Inheritance of Olfactory Preferences II. Olfactory Receptor Neuron Responses from <i>Heliothis subflexa</i> × <i>Heliothis virescens</i> Hybrid Male Moths

Abstract

Single-cell electrophysiological recordings were obtained from olfactory receptor neurons (ORNs) in sensilla trichodea on male antennae of hybrids formed mainly by crossing female Heliothis subflexa with male Heliothis virescens (‘SV hybrids’). We recorded from the A-, B-, and C-type sensilla trichodea, with the latter two types housing ORNs exhibiting response profiles to different pheromone components that we had previously found to be characteristic for each species. For both the B- and the C-type SV hybrid sensilla, most of the ORNs exhibited a spike amplitude and ORN co-compartmentalization within sensilla that more strongly resembled the ORNs of parental H. subflexa rather than those of H. virescens. The overall mean dose-response profiles of the ORNs in hybrid C- and B-type sensilla were intermediate between those of the H. virescens and H. subflexa parental type ORNs. However, not all hybrid ORNs were intermediate in their tuning spectra, but rather ranged from those that closely resembled H. subflexa or H. virescens parental types to those that were intermediate, even on the same antenna. The most noteworthy shift in ORN responsiveness in hybrid males was an overall increase in sensitivity to Z9–14:Ald exhibited by Z9–16:Ald-responsive ORNs. Heightened cross-responsiveness to Z9–14:Ald by hybrid ORNs correlates well with observed behavioral cross-responsiveness of hybrids in which Z9–14:Ald could substitute for Z9–16:Ald in the pheromone blend, a behavior not observed in parental types. The hybrid ORN shifts involving greater sensitivity to Z9– 14:Ald also correlate well with studies of hybrid male antennal lobe interneurons that exhibited a shift toward greater cross-responsiveness to Z9–14:Ald and Z9– 16:Ald. We propose that the differences between parental H. virescens, H. subflexa, and SV hybrid male pheromone ORN responsiveness to Z9–16:Ald and Z9–14:Ald are most logically explained by an increased or decreased co-expression of two different odorant receptors for each of these compounds on the same ORN.

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

“…In fact, two individuals possessed both parent-and hybrid-like cells in the same sensillum. The relationship between transcription factors and OR genes has been suggested as a pathway for the unique responses found in Heliothine hybrids (Baker et al, 2006). However, unlike the Heliothine study where the hybrid ORNs displayed a stereotypical, though unique, set of responses from the parents, the Rhagoletis hybrid ORN response profiles were much more diverse, and almost random in appearance.…”

“…A recent study of chemoreception in hybrids between two closely related moth species, Heliothis virescens and H. subflexa, found that some hybrid ORNs responded to unique combinations of pheromone components absent from either parent species (Baker et al, 2006). Combined with both flight tunnel assays (Vickers, 2006a) and antennal lobe recordings (Vickers, 2006b), Baker et al (Baker et al, 2006) postulated that the "broad yet specific tuning of certain ORN types" suggests that multiple olfactory receptors were expressed in the dendritic membranes of the olfactory neurons.…”

“…Combined with both flight tunnel assays (Vickers, 2006a) and antennal lobe recordings (Vickers, 2006b), Baker et al (Baker et al, 2006) postulated that the "broad yet specific tuning of certain ORN types" suggests that multiple olfactory receptors were expressed in the dendritic membranes of the olfactory neurons. In congruence with the hypothesis by Baker et al for Heliothine hybrids (Baker et al, 2006), it is also possible that Rhagoletis hybrid ORNs express multiple receptors, in combinations absent from parent ORNs. This could produce the diverse response profiles witnessed in hybrid ORN responses.…”

“…In the Heliothine study, Baker et al suggested that because the regulation of agonist/antagonist behaviors are believed to occur primarily in the antennal lobe and higher brain centers, a simple change in receptor expression at the periphery could allow a shift in the agonistic/antagonist properties of a compound (Baker et al, 2006). Olfactory receptor neurons expressing one type of olfactory receptor target a single glomerulus in the antennal lobe of the brain (Vosshall et al, 2000;Gao et al, 2000), and ORNs will target the same glomeruli regardless of normal receptor expression (Dobrista et al, 2003).…”

“…These previous studies revealed four different characteristics of hybrid olfactory receptor neurons (ORNs): (1) hybrids can possess identical ORNs to parental populations, but in different proportions [Ips pini (Mustaparta et al, 1985)]; (2) hybrids can respond more similarly to one parent over the other [Agrotis ipsilon ϫ A. segetum (Gadenne et al, 1997)]; (3) hybrid ORNs can generate intermediate spike amplitudes (Roelofs et al, 1987) and frequencies (Cossé et al, 1995); [two pheromone races of Ostrinia nubilalis]; and (4) hybrid ORNs can exhibit a variety of responses, some similar to the parents, and some 'atypical' responders [Ctenopseustis obliquana ϫ Ctenopseustis sp. (Hansson et al, 1989); Heliothis subflexa ϫ H. virescens (Baker et al, 2006)]. In this study, we test the hypothesis that Rhagoletis hybrid ORNs also exhibit unique characteristics from parent populations, and that these peripheral alterations can impact olfactory host volatile preference.…”