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

Abstract

SUMMARYThe primary olfactory centres of the sphinx moth Manduca sexta, the antennal lobes, contain a small number of sexually dimorphic glomeruli: the male-specific macroglomerular complex and the large female glomeruli. These glomeruli play important roles in sex-specific behaviours, such as the location of conspecific females and the selection of appropriate host plants for oviposition. The development of sexually dimorphic glomeruli depends strictly on the ingrowth of sex-specific olfactory receptor cell afferents. In the present study we tested the role of female-specific olfactory receptor cells (ORCs) in mediating femalespecific host plant approach behaviour and in determining the response of downstream antennal lobe neurons. We generated male gynandromorphs by excising one imaginal disc from a male larva and replacing it with the antennal imaginal disc from a female donor. Most male gynandromorphs had an apparently normal female antenna and a feminised antennal lobe. These gynandromorphs were tested for flight responses in a wind tunnel towards tomato plants, a preferred host plant for oviposition in M. sexta. Male gynandromorphs landed on host plants as often as normal females, demonstrating that the presence of the induced female-specific glomeruli was necessary and sufficient to produce female-like, odour-oriented behaviour, i.e. orientation towards host plants. We also characterised the physiological and morphological properties of antennal lobe neurons of male gynandromorphs. We found that projection neurons with arborisations in the induced female-specific glomeruli showed physiological responses akin to those of female-specific projection neurons in normal females. These results therefore indicate that ORCs confer specific odour tuning to their glomerular targets and, furthermore, instruct odour-specific behaviour.

The neural bases of host plant selection in a Neuroecology framework

“…A second AL subsystem comprises three male-specific glomeruli (the so-called macroglomerular complex) which process information about the conspecific female's sex pheromone (Figure 2B ; Christensen and Hildebrand, 1987 ; Heinbockel et al, 1999 , 2004 ). Females have a pair of large female-specific glomeruli (LFGs, Figures 2B,C , 4A,B ) which respond to particular host plant VOCs (Roche King et al, 2000 ; Reisenman et al, 2004 ) and are involved in mediating oviposition behavior (Kalberer et al, 2010 ), and three smaller female-specific glomeruli (Grosse-Wilde et al, 2011 ). Correspondingly, three male-specific and five female-specific OR genes have been described in M. sexta (Grosse-Wilde et al, 2011 ).…”

Sensation in a Single Neuron Pair Represses Male Behavior in Hermaphrodites

“…In Manduca sexta, transplanting the nascent male sensory apparatus (his antennae) to a female larva induces male development in the female brain, and the adult animal has male behaviors (Schneiderman et al, 1986). The reciprocal switch generates an animal that has female behaviors (Kalberer et al, 2010). In this case, a difference in detection induces sexually dimorphic wiring, resulting in a difference in processing.…”

Understanding smell—The olfactory stimulus problem

“…Several studies have found a relationship between differences in behavior and shifts in spatial patterns (Ho et al, 2006;Linster et al, 2002) and, even more, changing locations of glomeruli in mice can result in behavioral impairments, in spite of persistent physiological activations (Adam and Mizrahi, 2010). Similarly, in the AL of female moths, glomeruli in a sexually dimorphic region specialize in odorants that are related to oviposition (Kalberer et al, 2010;Reisenman et al, 2009). In Drosophila, it is known that particular glomeruli mediate appetitive and aversive behavioral responses (Semmelhack and Wang, 2009).…”