Detection and avoidance of a carnivore odor by prey

Abstract

Predator-prey relationships provide a classic paradigm for the study of innate animal behavior. Odors from carnivores elicit stereotyped fear and avoidance responses in rodents, although sensory mechanisms involved are largely unknown. Here, we identified a chemical produced by predators that activates a mouse olfactory receptor and produces an innate behavioral response. We purified this predator cue from bobcat urine and identified it to be a biogenic amine, 2-phenylethylamine. Quantitative HPLC analysis across 38 mammalian species indicates enriched 2-phenylethylamine production by numerous carnivores, with some producing >3,000-fold more than herbivores examined. Calcium imaging of neuronal responses in mouse olfactory tissue slices identified dispersed carnivore odor-selective sensory neurons that also responded to 2-phenylethylamine. Two prey species, rat and mouse, avoid a 2-phenylethylamine odor source, and loss-of-function studies involving enzymatic depletion of 2-phenylethylamine from a carnivore odor indicate it to be required for full avoidance behavior. Thus, rodent olfactory sensory neurons and chemosensory receptors have the capacity for recognizing interspecies odors. One such cue, carnivore-derived 2-phenylethylamine, is a key component of a predator odor blend that triggers hard-wired aversion circuits in the rodent brain. These data show how a single, volatile chemical detected in the environment can drive an elaborate danger-associated behavioral response in mammals.kairomone | olfaction | pheromone | trace amine-associated receptors | G protein-coupled receptor P redator-prey relationships provide a classic paradigm for understanding the molecular basis of complex behavior (1). Predator-derived visual, auditory, and olfactory cues induce hardwired defensive responses in prey that are sculpted by strong evolutionary pressure and are critical for survival. For example, odors from felines, canines, and other predators elicit innate reactions in rodents, including stereotyped avoidance behaviors and stimulation of the hypothalamic-pituitary-adrenal axis that coordinates sympathetic stress responses (1). Aversive reactions to odors can function in reverse as well, as skunk thiols facilitate prey escape by repelling predator species (2).Predator odors contain a class of ecological chemosignals termed kairomones, cues transmitted between species that benefit the detecting organism. Predator odor-derived kairomones that elicit defensive responses in rodents are largely unknown and can be found in fur, dander, saliva, urine, or feces of divergent predator species. One volatile chemical produced by foxes, 2,5-dihydro-2,4,5-trimethylthiazole (TMT), and two nonvolatile lipocalins produced by cats and rats elicit fear-like or aversive behavior in mice, enabling remote or contact-based detection of predator cues (3-5). Each of these chemicals is not broadly produced by predators, raising the possibility that rodents detect a multitude of species-specific predator signals, each of which triggers a hardwir...

Phantoms of the forest: legacy risk effects of a regionally extinct large carnivore

“…Indeed, Ferrero et al. (2011) recently showed that, contrary with noncarnivores, a large range of carnivores produce large amounts of the exact same chemical in their urine and that this chemical elicits antipredator responses in prey. Predator avoidance by prey species without prior experience to the predator is important, because innate antipredator responses will likely reduce the risk of prey populations suffer from high predation rates due to prey naivety if predators return (Berger et al.…”

High-affinity olfactory receptor for the death-associated odor cadaverine

“…In vitro studies did not identify a high-affinity cadaverine receptor among mouse, rat, or human TAARs (18), although cadaverine reportedly activates TAAR-containing glomeruli in mice at high concentrations (8). Other mammalian TAARs also detect aversive amines; for example, isoamylamine (TAAR3) and 2-phenylethylamine (TAAR4), both likewise produced by decarboxylation of amino acids (16,18,19,32). Indeed, amines are an odor group that is chemically suited both to aquatic and airborne detection.…”

“…We reasoned that a zebrafish TAAR could mediate the cadaverine avoidance behavior because several rodent TAARs detect biogenic amines, including some highly aversive odors (16,(18)(19)(20). As a result of numerous gene-duplication events, the zebrafish TAAR family is large, with 112 receptors encoded by the zebrafish genome (17).…”

“…3D for phylogenetic position of genes analyzed). We previously developed a reporter gene system to measure ligand-induced TAAR activation (16,19); here, we used this system to identify zebrafish TAAR agonists among 93 test odorants, including a large number of amines, diamines, polyamines, and amino acids.…”

Olfactory receptor genes expressed in distinct lineages are sequestered in different nuclear compartments

“…olfactory receptor genes | Taar genes | nuclear organization T he mammalian olfactory system possesses enormous discriminatory power (1,2). It can distinguish a multitude of volatile odorants as having specific odors as well as elicit innate behavioral or physiological responses (3)(4)(5)(6).…”