The female pheromone (Z)-4-undecenal mediates flight 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 (Z)-4-undecenal (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. 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.

特定的配偶交流与识别是繁殖乃至物种形成的基础。配偶交流在对生态位的适应过程中演化，并依托社会信号与生境线索完成信息传递。本研究针对黑腹果蝇（Drosophila melanogaster）的交配前嗅觉交流展开探究，揭示了雌性信息素(Z)-4-十一碳烯醛[(Z)-4-undecenal, 简称Z4-11Al]与雄性信息素cVA可通过性别特异性方式与食物气味发生相互作用。此外，可介导两性逆风飞行趋性的Z4-11Al，还能唤起经验丰富雄性的求偶行为。嗅觉受体Or69a的两种同源变异亚型，可在同一嗅觉感觉神经元中共表达，并投射至触角叶的同一个肾小球。Z4-11Al可通过Or69aB被感知，而食物气味分子(R)-芳樟醇[(R)-linalool]则是另一变异亚型Or69aA的主要配体。Z4-11Al可唤起经验雄性的求偶行为，而(R)-芳樟醇则无此效应，这一现象或源于求偶学习过程。这两种化合物可引发触角叶截然不同的肾小球激活模式，这一钙成像结果也印证了行为层面的识别差异。已知雄性信息素cVA可在近距离范围内影响雌雄个体的求偶行为，但与Z4-11Al不同，单一的cVA无法引发逆风飞行趋性。cVA与食物气味醋的混合组分可吸引雌性，而雌性信息素Z4-11Al与醋的混合组分则可吸引雄性。分别针对食物挥发物与雌雄信息素的混合组分所展现出的性别特异性逆风飞行趋性，为黑腹果蝇的交配前嗅觉交流研究增添了全新维度，同时也为鉴定行为活性组分提供了明确的研究范式，有助于构建更为完整的食物-信息素气味对象概念。