Consequences of interspecies antennal imaginal disc transplantation on organization of olfactory glomeruli and pheromone blend discrimination

Abstract

The antennal imaginal disc was transplanted between male larvae of two different heliothine moth species, Heliothis virescens (HV) and Helicoverpa zea (HZ). Males of these species respond to distinct pheromone blends, have different peripheral and central olfactory neuron specificities, as well as distinct arrangements of antennal lobe olfactory glomeruli, in the specialized male macroglomerular complex (MGC). After pupal development and adult eclosion, unilateral (with one antennal disc left intact) and bilateral antennal transplant males were assayed in a wind tunnel to both species' pheromone blends to determine their ability to discriminate between the two signals. The postmetamorphic developmental effects of interspecific transplantation upon the primary olfactory centers in the moth brain were then examined in these same individuals. Behavioral tests showed that both types of unilateral transplant continued to exhibit upwind anemotactic flight to the normal recipient blend with occasional flights to the donor blend. In contrast, bilateral transplants preferred the HV pheromone blend regardless of the direction of transplant, with some males of each type also responding to the HZ blend. Neuroanatomic evaluation of the MGC revealed that the donor arrangement of MGC glomeruli was induced in 73% HZ donor to HV recipient transplants and 56% of the reciprocal transplant. Surprisingly, several V-Z bilateral transplant males responded to both HV and HZ pheromone blends and had two HV MGC structures. This behavioral outcome was unexpected, because responses to the HV blend are mediated by inputs that are normally antagonistic to HZ males and the normal HV antenna lacks olfactory receptor neurons capable of responding to the essential minor pheromone component of the HZ blend. These data indicate a plasticity in developmental pathways regulating the expression of peripheral olfactory receptor neurons and in the glomerular processing of species-specific olfactory information.

A Single Sex Pheromone Receptor Determines Chemical Response Specificity of Sexual Behavior in the Silkmoth Bombyx mori

“…However, whole antennae were replaced by donor antennae. In addition, the transplantation also modified the anatomy of the recipient MGC to that of the donor MGC [43], [44]. Therefore, molecular factors responsible for the modification of behavioral preference could not be identified.…”

Responses of protocerebral neurons in Manduca sexta to sex-pheromone mixtures

“…Tumlinson et al 1989,1994; Vickers et al 2003; Domingue et al 2007, 2008; Kanno et al 2010; El-Sayed et al 2011; Leary et al 2012; Martin et al 2013), our finding that 24% of the sampled, pheromone-responsive protocerebral neurons in this study did not distinguish among the tested stimuli (supplemental Table 1) is surprising. Pairwise comparisons of responses to different pheromonal stimuli (EEZ vs. BAL, EEZ vs. mixture, BAL vs. mixture) showed that 50–80% of neurons exhibited no significant differences in their responses to these stimulus pairs (Figure 1, bottom).…”

Male moths bearing transplanted female antennae express characteristically female behaviour and central neural activity

“…This behaviour is exhibited by normal males but has not been observed in normal females because the antennae of M. sexta females lack ORCs responsive to the main sex pheromone components (Kaissling, 1989). In interspecific antennal imaginal disc transplantation experiments between Heliothis virescens and Helicoverpa zea males, both types of unilateral transplants continued to exhibit upwind antemotactic flight in a wind tunnel to the recipient pheromone blend (Vickers et al, 2003). In contrast with our results, the interspecific transplantation of only one antenna was not sufficient to produce a behavioural change.…”