Abstract
In the wild, animals have developed survival strategies relying on their senses. The individual ability to identify threatening situations is crucial and leads to increase in the overall fitness of the species. Rodents, for example have developed in their nasal cavities specialized olfactory neurons implicated in the detection of volatile cues encoding for impending danger such as predator scents or alarm pheromones. In particular, the neurons of the Grueneberg ganglion (GG), an olfactory subsystem, are implicated in the detection of danger cues sharing a similar chemical signature, a heterocyclic sulfur- or nitrogen-containing motif. Here we used a “from the wild to the lab” approach to identify new molecules that are involuntarily emitted by predators and that initiate fear-related responses in the recipient animal, the putative prey. We collected urines from carnivores as sources of predator scents and first verified their impact on the blood pressure of the mice. With this approach, the urine of the mountain lion emerged as the most potent source of chemical stress. We then identified in this biological fluid, new volatile cues with characteristic GG-related fingerprints, in particular the methylated pyridine structures, 2,4-lutidine and its analogs. We finally verified their encoded danger quality and demonstrated their ability to mimic the effects of the predator urine on GG neurons, on mice blood pressure and in behavioral experiments. In summary, we were able to identify here, with the use of an integrative approach, new relevant molecules, the pyridine analogs, implicated in interspecies danger communication.
Highlights
Predators and preys interact actively and continuously using their senses to find food or to avoid being eaten (Kavaliers and Choleris, 2001)
We took advantage of a rapid and non-invasive experimental strategy to screen bioreactive predator urines (Figure 1) by measuring the elevation of mice blood pressure with the tail-cuff approach (Figure 1A) (Krege et al, 1995). We first challenged this method by measuring the variation of the blood pressure of mice exposed to 1% TMT, a potent red fox-derived kairomone known to elicit fear in rodents (Fendt et al, 2005; Horii et al, 2010, 2013; Hacquemand et al, 2013; Takahashi, 2014)
The mountain lion emerged (Figure 1E) as the most potent source of volatile kairomones across the tested carnivore urines as its presence significantly increased mice blood pressures nearly by 15% compared to the control level for the systolic
Summary
Predators and preys interact actively and continuously using their senses to find food or to avoid being eaten (Kavaliers and Choleris, 2001). Profound behavioral alterations as well as modulation of essential physiological conditions such as the increase of stress-related hormones or the elevation of the blood pressure of the preys have been, for example, observed in the presence of these predator scents (Dielenberg and McGregor, 2001; Horii et al, 2010; Takahashi, 2014). Small volatile kairomones are mainly detected by sensory neurons found in the main olfactory epithelium (MOE) or in the Grueneberg ganglion (GG) subsystems Kairomones may have their physiological effects in preys as single chemical cues. The 2,4,5-trimethylthiazoline (TMT) found in red fox feces (Fendt et al, 2005) is a robust single volatile kairomone that is detected concomitantly by the dorsal MOE (Kobayakawa et al, 2007) as well as by the GG (Brechbühl et al, 2013b) to further initiate important behavioral effects (Perez-Gomez et al, 2015)
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