A mammalian blood odor component serves as an approach-avoidance cue across phylum border - from flies to humans

Abstract

Chemosignals are used by predators to localize prey and by prey to avoid predators. These cues vary between species, but the odor of blood seems to be an exception and suggests the presence of an evolutionarily conserved chemosensory cue within the blood odor mixture. A blood odor component, E2D, has been shown to trigger approach responses identical to those triggered by the full blood odor in mammalian carnivores and as such, is a key candidate as a food/alarm cue in blood. Using a multidisciplinary approach, we demonstrate that E2D holds the dual function of affecting both approach and avoidance behavior in a predator-prey predicted manner. E2D evokes approach responses in two taxonomically distant blood-seeking predators, Stable fly and Wolf, while evoking avoidance responses in the prey species Mouse. We extend this by demonstrating that this chemical cue is preserved in humans as well; E2D induces postural avoidance, increases physiological arousal, and enhances visual perception of affective stimuli. This is the first demonstration of a single chemical cue with the dual function of guiding both approach and avoidance in a predator-prey predicted manner across taxonomically distant species, as well as the first known chemosignal that affects both human and non-human animals alike.

Figure 1

The odor of E2D is sufficient to elicit approach response in blood-seeking animals. (A) Chemical structure of trans-4,5-epoxy-(E)-2-decenal (E2D). (B) Schematic drawing of the Y maze olfactory assay used for the fly behavioral experiment. (C) Mean percentage of flies choosing between E2D in a background of host odor and host odor only (left) and between E2D and cattle blood both in a host background. (D) A wolf displaying biting on the scented log, one of the eleven behaviors present in the ethogram. (E) Mean total number of interactions during a session with the four odor stimuli for the wolf pack. Error bars indicate standard error of the mean (SEM). *p < 0.05, ***p < 0.001.

Figure 2

E2D induces avoidance behavior in the prey species mouse and in human participants. (A) Upper panel: A mouse displaying aversion towards E2D. Lower panel: mean aversion index of the time spent in the non-odorized compartments. (B) A human participant standing on the force platform measuring approach (anterior)-avoidance (posterior). (C) Mean total movement (cm) in the anterior-posterior direction as a function of E2D, and the control odors trans-2-decenal (T2D) and butanol (BUT). (D) Mean GSR signal as a function of E2D, T2D and BUT. (E) Mean visual reaction time to affective faces in human participants as function of E2D, BUT, and odorless control. Error bars indicate s.e.m. *p < 0.05, **p < 0.01, ***p < 0.001.