Specific olfactory neurons and glomeruli are associated to differences in behavioral responses to pheromone components between two Helicoverpa species

Abstract

Sex pheromone communication of moths helps to understand the mechanisms underlying reproductive isolation and speciation. Helicoverpa armigera and Helicoverpa assulta use (Z)-11-hexadecenal (Z11-16:Ald) and (Z)-9-hexadecenal (Z9-16:Ald) as pheromone components in reversed ratios, 97:3 and 5:95, respectively. H. armigera also produces trace amount of (Z)-9-tetradecenal (Z9-14:Ald) in the sex pheromone gland, but H. assulta does not. Wind tunnel studies revealed that the addition of small amounts (0.3%) of Z9-14:Ald to the main pheromone blend of H. armigera increased the males' attraction, but at higher doses (1%, 10%) the same compound acted as an inhibitor. In H. assulta, Z9-14:Ald reduced male attraction when presented as 1% to the pheromone blend, but was ineffective at lower concentrations (0.3%). Three types (A–C) of sensilla trichodea in antennae were identified by single sensillum recording, responding to Z11-16:Ald, Z9-14:Ald, and both Z9-16:Ald and Z9-14:Ald, respectively. Calcium imaging in the antennal lobes (ALs) revealed that the input information of the three chemicals was transmitted to three units of the macroglomerular complex (MGC) in ALs in both species: a large glomerulus for the major pheromone components, a small one for the minor pheromone components, and a third one for the behavioral antagonists. The type A and C neurons tuned to Z11-16:Ald and Z9-16:Ald had a reversed target in the MGC between the two species. In H. armigera, low doses (1, 10 μg) of Z9-14:Ald dominantly activated the glomerulus which processes the minor pheromone component, while a higher dose (100 μg) also evoked an equal activity in the antagonistic glomerulus. In H. assulta, instead, Z9-14:Ald always strongly activated the antagonistic glomerulus. These results suggest that Z9-14:Ald plays different roles in the sexual communication of two Helicoverpa species through activation of functionally different olfactory pathways.

The Inheritance of the Pheromone Sensory System in Two Helicoverpa Species: Dominance of H. armigera and Possible Introgression from H. assulta

“…The spike frequencies (spikes/s) were calculated by counting the number of spikes with the same amplitude during the first 200 ms of the response. However, we counted the total number of spikes from the C type sensilla of H. armigera because our previous cross-adaptation test indicated this type sensilla of H. armigera contain two OSNs with similar spike amplitudes which are difficult to differentiate (Wu et al, 2015). For both non-responding and poorly responding OSNs, spikes were counted during the same 200 ms post-stimulus interval.…”

“…One large amplitude neuron responding to Z9-16:Ald, and one with small amplitude responding to Z9-14:Ald, and have been previously identified on the basis of their different spike amplitudes (Berg and Mustaparta, 1995; Berg et al, 2005). In H. armigera , the two neurons in C type sensilla are difficult to differentiate due to their similar spike amplitudes (Wu et al, 2015; Xu et al, 2016). As in other Heliothine species (Christensen et al, 1991; Berg et al, 1998; Vickers and Christensen, 2003), the pheromonal information received by OSNs is conveyed to the MGC area of the AL (Berg et al, 2005; Zhao and Berg, 2010; Wu et al, 2013, 2015).…”

“…In H. armigera , the two neurons in C type sensilla are difficult to differentiate due to their similar spike amplitudes (Wu et al, 2015; Xu et al, 2016). As in other Heliothine species (Christensen et al, 1991; Berg et al, 1998; Vickers and Christensen, 2003), the pheromonal information received by OSNs is conveyed to the MGC area of the AL (Berg et al, 2005; Zhao and Berg, 2010; Wu et al, 2013, 2015). In H. armigera , the major sex pheromone component Z11-16:Ald elicits a response in the larger glomerulus of the MGC, the cumulus, while the minor component Z9-16:Ald activates one smaller glomerulus of MGC, the posterior dorsomedial unit (Dm-p) (Wu et al, 2013).…”

Ultrastructure of antennal sensilla of Erannis ankeraria Staudinger (Lepidoptera: Geometridae)

“…Presumably, void of socket would restrict the mechano-sensation (Schneider, 1964), while the long hair-shaped STs are specialized for pheromone sensory (Prestwich, Du, & LaForest, 1995;Steinbrecht, Laue, Maida, & Ziegelberger, 1996). Single sensillum recording has substantiated the pheromone sensitivity of ST on male antennae of Heliothis, Helicoverpa, and Manduca species (Baker et al, 2004;Kaissling, Hildebrand, & Tumlinson, 1989;Wu et al, 2015). Furthermore, molecular studies on other species have continually validated the abundance of pheromone-binding proteins in ST, indicating their participation in pheromone detection (Laue, Maida, & Redkozubov, 1997;Yu et al, 2018).…”

Prefrontal Cortical Activity During the Stroop Task: New Insights into the Why and the Who of Real-World Risky Sexual Behavior

“…Similarly, the amygdala and striatum have been implicated in the processing of sexual stimuli (15, 16). Stronger striatal reactivity in response to sexual cues has been shown to predict subsequent sexual behavior (17) and striatal sensitivity to sexual cues has been observed in individuals with compulsive sexual behavior relative to controls (16, 18). Based on this model and the existing work on the neurobiology of sexual risk, one contributor to risky sexual behavior in MSM may be individual variability within the prefrontal cortex system, leading to individual differences in executive functioning.…”