Flies live in an intensely olfactory world. Tracking mates and homing in on treats, flies are guided by their keen sense of smell. Explaining that flies turn constantly when exploring to locate luscious odours, Sara Wasserman from the University of California Los Angeles, USA, adds that when vinegar flies latch onto an attractive odour trail – such as apple cider vinegar – they stop turning, align their antennae with the steepest gradient of the odour, and track the plume until it guides them to the source. But how would the same insect react when faced with a repulsive odour? Would it turn randomly in a bid to evade the stench or would it latch on to the plume, but pursue it in the opposite direction, anti-tracking it as it became increasingly dilute? ‘We thought they would just avoid the area where the aversive odour was coming from’, recalled Wasserman, so she and her colleagues tested vinegar flies' responses to an odour that the insects find particularly repulsive: benzaldehyde (p. 2833).

Describing the high-tech flight arena where she and her colleagues, Patrick Lu, Jacob Aptekar and Mark Frye, tested the insect's aversive behaviour, Wasserman says, ‘We give the flies an odour and look at where they orient.’ Gently gluing a small pin to a fly's back and attaching it to a frictionless magnetic bearing that allowed the fly to swivel and change direction, Wasserman generated a plume of unpleasant benzaldehyde odour that wafted over the fly and watched the insect's response. Amazingly, it instantly turned tail and tried to head away from the odour, following the direction of the plume.

‘I ran and got Mark and showed him and we both said, “Let's see 10 more flies”’, recalls Wasserman, who couldn't believe the clear-cut response. However, all of the subsequent flies reacted in the same way: the insects were anti-tracking the plume to evade the odour. Could they be using the same mechanism to avoid repellent odours as they use to track attractive scents, but simply switching the direction of their response? Knowing that the flies found it difficult to position themselves correctly in an attractive plume when the odour receptors on one antenna were blocked with glue – effectively blocking one ‘nostril’ – the team decided to test how flies with a blocked antenna reacted to a jet of repellent benzaldehyde to see whether they were using the same tracking algorithm as the flies without blocked antennae. Dabbing a spot of glue on the third segment of one of the fly's antennae and positioning it sideways across the odour current, Wasserman saw that the blocked flies were unable to antitrack the repulsive odour – just like the blocked flies in an attractive plume.

Finally, she secured flies to a rigid tether – where she could control the movement of the fly's visual world in response to their flight patterns to find out how visually alert they were – and found that the odour increased the fly's alertness, while the visual environment affected their ability to anti-track the repellent plume. ‘This suggests that they utilise the same underlying strategy for tracking an attractive odour and an aversive odour and they just flip the sign somewhere, depending on whether they find it attractive or aversive’, says Wasserman, who is keen to locate the neural switch in order to better understand how flies integrate sensory stimuli.

J. W.
M. A.
Flies dynamically anti-track, rather than ballistically escape, aversive odor during flight
J. Exp. Biol.