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Khallaf, M. A.

Publications and source records attributed to Khallaf, M. A..

6 recordsLinked to original sources

Natural statistics of host odours predict species-specific olfactory behaviours in Drosophilids

Animals rely on olfaction to locate food, mates, and suitable habitats, yet natural odour environments contain thousands of volatile molecules, creating a high-dimensional sensory problem for both nervous systems and the researchers who study them 1-5. For example, a banana emits around 100 individual volatiles4,6. It remains unclear which components of complex odour blends animals have evolved to use as behavioural cues. Here, combining fieldwork, chemical and behavioural analyses, we show across multiple Drosophila species that behaviourally relevant cues can be predicted directly from the statistical structure of natural odour environments. Animals preferentially respond to components that are most distinctive within their natural host odour blends, and therefore most ecologically informative. These cues can be either major or minor blend components. Our results indicate that host-guided olfactory behaviours have evolved to exploit the statistical structure of natural odour environments by selectively targeting the most informative features of odour blends.

neuroscience↗

Natural evolution of intermale sexual behavior by multiple pheromone switches among Drosophila species

We have identified a Drosophila species which exhibits spontaneous and robust intermale sexual behavior. D. santomea males distinguish conspecific sexes but court both vigorously and seldom attack. Elevated intermale courtship stems from at least three evolutionarily derived pheromonal changes. In males, the sexually monomorphic cuticular pheromone 7-tricosene promotes rather than inhibits courtship and the courtship-inhibiting olfactory pheromone cVA is reduced 84-92% compared to close relatives. The third switch is in D. santomea females, where cVA suppresses rather than promotes sexual receptivity. Female cVA aversion and male cVA reduction may have co-evolved to maintain efficient intraspecific mating but prevent hybridization with the sympatric sibling species D. yakuba. High intermale courtship and low cVA also co-occur and appear selectively derived in a distant monomorphic species D. persimilis, implying pheromonal and social behavioral convergence. Changes in pheromone valence and levels may therefore explain the recent evolutionary emergence of intermale sexual behavior in Drosophila.

evolutionary biology↗

Large-scale characterization of sex pheromone communication systems in Drosophila

Insects use sex pheromones as a reproductive isolating mechanism to attract conspecifics and repel heterospecifics. Despite the profound knowledge of sex pheromones, little is known about the coevolutionary mechanisms and constraints on their production and detection. Using whole-genome sequences to infer the kinship among 99 drosophilids, we investigate how phylogenetic and chemical traits have interacted at a wide evolutionary timescale. Through a series of chemical syntheses and electrophysiological recordings, we identify 51 sex-specific compounds, many of which are detected via olfaction. Behavioral analyses reveal that many of the 42 male-specific compounds are transferred to the female during copulation and mediate female receptivity and/or male courtship inhibition. Measurement of phylogenetic signals demonstrates that sex pheromones and their cognate olfactory channels evolve rapidly and independently over evolutionary time to guarantee efficient intra- and inter-specific communication systems. Our results show how sexual isolation barriers between species can be reinforced by species-specific olfactory signals.

evolutionary biology↗

Mate discrimination among subspecies through a conserved olfactory pathway

Signaling mechanisms underlying the sexual isolation of species are poorly understood. Using four subspecies of Drosophila mojavensis as a model, we identify two behaviorally active male-specific pheromones. One functions as a conserved male anti-aphrodisiac in all subspecies and acts via gustation. The second induces female receptivity via olfaction exclusively in the two subspecies that produce it. Genetic analysis of the cognate receptor for the olfactory pheromone indicates an important role for this sensory pathway in promoting sexual isolation of subspecies, in collaboration with auditory signals. Surprisingly, the peripheral sensory pathway detecting this pheromone is conserved molecularly, physiologically and anatomically across subspecies. These observations imply that subspecies-specific behaviors arise from differential interpretation of the same peripheral cue, reminiscent of sexually conserved detection but dimorphic interpretation of male pheromones in D. melanogaster. Our results reveal that, during incipient speciation, pheromone production, detection and interpretation do not necessarily evolve in a coordinate manner.

neuroscience↗

Functional integration of \"undead\" neurons in the olfactory system

Programmed cell death (PCD) is widespread during neurodevelopment, typically eliminating the surpluses of neuronal production. Employing the Drosophila olfactory system, we examined the potential of cells fated to die to contribute to circuit evolution. Inhibition of PCD is sufficient to generate many new cells that express neural markers and exhibit odor-evoked activity. These \"undead\" neurons express a subset of olfactory receptors that, intriguingly, is enriched for recent receptor duplicates and include some normally found in other chemosensory organs and life-stages. Moreover, undead neuron axons integrate into the olfactory circuitry in the brain, forming novel receptor/glomerular couplings. Comparison of homologous olfactory lineages across drosophilids reveals natural examples of fate changes from death to a functional neuron. Finally, we provide evidence that PCD contributes to evolutionary differences in carbon dioxide-sensing circuit formation in Drosophila and mosquitoes. These results reveal the remarkable potential of alterations in PCD patterning to evolve new neural pathways.

neuroscience↗

The making of an olfactory specialist

The evolution of animal behaviour is poorly understood. Despite numerous correlations of behavioural and nervous system divergence, demonstration of the genetic basis of interspecific behavioural differences remains rare. Here we develop a novel neurogenetic model, Drosophila sechellia, a close cousin of D. melanogaster that displays profound behavioural changes linked to its extreme host fruit specialisation. Through calcium imaging, we identify olfactory pathways detecting host volatiles. Mutational analysis indicates roles for individual receptors in long- and short-range attraction. Cross-species allele transfer demonstrates that differential tuning of one receptor is important for species-specific behaviour. We identify the molecular determinants of this functional change, and characterise their behavioural significance and evolutionary origin. Circuit tracing reveals that receptor adaptations are accompanied by increased sensory pooling onto interneurons and novel central projection patterns. This work links molecular and neuronal changes to behavioural divergence and defines a powerful model for investigating nervous system evolution and speciation.

neuroscience↗