The chemosensory basis for behavioral divergence involved in sympatric host shifts II: olfactory receptor neuron sensitivity and temporal firing pattern to individual key host volatiles

Abstract

The Rhagoletis species complex has been a key player in the sympatric speciation debate for much of the last 50 years. Studies indicate that differences in olfactory preference for host fruit volatiles could be important in reproductively isolating flies infesting each type of fruit via premating barriers to gene flow. Single sensillum electrophysiology was used to compare the response characteristics of olfactory receptor neurons from apple, hawthorn, and flowering dogwood-origin populations of R. pomonella, as well as from the blueberry maggot, R. mendax (an outgroup). Eleven volatiles were selected as stimuli from behavioral/electroantennographic studies of the three R. pomonella host populations. Previously, we reported that differences in preference for host fruit volatile blends are not a function of alterations in the general class of receptor neurons tuned to key host volatiles. In the present study, population comparisons involving dose-response trials with the key volatiles revealed significant variability in olfactory receptor neuron sensitivity and temporal firing pattern both within and among Rhagoletis populations. It is concluded that such variability in peripheral sensitivity and temporal firing pattern could influence host preference and contribute to host fidelity and sympatric host shifts in the Rhagoletis complex.

Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia

“…As mentioned in Relaxed Purifying Selection and/or Positive Selection, specialized insects appear to have narrow host preferences largely because they are more sensitive than generalists to deterrent chemicals in nonhosts (22). One might therefore expect specialization on one of many former plants (or the abandonment of ancestral hosts in general) to be associated with amino acid substitutions that increase sensitivity to deterrents in abandoned hosts; i.e., elevated Ka/Ks (32,33). Whereas loss of function may be restricted to insects that acquire/shift to novel hosts (because such losses provide one of many ways to disrupt receptor genes that respond to deterrents in the new hosts) or simply to the subset of receptors that are not directly involved in host selection.…”

Receptor expression and sympatric speciation: unique olfactory receptor neuron responses in F1 hybrid Rhagoletis populations

“…For statistical comparison of ORN responses, parsimony networks depicting the interrelationship of single cell sensillum response patterns for parents (Olsson et al, 2006a;Olsson et al, 2006b) and F 1 hybrids to the 11 volatile compounds tested in the study were constructed using the program TCS v. 1.13 (Clement et al, 2000). These networks provided a graphic overview of ORN response relationships for the entire sample population, allowing for multi-dimensional characterization of similarities and differences in the patterns of variation for parents and hybrids.…”

“…This latter analysis determined whether any observed difference between parent and hybrid response patterns could be caused by biased sampling of parent neurons due to smaller sample sizes in parent (N=77) vs hybrid (N=118) populations. (N=118) (Olsson et al, 2006a;Olsson et al, 2006b). Fig.·1 illustrates typical parent and hybrid ORN response profiles for three basic classes of Rhagoletis ORNs, as described by Olsson et al (Olsson et al, 2006a) (see Table·2).…”

“…Previously, we found that ORNs from various parental Rhagoletis host populations demonstrated inter-population variation in ORN sensitivities and temporal firing patterns to an array of key host fruit volatiles (Olsson et al, 2006b). However, all populations tested possessed similar classes of ORNs responding with similar odor specificities (Olsson et al, 2006a).…”

“…Chemical stimuli and neurophysiological analyses were similar to those previously published (Olsson et al, 2006a;Olsson et al, 2006b). We briefly overview these methods below.…”