Abstract
A growing number of studies demonstrate, or suggest, that vector-borne parasites manipulate phenotypic traits of their vectors and hosts in ways that increase contacts between them, and hence favour the parasites' transmission [1,2]. Understanding these processes is not only exciting for purely scientific reasons but also important because of their role in applied parasitology, such as epidemiology and medicine. The most frequently reported changes induced by vector-borne parasites are alterations of biting rates in vectors or of attractiveness in vertebrate hosts [3,4]. Our aim here is to elaborate further on some potentially interesting and important avenues for future research in this area. We begin this paper with a brief overview of the main mechanisms used by vectors to locate their vertebrate host, as it helps to grasp the fundamentals of the research on manipulation in vectors, as well as its current challenges. Bloodsucking insects have well-developed sensorial machinery to locate and choose their host [5]. Host location behaviour is usually organized into three areas which show considerable variation among vector species: (i) the appetitive search, (ii) the activation and orientation, and (iii) the attraction. The two last steps involve insect responses to external stimuli, mainly visual and odour cues, but also heat and to a lesser extent, water vapour and sound [5]. Vision is most widely used by diurnal insect vectors (e.g., blackflies, tsetse flies, several mosquitoes). The detection depends mainly on differences in colour contrast and intensity contrast; generally, flies are attracted to blue/black objects while they are repelled by yellow ones. Odour-mediated host-seeking has been more thoroughly studied and seems to be utilized by virtually all bloodsucking insects. The olfactory stimuli used by the insects are various, ranging from carbon dioxide to lactic acid, ammonia, acetone, octenol, phenolic components of urine, and sweat. Bloodsucking insects can be also very sensitive to heat [5]. Although some of these components (vision, olfaction, hearing) could be theoretically altered by parasites in ways that may be predicted to enhance parasite transmission, only a few have been considered. Bite more or bite better? Qualitative manipulation, according to which generalist bloodfeeding insects, once infected, would develop a feeding preference for hosts targeted by the parasite, is an underexplored scenario. Maximising transmission towards a suitable host could be achieved by parasites by inducing in the vector a sensory bias for host traits that are correlated with optimal suitability for the parasite. Qualitative manipulation could theoretically occur at two levels: (i) at the interspecific level, with infected vectors biting more than expected on suitable host species for the parasite and (ii) at the intraspecific level, when infected vectors prefer feeding on less-immune hosts or on individuals that are uninfected (and thus do not yet harbour potential competitors). In particular cases, however (e.g., Plasmodium), the reverse tendency might be expected in order to find a sexual partner of a different strain. To test for the qualitative manipulation hypothesis, a dual-port olfactometer could be used to quantify the behavioural responses of infected and uninfected insect vectors to volatiles emitted by different host species. For instance, Glossina palpalis gambiensis has a broad range of hosts in central Africa (humans, reptiles, bushbuck, and ox) and is the main vector of Trypanosoma brucei gambiense responsible for the medically important Human African trypanosomiasis. We would predict that once infected, flies are more attracted by human cues than by those of other vertebrates.