals are more attractive to mosquitoes than others, and this has an important impact on the risk of infection by pathogens transmitted by these vectors, such as arboviruses and malaria parasites. Variability in human attractiveness to mosquitoes is partially due to individual characteristics in the composition and intensity in the release of mosquito attractants. The factors that determine these particularities are diverse, modestly understood and still quite controversial. Thus, this review discusses the role of pregnancy, infection with malaria parasites (Plasmodium spp.), skin microbiota, diet, and genetics in human attractiveness to mosquitoes. In brief, pregnancy and Plasmodium infection increase the host attractiveness to mosquitoes. Skin microbiota and human genetics (especially HLA alleles) modulate the production of mosquito attractants and therefore influence individual susceptibility to these insects. There is evidence pointing to a role of diet on human susceptibility to mosquitoes, with some dietary components having a bigger influence than others. In the last part of the review, other factors affecting human-mosquito interactions are debated, with a special focus on the role of mosquito genetics, pathogens and environmental factors (e.g. wind, environmental disturbances). This work highlights that individual susceptibility to mosquitoes is composed of interactions of different human-associated components, environmental factors, and mosquito characteristics. Understanding the importance of these factors, and how they interact with each other, is essential for the development of better mosquito control strategies and studies focused on infectious disease dynamics.

Keywords: Culicidae; Genetics; Human attractiveness; Microbiota; Mosquito; Mosquito bites.

Graphical abstract

Fig. 1

Differences in human susceptibility to mosquitoes due to the intensity in the production of mosquito attractants. Individuals who produce mosquito attractants (kairomones) more intensely may show increased susceptibility to mosquitoes, considering attractiveness and biting rate (A). Alternatively, individuals who produce a reduced amount of mosquito attractants may show reduced susceptibility to mosquitoes (B). Mosquito attractants (e.g. CO₂, lactic acid, ketones, ammonia) are represented by colored dots. The gradual molecular diffusion of volatile compounds is a visual simplification. It is necessary to consider that host-derived volatile kairomones can be dispersed into the air as “packages” and depending on the wind direction. See the main text for references. Human illustrations were obtained from Servier Medical Art (available at https://smart.servier.com, under a Creative Commons Attribution 3.0 Unported License). Mosquito illustrations were obtained from Mind the Graph (available at www.mindthegraph.com).

Fig. 2

Differences in susceptibility to mosquitoes due to differences in the combination (blend) of mosquito attractants. Increased susceptibility to mosquitoes may be due to the production of a combination of mosquito attractants (kairomones) associated with greater mosquito attraction, considering attractiveness and biting rate (A). On the other hand, reduced susceptibility to mosquito attraction and biting rate may be due to the production of a combination of mosquito attractants associated with reduced mosquito attraction. Of note, the production of natural mosquito repellents can also contribute to a reduced human susceptibility to mosquitoes (B). Mosquito attractants are represented by colored dots. The gradual molecular diffusion of volatile compounds is a visual simplification. It is necessary to consider that host-derived volatile compounds can be dispersed into the air as “packages” and depending on the wind direction. See the main text for references. Human illustrations were obtained from Servier Medical Art (available at https://smart.servier.com, under a Creative Commons Attribution 3.0 Unported License). Mosquito illustrations were obtained from Mind the Graph (available at www.mindthegraph.com).

Fig. 3

Factors that interfere with human-mosquito interactions. Skin microbiota, pregnancy, malaria parasites (Plasmodium infection), human genetic factors (e.g. HLA alleles) and diet affect the release patterns of mosquito attractants (kairomones), impacting human-mosquito interactions. In association with mosquito-linked characteristics (e.g. mosquito genetics, infectious status) and environmental components (e.g. wind, humidity), these factors can increase or decrease the susceptibility of an individual to mosquito bites, affecting the risk of infection by pathogens transmitted by mosquitoes (arboviruses, malaria parasites, among others). These factors can affect either the intensity of production or the composition of mosquito attractants. See the main text for references. Human illustration was obtained from Servier Medical Art (available at https://smart.servier.com, under a Creative Commons Attribution 3.0 Unported License). Mosquito and tree illustrations were obtained from Mind the Graph (available at www.mindthegraph.com).