Z4-11Al mediates olfactory attraction and courtship in Drosophila melanogaster

Specific mate communication and recognition underlies reproduction and hence speciation. Mate communication evolves during adaptation to ecological niches and makes use of social signals and habitat cues. Our study provides new insights in Drosophila melanogaster premating olfactory communication, showing that female pheromone Z4-11Al and male pheromone cVA interact with food odour in a sex-specific manner. Furthermore, Z4-11Al, which mediates upwind flight attraction in both sexes, also elicits courtship in experienced males. Twin variants of the olfactory receptor Or69a are co-expressed in the same olfactory sensory neurons, and feed into the same glomerulus in the antennal lobe. Female pheromone Z4-11Al is perceived via Or69aB, while the food odorant (R)-linalool is a main ligand for the other variant, Or69aA. That Z4-11Al mediates courtship in experienced males, not (R)-linalool, is probably due to courtship learning. Behavioural discrimination is reflected by calcium imaging of the antennal lobe, showing distinct glomerular activation patterns by these two compounds. Male sex pheromone cVA is known to affect male and female courtship at close range, but does not elicit upwind flight attraction as a single compound, in to contrast to Z4-11Al. A blend of cVA and the food odour vinegar attracted females, while a blend of female pheromone Z4-11Al and vinegar attracted males instead. Sex-specific upwind flight attraction to blends of food volatiles and male and female pheromone, respectively, adds a new element to Drosophila olfactory premating communication and is an unambiguous paradigm for identifying the behaviourally active components, towards a more complete concept of food-pheromone odour objects.

Soaring styles of extinct giant birds and pterosaurs

The largest extinct volant birds (Pelagornis sandersi and Argentavis magnificens) and pterosaurs (Pteranodon and Quetzalcoatlus) are thought to have used wind-dependent soaring flight, similar to modern large birds. There are two types of soaring: thermal soaring, used by condors and frigatebirds, which involves the use of updrafts to ascend and then glide horizontally over the land or the sea; and dynamic soaring, used by albatrosses, which involves the use of wind speed differences with height above the sea surface. Previous studies have suggested that Pelagornis sandersi used dynamic soaring, while Argenthavis magnificens, Pteranodon, and Quetzalcoatlus used thermal soaring. However, the performance and wind speed requirements of dynamic and thermal soaring for these species have not yet been quantified comprehensively. We quantified these values using aerodynamic models and compared them with that of extant birds. For dynamic soaring, we quantified maximum flight speeds and maximum upwind flight speeds. For thermal soaring, we quantified the animal′s sinking speed circling at a given radius and how far it could glide losing a given height. Our results confirmed those from previous studies that Pteranodon and Argentavis magnificens used thermal soaring. Conversely, the results for Pelagornis sandersi and Quetzalcoatlus were contrary to those from previous studies. Pelagornis sandersi used thermal soaring, and Quetzalcoatlus had a poor ability both in dynamic and thermal soaring. Our results demonstrate the need for comprehensive assessments of performance and required wind conditions when estimating soaring styles of extinct flying species.

Flying Drosophila show sex-specific attraction to fly-labelled food

Animals searching for food and sexual partners often use odourant mixtures combining food-derived molecules and pheromones. For orientation, the vinegar fly Drosophila melanogaster uses three types of chemical cues: (i) the male volatile pheromone 11-cis-vaccenyl acetate (cVA), (ii) sex-specific cuticular hydrocarbons (CHs; and CH-derived compounds), and (iii) food-derived molecules resulting from microbiota activity. To evaluate the effects of these chemicals on odour-tracking behaviour, we tested Drosophila individuals in a wind tunnel. Upwind flight and food preference were measured in individual control males and females presented with a choice of two food sources labelled by fly lines producing varying amounts of CHs and/or cVA. The flies originated from different species or strains, or their microbiota was manipulated. We found that (i) fly-labelled food could attract—but never repel—flies; (ii) the landing frequency on fly-labelled food was positively correlated with an increased flight duration; (iii) male—but not female or non-sex-specific—CHs tended to increase the landing frequency on fly-labelled food; (iv) cVA increased female—but not male—preference for cVA-rich food; and (v) microbiota-derived compounds only affected male upwind flight latency. Therefore, sex pheromones interact with food volatile chemicals to induce sex-specific flight responses in Drosophila.

Turbulent plumes of heat, moist heat, and carbon dioxide elicit upwind anemotaxis in tsetse flies Glossina morsitans morsitans Westwood (Diptera: Glossinidae)

The roles and interactions of turbulent plumes of heat, moist heat, and carbon dioxide in mediating upwind flight of adult tsetse flies (Glossina morsitans morsitans Westwood) were investigated using a wind tunnel in a constant-environment chamber. Heat fluctuations in the plume that were detected by a thermocouple and displayed as oscilloscope traces allowed direct visualization of the structures of the plumes. Significantly more flies flew upwind when exposed to plumes of (i) carbon dioxide (0.0051% above background) and air (58% relative humidity) compared with air alone; (ii) carbon dioxide and heated air (35% relative humidity and temperature fluctuating up to 0.09°C above background) compared with carbon dioxide and air; and (iii) carbon dioxide and moist (82% relative humidity) heated air (temperature fluctuating up to 0.05°C above background) compared with carbon dioxide and heated air. However, there were no significant differences in upwind flight of flies exposed to plumes of (i) air compared with humidified air (65% relative humidity); (ii) carbon dioxide and heated air compared with heated air alone; and (iii) carbon dioxide and moist heated air compared with moist heated air alone. Recorded temperature fluctuations in heat plumes transported downwind from a tethered steer in a pasture showed patterns similar to those produced in the wind-tunnel plumes. These results suggest that host emissions of carbon dioxide alone and combined heat and moisture carried downwind by low-velocity winds elicit upwind anemotaxis in tsetse flies, which distinguish these emissions from a background of lower atmospheric levels.

Influence of odour plume structure on upwind flight of mosquitoes towards hosts

Both the concentration and the fine-scale plume structure of host odours influence the upwind flight of female mosquitoes Aedes aegypti (L.) (Diptera: Culicidae) in a wind tunnel. The attractive effects of carbon dioxide, human skin odour and l-(+)-lactic acid were tested in homogeneous, turbulent and filamentous odour plumes. With carbon dioxide, the percentage of upwind-flying mosquitoes increased with the increasing fluctuations in concentration that occur in turbulent and filamentous plumes. In homogeneous plumes, an initial activation effect was observed, but sustained upwind flights were less frequent than in the other plumes. The opposite was found with plumes of human skin odour: the highest number of mosquitoes flew upwind in the homogeneous plume, whereas in turbulent or filamentous plumes their numbers were significantly lower. Regardless of plume type, the percentage of upwind-flying mosquitoes increased with increasing concentrations of carbon dioxide and of skin odour. With l-(+)-lactic acid, the dose-response characteristics were not consistent, and the relative effects of different plume types upon upwind flights differed within different ranges of concentration. Even maximum reactions to this compound were modest compared with those to carbon dioxide or to skin odour. Our findings demonstrate (1) that mosquitoes are able to orient upwind under continuous odour stimulation and (2) that upwind flight is dependent upon plume structure in different ways for different host odour components.