The Drosophila pheromone cVA activates a sexually dimorphic neural circuit

Abstract

Courtship is an innate sexually dimorphic behaviour that can be observed in naive animals without previous learning or experience, suggesting that the neural circuits that mediate this behaviour are developmentally programmed. In Drosophila, courtship involves a complex yet stereotyped array of dimorphic behaviours that are regulated by Fru(M), a male-specific isoform of the fruitless gene. Fru(M) is expressed in about 2,000 neurons in the fly brain, including three subpopulations of olfactory sensory neurons and projection neurons (PNs). One set of Fru(+) olfactory neurons expresses the odorant receptor Or67d and responds to the male-specific pheromone cis-vaccenyl acetate (cVA). These neurons converge on the DA1 glomerulus in the antennal lobe. In males, activation of Or67d(+) neurons by cVA inhibits courtship of other males, whereas in females their activation promotes receptivity to other males. These observations pose the question of how a single pheromone acting through the same set of sensory neurons can elicit different behaviours in male and female flies. Anatomical or functional dimorphisms in this neural circuit might be responsible for the dimorphic behaviour. We therefore developed a neural tracing procedure that employs two-photon laser scanning microscopy to activate the photoactivatable green fluorescent protein. Here we show, using this technique, that the projections from the DA1 glomerulus to the protocerebrum are sexually dimorphic. We observe a male-specific axonal arbor in the lateral horn whose elaboration requires the expression of the transcription factor Fru(M) in DA1 projection neurons and other Fru(+) cells. The observation that cVA activates a sexually dimorphic circuit in the protocerebrum suggests a mechanism by which a single pheromone can elicit different behaviours in males and in females.

Postembryonic development of sexually dimorphic glomeruli and related interneurons in the cockroach Periplaneta americana

“…The primary targets of PNs in the protocerebrum are calyces of the 6 mushroom body and/or part of the lateral protocerebrum, also known as the lateral horn (Fig. 3a) [3,9]. The PNs were classified as either uniglomerular PNs which spread dendrites to a single glomerulus (Fig.…”

“…3), suggesting that the male-specific pathways could be formed by modification of the pre-existing, female-like pathways, analogous to the development of sexually dimorphic antennal sensilla. As it is presumed that integration of sensory signals and their conversion to behavioral decisions occurs in the neural pathway involving the lateral horn [3] this morphologic change must be preparatory to initiation of pheromone-triggered orientation behavior in adult males to adult females [5].…”

Dendritic Eph organizes dendrodendritic segregation in discrete olfactory map formation in Drosophila

“…Among them, Or67d, the primary neuron of the DA1 olfactory circuit, detects Drosophila male-specific pheromone 11 cis-vaccenyl acetate (cVA) and triggers sex-specific courtship behavior in both male and female flies (Kurtovic et al 2007). In addition, the DA1 PNs show sexually dimorphic neural circuitry (Datta et al 2008). The primary neuron of DL3 (Or65a) also responds to cVA when flies are exposed to it for a long period.…”

Sexual isolation of male moths explained by a single pheromone response QTL containing four receptor genes

“…It is surprising to find that a change in receptors for Z11-16:OAc could be responsible for the switch between the positive behavioral response of Hs and the negative response of Hv to this compound. In Drosophila where cis-vaccenyl acetate is attractive to females but repulsive to males, it is a central nervous system difference that controls the switch between positive and negative response (22). Furthermore, previous work showed that acetate responsive receptor neurons of Hv converge on a different glomerulus of the male macroglomerular complex compared to those of Hs (51).…”

“…We now know that peripheral reception of pheromones involves a number of proteins in male antennae, including pheromone binding proteins (PBP), general odorant binding proteins (GOBP), chemosensory proteins (CSP), two classes of odorant receptors (OR), pheromone degrading enzymes (PDE), and sensory neuron membrane proteins (SNMP) (19)(20)(21). Genetic changes in the structure/expression of any or all of these proteins could have been involved in evolutionary diversification of moth sexual communication systems, but it is also possible that the crucial changes were in the male moth central nervous system (5,22).…”