An Acute Olfactory System Is Essential for Reproduction-The Raison D'être for Adult Insects1

Article excerpt

INSECTS are extremely successful animals whose lives intertwine with ours. They negatively affect human society when they become (i) agricultural pests that damage our crops and stored products or I(ii) vectors of diseases causing tragic human suffering and death. Mosquitoes, for example, can transmit deadly pathogens and parasites while feeding on human blood. Every year, Anopheles mosquitoes, mainly An. gambiae and An. funestus, kill about one million humans, primarily women and children (Anonymous 2004). While feeding on their victims' blood, they unwittingly transmit the malaria-causing parasite that threatens half of the world's population. Globally, the number of people who contract malaria each year is greater than the population of the United States (Leal 2010). In sharp contrast, many other insect species are beneficial, and at least one, the honeybee, is essential for life on our planet as we know it. Honeybee pollination, for example, is responsible for about one third of our daily diet (McGregor 1976). The value of the increased yield and quality to U.S. agriculture achieved through honeybee pollination alone exceeds $14 billion (Morse and Calderone 2000). Some insect species facilitate breakdown of organic materials. Some are natural enemies of insect pests and are part of our arsenal of environmentally friendly tools for minimizing crop damage. Some insects may be perceived as deleterious from an economic perspective due to the harm they cause, but others are economic commodities. For example, silk produced by the silkworm is highly valuable; indeed, ancient Oriental economies considered it a major commodity.

In addition to behavior associated with survival, much of the life of insects is dedicated to reproduction. Their reproductive system enables them to be the most prominent animals on the planet (Klowden 2007). Adult insects in various taxonomic groups (e.g., moths) have a short life, which is geared toward reproduction (fig. 1). To provide nutrients for egg production, females of some species (e.g., mosquitoes) may require a blood meal following mating (fig. 2). Thus, mate- and hostfinding, respectively, are essential for successful reproduction in these two groups of insects. Consequently, insects have evolved an acute olfactory system, which is both remarkably sensitive and extremely dynamic (Leal 2005). This enables male moths to follow the trail of a scent remotely released by conspecific females overtly advertising their readiness to mate. Likewise, the olfactory system of female mosquitoes enables them to expeditiously find suitable hosts for a blood meal. These chemicals involved in insect chemical communication are referred to as semiochemicals and odorants in the jargons of chemical ecology and olfaction, respectively.

Insects detect these semiochemicals with specialized peripheral sensory structures, the olfactory sensilla, present on different chemosensory tissues such as antennae, maxillary palps, and proboscises. Odorant receptors (ORs) (Clyne et al. 1999; Vosshall et al. 1999) are expressed in the dendritic membrane of olfactory receptor neurons (ORNs) housed in these sensilla. Pheromones, human-derived chemical signals, and other odorant molecules are normally hydrophobic compounds. They have to pass through an aqueous medium, the sensillar lymph, surrounding the dendrites and separating the port of entry on the sensilla (the pore tubules) and the receptor neurons. To deal with this solubility issue, insects utilize odorant-binding proteins (OBPs) (Vogt and Riddiford 1981) to solubilize and transport semiochemicals through the sensillar lymph (fig. 3). Our biochemical and biophysical studies on an OBP from the silkworm moth that binds the sex pheromone bombykol (thus named pheromone-binding protein, BmorPBP) led us to hypothesize that moth PBPs deliver pheromones by a conformation change triggered by the low pH in the vicinity of ORs (Wojtasek and Leal 1999). In collaboration with Professors Jon Clardy (Harvard Medical School) and Kurt Wüthrich (ETH, Switzerland, and the Scripps Research Institute, La Jolla) we were able to unveil the structural details of this pH-mediated conformational change. …