Enhanced Attraction of Arthropod Vectors to Infected Vertebrates: A Review of Empirical Evidence

Abstract

A large diversity of parasites manipulates their hosts in various ways to complete their own life cycle. Enhancing the attractiveness of their host to vectors has been suggested as a strategy allowing vector-borne parasites to increase their transmission. Indeed, a higher attraction of hematophagous, arthropod vectors to infected vertebrates compared to uninfected individuals has been found in many systems (e.g., Trypanosoma-tsetse flies, Leishmania-sand flies, Borrelia-ticks) but was most often verified in the Plasmodium-mosquitoes model. However, a number of studies found no difference in attractiveness, or a higher attractiveness of uninfected hosts. In this review, we present studies reporting a comparison of the attractiveness and/or the biting rate of infected and uninfected vertebrates. We then discuss several biological factors and experimental design aspects that can explain discrepancies between studies. Finally, we stress the importance of investigating the mechanisms of parasiteinduced increased attractiveness of infected hosts to conclude that such observations are cases of adaptive manipulation.

Microbially Mediated Chemical Ecology of Animals: A Review of Its Role in Conspecific Communication, Parasitism and Predation

“…Further examples of symbiotic bacteria indirectly mediating host detection by enemies come from research on host preference by mosquitoes and related ectoparasites [ 77 ]. Although parasites may directly induce behavioral changes in their hosts that are aimed at increasing parasite transmission [ 78 ], preferences by mosquitoes toward odors of already parasitized hosts are likely mediated by changes in host microbiotas [ 79 , 80 ].…”

“…Hematophagous insects acting as vectors of human diseases (e.g., malaria, yellow fever, dengue) [ 81 , 82 , 83 , 84 , 85 ] might exemplify this possibility. It has been suggested that mosquitoes may be more attracted to the odor of Plasmodium -infected humans and birds [ 72 , 73 ], but see [ 77 ], and some evidence suggests that bacteria play key roles in determining host preference by mosquitoes. For example, laboratory experiments have revealed that the mosquito Anopheles gambiae , a main malaria vector in humans, is more attracted to individuals whose skin bacterial community is less diverse, but more abundant, and that includes Staphylococcus epidermis [ 82 ].…”

“…Most ectoparasites are vectors of important human and animal diseases. Discovering connections between the animal microbiome and the volatiles that attract or deter ectoparasites may aid in the development of new products or methods for protection against ectoparasites and the diseases they transmit [ 76 , 77 ]. Besides health concerns [ 154 ], parasites cause great economic losses [ 155 , 156 ].…”

Epidemiological and ecological consequences of virus manipulation of host and vector in plant virus transmission

“…Vectors show preferences in their interactions with plants that can directly influence the rate of transmission. Preference can take many forms, with much past work focusing on arthropod vectors of vertebrate-host parasites [9][10][11][12]. Focusing on plant viruses in particular, vector preference can be expressed in different ways: (i) host preference within a vector's host range; (ii) preference for the host phenotype, restricted in the sense here to whether the host is infected or healthy; and (iii) conditional preference, whereby the preference for infected or healthy hosts depends on whether the vector is viruliferous or nonviruliferous.…”

Epidemiological and ecological consequences of virus manipulation of host and vector in plant virus transmission

“…Vectors show preferences in their interactions with plants that can directly influence the rate of transmission. Preference can take many forms, with much past work focusing on arthropod vectors of vertebrate-host parasites (Kingsolver, 1987;Chamchod & Britton, 2011;Gandon, 2018;Cozzarolo et al, 2020). Focusing on plant viruses in particular, vector preference can be expressed in different ways: (i) host preference within a vector's host range; (ii) preference for the host phenotype, restricted in the sense here to whether the host is infected or healthy; and (iii) conditional preference, whereby the preference for infected or healthy hosts depends on whether the vector is viruliferous or non-viruliferous.…”