Summary Although males and females largely share the same genome and nervous system, they differ profoundly in reproductive investments and require distinct behavioral, morphological, and physiological adaptations. How can the nervous system, while bound by both developmental and biophysical constraints, produce these sex differences in behavior? Here, we uncover a novel dimorphism in Drosophila melanogaster that allows deployment of completely different behavioral repertoires in males and females with minimum changes to circuit architecture. Sexual differentiation of only a small number of higher order neurons in the brain leads to a change in connectivity related to the primary reproductive needs of both sexes—courtship pursuit in males and communal oviposition in females. This study explains how an apparently similar brain generates distinct behavioral repertoires in the two sexes and presents a fundamental principle of neural circuit organization that may be extended to other species.

Summary1. Neighbouring resources have been found to either decrease or increase the likelihood that a consumer organism attacks a focal resource. These phenomena are referred to as associational resistance (AR) and associational susceptibility (AS), respectively. While associational effects have been observed in various field studies, little is known on how resource heterogeneity can cause associational effects. 2. We used a laboratory approach in which we studied the effects of resource density and frequency in the search behaviour of Drosophila melanogaster as a model organism for olfactoryguided behaviour in insects. We first determined whether D. melanogaster could discriminate between odour sources that differ quantitatively. Secondly, we determined what the effect of resource density and frequency was on the search behaviour of D. melanogaster by combining these resources into various patch arrangements. Finally, we used the outcome of our experiments to disentangle the role of resource density and frequency in associational effects. 3. We found that D. melanogaster has the ability to discriminate between quantitatively different resources, but that the attraction to resource density is constrained by an optimum after which attraction decreases. Furthermore, in heterogeneous environments, flies showed a strong preference towards the more apparent resource, leading to AS for the more apparent resources and AR for the less apparent resource. The strength of this interaction increased with a decreasing frequency of the more apparent resource. 4. These results imply that D. melanogaster mainly selects patches at the level of individual resources. Consequently, when a patch contains qualitatively different resources, the more apparent resource will attract a higher number of flies than the less apparent resource irrespective of the frequency of the apparent resource within the patch. 5. Our study shows that associational effects can be explained by determining the hierarchical level at which a consumer selects its resources. When a consumer selects resources at the individual level rather than at the patch level, our results can be used to explain the population dynamics of host plants and their associated consumers under field conditions.

The Queensland fruit fly, Bactrocera tryoni, is considered one of the worst horticultural pests in Australia attacking a large variety of fruit crops. To defeat pest insects, olfactory attractants have been developed and widely used in lure and kill strategies. Male B. tryoni are strongly attracted to the compound raspberry ketone and its synthetic analog, cuelure. Despite the strong behavioral response, a recent study failed to show any activation of antennal receptors to cuelure. Therefore, we hypothesized that cuelure may be detected by an accessory olfactory organ, the maxillary palp. Combining behavioral and physiological experiments we clearly demonstrate that male flies, but not female flies, primarily use the maxillary palps and not the antennae to detect and respond to cuelure. Furthermore, regardless of satiety status, male flies always preferred cuelure over a sugar rich source, unless the maxillary palps were excised.

Neighboring resources can affect insect oviposition behavior when the complexity of sensory information obscures information about host resource availability in heterogeneous resource patches. These effects are referred to as associational effects and are hypothesized to occur through constraints in the sensory processing of the insect during host search, resulting into suboptimal resource use. Because the possibilities to study these constraints on naturally occurring animals are limited, we instead used sensory mutants of Drosophila melanogaster to determine the importance of sensory information in the occurrence of associational effects. We found that oviposition was mainly governed by non-volatile chemical cues and less by volatile cues. Moreover, the loss of gustatory sensilla resulted in random resource selection and eliminated associational effects. In conclusion, our study shows that associational effects do not necessarily depend on constraints in the sensory evaluation of resource quality, but may instead be a direct consequence of distinctive selection behavior between different resources at small scales.

Female fruit flies (Drosophila melanogaster) oviposit at communal sites where the larvae may cooperate or compete for resources depending on group size. This offers a model system to determine how females assess quantitative social information. We show that the concentration of pheromones found on a substrate increases linearly with the number of adult flies that have visited that site. Females prefer oviposition sites with pheromone concentrations corresponding to an intermediate number of previous visitors, whereas sites with low or high concentrations are unattractive. This dose-dependent decision is based on a blend of 11-cis-Vaccenyl Acetate (cVA) indicating the number of previous visitors and heptanal (a novel pheromone deriving from the oxidation of 7-Tricosene), which acts as a dose-independent co-factor. This response is mediated by detection of cVA by odorant receptor neurons Or67d and Or65a, and at least five different odorant receptor neurons for heptanal. Our results identify a mechanism allowing individuals to transform a linear increase of pheromones into a non-linear behavioral response.