Divergent Evolutionary Pressures Shape Olfactory Sensitivity of the Maxillary Palps in Tephritidae Fruit Flies

Olfaction is a rapidly evolving sense. Given its diverse functions, from finding ecological niches to selection of mates, we hypothesized that olfaction is subjected to divergent evolutionary pressures. We compared the olfactory sensitivity of five species of Tephritidae fruit flies to two broad classes of volatiles: general niche-related volatiles (food and fruit odors) and volatiles used in sexual communication (pheromones and "parapheromones"). We then analyzed whether the differential sensitivities across species harbor "signals" of such contrasting evolutionary pressures. As recent studies highlight the maxillary palps as key auxiliary olfactory organs for detecting both classes of volatiles, we focused our sensory analysis on this auxiliary olfactory organ. Using gas chromatography coupled to electropalpographic detection (GC-EPD), we recorded sensory responses from five species with a diverse phylogenetic and ecological separation. Detection overlapped considerably across taxa; however, the maxillary palp exhibited distinct sex and clade-specific patterns in sensitivity to pheromones and parapheromones. Cluster analysis of sensitivities to (para)pheromones aligned strongly with the species' phylogeny. In contrast, cluster analysis of sensitivities to general food and fruit odors clustered separately and showed a strong correlation with ecological niche rather than phylogeny. Clearly, the selection pressures that shape the evolutionary direction of olfactory sensitivity to (para)pheromones and niche-related odors are diametrical opposites, reminiscent of stabilizing versus directional selection. Understanding the detection and evolution of distinct volatile classes provides valuable insights into the evolutionary ecology of olfaction, studies on olfactory receptors, and sensory and preference coding, and supports the rational development of novel lures to manage these pest insects.