Aversive Responses of Female Mice to the Odors of Parasitized Males: Neuromodulatory Mechanisms and Implications for Mate Choice

The detection and avoidance of parasitized conspecifics is proposed to have important consequences for the behavior of animals, especially as related to mate choice. A reduction in pain sensitivity (i.e. analgesia) is a major correlate of exposure to real or potential danger and threatening stimuli, facilitating the expression of various active (e.g. fleeing) and passive (e.g. immobilization) defense responses. The present study examined pain sensitivity (latency of a foot‐lifting response to 50 ° C thermal surface) of female mice, Mus musculus , that were exposed to the urine and other odor secretions of male mice subclinically infected with the naturally occurring, enteric, sporozoan parasite, Eimeria vermiformis. A 30‐min exposure to the odors of a parasitized male induced an analgesia in the female mice that was found to be mediated by the increased activity of endogenous opioid peptide systems. A brief 1‐min exposure to the male odors induced a shorter duration and lower amplitude analgesia of a non‐opioid (serotonergic) nature. Maximum analgesic responses were induced by the odors of pre‐infective [5 days post‐infection (PI)] and infective (day 10 PI) males, with significantly lower responses elicited by the odors of post‐infective (day 17 PI) male mice. Exposure to the odors of unparasitized males had no significant effects on the pain sensitivity of female mice. These results indicate that female mice can distinguish between the odors of parasitized and non‐parasitized male mice, and find the odors of parasitized males threatening and/or stressful. These odor‐induced analgesic responses and their neurohormonal correlates may be part of an adaptive preparatory defense mechanism that facilitates the detection and avoidance of parasitized males by female mice and contributes to female mate choice.