Abstract
Insects use sensitive olfactory systems to detect relevant host volatiles and avoid unsuitable hosts in a complex environmental odor landscape. Insects with short lifespans, such as gall midges (Diptera: Cecidomyiidae), are under strong selection pressure to detect and locate suitable hosts for their offspring in a short period of time. Ephemeral gall midges constitute excellent models for investigating the role of olfaction in host choice, host shift, and speciation. Midges mate near their site of emergence and females migrate in order to locate hosts for oviposition, thus females are expected to be more responsive to olfactory cues emitted by the host compared to males. In this study, we explored the correlation between host choice and the function of the peripheral olfactory system in 12 species of gall midges, including species with close phylogenetic relationships that use widely different host plants and more distantly related gall midge species that use similar hosts. We tested the antennal responses of males and females of the 12 species to a blend of 45 known insect attractants using coupled gas chromatographic-electroantennographic detection. When the species-specific response profiles of the gall midges were compared to a newly generated molecular-based phylogeny, we found they responded to the compounds in a sex- and species-specific manner. We found the physiological response profiles of species that use annual host plants, and thus have to locate their host every season, are similar for species with similar hosts despite large phylogenetic distances. In addition, we found closely related species with perennial hosts demonstrated odor response profiles that were consistent with their phylogenetic history. The ecology of the gall midges affects the tuning of the peripheral olfactory system, which in turn demonstrates a correlation between olfaction and speciation in the context of host use.
Highlights
Olfaction evokes the most basic, often instinctive, reactions such as memory, hunger, attraction, and revulsion
The phylogeny among the 12 midge species tested is based on the DNA sequence similarities among three loci, c oxidase subunit I (COI), ef1α, 12S (Figure 1)
There was high withinspecies variation in response profiles, with some, but not all individuals capable of detecting the compounds (Figure 3, blue squares). This response pattern resulted in species-specific response profiles that are used in the following analyses
Summary
Olfaction evokes the most basic, often instinctive, reactions such as memory, hunger, attraction, and revulsion. Behaviors essential for the fitness of an individual, such as mate and habitat choice, are driven to a large extent by olfaction (Hansson and Stensmyr, 2011). The gall midges expanded greatly on flowering plants during the Cretaceous Period (Gagné, 2004). There are currently more than 6,000 described gall midge species, of which approximately 80% are closely associated with flowering plants (Gagné, 2004, 2010). Gall-inducing species are among the most hostspecialized. Most gall midges are either monophagous or oligophagous (Gagné, 2004), only inducing galls on a single or a few host plant species (Carneiro et al, 2009)
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