Do fruit flies group together the same odors that humans find similar? A 2007 study found some shared patterns in odor intensity between humans and flies, but differences in which odors were grouped as similar.
The researchers developed two methods for measuring the movements of individual flies and examined responses to many odors, the effects of losing particular odorant receptors, and comparisons with humans. The study asked whether odor qualities depend not only on molecules but also on the olfactory system receiving them.
Flies answer through behavior rather than words
People can be asked which odor is stronger or which odors resemble one another. Since flies cannot be asked the same questions directly, the researchers developed two kinds of behavioral measurement.
In the first, a fly in a circular arena received clean air for two minutes, followed by odor-containing air for four minutes. Video recordings measured its movements to determine how much its activity changed when the odor arrived.
In the second, an odor sample was placed against the wall of a Petri dish. The fly’s position was tracked for three minutes to measure changes in its distance from the odor source. A fly may respond differently to the same odor when it fills the surrounding space than when the fly can move toward or away from its source.
Responses extended well beyond fruity odors
Across the two methods, flies showed behavioral responses to 70 of the 73 odors tested. They responded not only to alcohols and esters found in fruit, but also to plant-derived substances with various molecular structures.
Significant responses occurred for 44 of 62 odors in the airflow experiment and 61 of 69 in the stationary-source experiment. The time courses also differed: some odors caused an initial rise in activity followed by settling, others produced sustained responses, and still others caused activity to increase over time.
Even after the antennae, the main olfactory organs, were removed, flies retaining another olfactory organ, the maxillary palps, responded to approximately 61% of the 59 odors tested. This suggests that even a small number of receptors may support responses to a fairly broad range of odors.
The study did not support a narrow picture of fly olfaction as dealing only with fruit odors. At the same time, the authors noted that an odor is not invariably attractive or unpleasant to a fly: responses depend on concentration, states such as hunger, and the task being measured.
Losing one receptor does not always produce the expected change
Next, the researchers examined flies lacking particular odorant receptors. In flies missing a genomic region that includes Or22a, the behavioral response to 1-heptanol was reduced among the 23 odors tested. This molecule was a relatively weak stimulus for Or22a, rather than a particularly strong one. Esters that strongly stimulate the receptor did not show the same reduction.
In flies lacking another receptor, Or43b, responses to D-carvone and L-limonene were instead increased among the 29 odors tested. This change was not seen for their mirror-image counterparts, L-carvone and D-limonene.
Thus, losing a receptor did not simply weaken behavior most strongly toward the odor that best activates that receptor. The authors proposed possible explanations involving compensation by multiple receptors responding to the same molecule and changes in the combination of inputs. These were behavioral results at the tested concentrations; losing a receptor might have different effects at other concentrations.
Intensity rankings agreed in 72% of comparisons
In the human experiment, 29 people arranged sample bottles from weakest to strongest. For flies, changes in movement when an odor was delivered served as an intensity indicator.
When pairs of substances within the same chemical group were compared for which was stronger, human and fly rankings agreed in 72% of comparisons. For example, among aldehydes and acetate esters, more volatile substances tended to rank as stronger in both species. Alcohols showed a trend in the opposite direction.
There were exceptions. Humans perceived 1-heptanol as strong, but flies showed no significant behavioral response in this airflow condition. Methyl acetate produced a large response in flies but ranked toward the weaker end for humans.
The figure of 72% does not describe how often humans and flies experience odors in the same way overall. It comes from pairwise comparisons of stronger and weaker odors within chemical groups, comparing human intensity rankings with an indicator based on fly activity.
Different groupings of similar odors
Nine odors were used to compare similarity. Twenty-seven human participants freely grouped sample bottles according to perceived resemblance. Rather than choosing from a list of descriptive words, participants also decided how many groups to make.
For flies, the researchers first exposed them to one odor for 30 minutes, then measured their response to another. They inferred relationships between odors through cross-adaptation: how much adapting to one odor changed the response to the other.
Ethyl hexanoate offers a clear example. Humans tended to place this substance apart from the other esters, assigning it to a group of its own in 43% of classifications. In contrast, the analysis based on fly cross-adaptation grouped it closely with butyl acetate and isoamyl acetate.
The paper describes these three compounds as banana-like, but the experiment did not test whether flies recognized “banana.” Moreover, in the fly classification tree, it was mainly this three-compound grouping that was statistically stable; there are limits to treating every branch as conclusive.
The measurement methods themselves also differed: direct grouping by humans versus behavioral changes after adaptation in flies. With those conditions in mind, the authors suggest that animals with different combinations of receptors may also differ in which odors they find similar.
Summary
The two new behavioral methods showed that fruit flies responded to 70 of 73 odors, demonstrating broad responses extending beyond fruity smells. The effects of losing particular receptors were small and could not be predicted simply from the known strength of those receptors’ responses.
In comparisons with humans, intensity rankings agreed for many pairs, but groupings of similar odors differed for substances such as ethyl hexanoate. Understanding fragrance requires attention not only to molecular structure, but also to the olfactory system receiving it and to the behavior or judgment being measured.
The research was supported by US NIH funding and a Marco S. Stoffel research fellowship. The authors declared no conflicts of interest.
Reference
Keller A, Vosshall LB. Influence of odorant receptor repertoire on odor perception in humans and fruit flies. Proceedings of the National Academy of Sciences. 2007;104(13):5614–5619. doi:10.1073/pnas.0605321104. Full text from the authors’ institution.
