Olfactory regulation of mosquito–host interactions
Introduction
The success of mating, blood feeding and oviposition determine life history strategies of mosquitoes. Each of these behaviors is mediated by both internal and external factors. The principle external cues affecting mosquito behavior are temperature, humidity, visual objects, and most importantly, odor. Ambient temperature affects general mosquito activity and survival, whereas host temperature may affect host seeking, landing and probing (Bowen, 1991). Likewise, humidity influences general activity, survival, host seeking at close range and possibly oviposition. It is not clear to what extent mosquitoes respond to colors, but they certainly respond to shapes and they require adequate contrast for flight orientation (Bidlingmeyer, 1994). Males generally use visual markers for swarm formation (Yuval and Bouskila, 1993). Many behavioral expressions of mosquitoes are mediated by olfaction. Indeed, the chemical ecology of mosquitoes is now widely recognized as one area of investigation on which future control strategies may depend. Host seeking and feeding behaviors are much affected by host odors, and many mosquito species use olfaction for oviposition (Takken and Knols, 1999). It is not known, though, whether mating is also mediated by smell, although there is indirect evidence that for at least a few species an olfactory component is involved in mating. (Gomulski, personal communication).
Most of the available literature on mosquito olfaction relates to host seeking and feeding behavior. Major reviews by Bowen, 1991, Takken, 1991, Foster, 1995, Gibson and Torr, 1999, Takken and Knols, 1999 cover the subject in detail, including electrophysiological work, volatiles affecting males and female host seeking. Some of this work includes studies on important vectors such as the yellow fever mosquito Aedes aegypti (L.), the African malaria vector Anopheles gambiae Giles sensu stricto and the filariasis vector Culex quinquefasciatus (Say). Fundamental aspects of olfactory signal transduction at the peripheral level have revealed the involvement of olfactory receptors on maxillary palpi and antennae. The detection of carbon dioxide (CO2) and l-lactic acid by Ae. aegypti in particular has been well established. Studies of the responses of these species to other host odors are in progress and have not yet been reviewed. Behavioral studies in wind tunnels and olfactometers have shown that human volatiles have a role as kairomones for the three mosquito species mentioned. Lactic acid and carboxylic acids have been singled out as likely candidates involved with the attraction of these insects to humans These studies have been corroborated by field studies, mostly with An. gambiae and Cx. quinquefasciatus, which have shown that these insects are attracted to human volatiles from a distance (Costantini et al., 1996, Mboera et al., 1997).
Considerable progress has been made in the field of olfaction with respect to mosquito–host interactions. The recent publication of the An. gambiae genome (Holt et al., 2002) as well as ongoing sequencing projects of other important mosquito vectors offers new opportunities to advance our knowledge on mosquito olfaction by the identification of genes that regulate olfactory behavior. This may ultimately lead to a better understanding of the genetic basis of important processes such as host selection, repellent behaviors, landing and probing. The significance of this knowledge with relevance for new strategies of vector-borne disease control will be discussed.
Section snippets
Olfactory mechanisms
Vertebrates and invertebrates are remarkably similar with regard to the molecular mechanisms through which they sense chemicals and other environmental cues (Hildebrand and Shepherd, 1997). Information carried by odor molecules is encoded in electrical signals that are active in sensory and other neurons. The activation of different subsets of sensory neurons to different degrees is the basis for neural encoding and further processing of the odor information by higher centers in the olfactory
Behavior and sensory physiology
Recent behavioral studies on mosquitoes have focused mostly on Ae. aegypti and An. gambiae. Both species are highly anthropophilic. In An. gambiae s.s. the strong dominance of anthropophily was demonstrated in choice studies in an olfactometer, with both An. gambiae s.s. and the more zoophilic sibling An. quadriannulatus (Theobald) (Pates et al., 2001a). The former expressed a strong aversion to cow odor and was significantly more attracted to human odor, while the latter species had no
Molecular genetics
In recent years using both molecular and genomic approaches, several proteins that are involved in fundamental aspects of olfactory signal transduction have been molecularly cloned and characterized in An. gambiae and other vector mosquitoes. With the recent publication of the complete genomic sequence of An. gambiae (Holt et al., 2002) as well as rapid advances in completing similar projects for other mosquito vectors, there can be little doubt that the coming years will see a dramatic
Concluding remarks
Rapid advances along several research fronts have laid the foundation for a novel approach toward the design and development of a new generation of vector-borne disease control strategies. By combining the knowledge that is generated from the behavioral, molecular, neurological and physiological studies outlined in this review, as well as additional efforts currently underway, the fundamental elements that underlie critically important vector behaviors such as host selection may be further
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