Involvement of the oxytocin gene in the recognition and avoidance of parasitized males by female mice

Abstract

A major cost of social behaviour is the increased risk of exposure to parasites. Female mice discriminate between uninfected males and males infected with parasites such as the intestinal nematode Heligmosomoides polygyrus, on the basis of social cues, displaying aversive responses to the odours of infected males and preferentially mating with nonparasitized males. Here, using female mice whose gene for the neuropeptide, oxytocin (OT), has been deleted (OT knockout mice, OTKO), we show that at least one normal allele for OT is required for the discrimination, individual recognition and avoidance of H. polygyrus parasitized males on the basis of odour. In an odour choice test, female wild-type (OTWT) and heterozygous (OTHT) mice displayed a marked initial choice for the odours of uninfected males over infected males that were either familiar or novel, whereas the OTKO females showed no consistent initial choice. This was not associated with olfactory deficits because females of all three genotypes distinguished between the odours of uninfected males of varying sexual states. A 1-min exposure to the odours of infected males also induced analgesic responses (i.e. pain inhibition) in OTWT and OTHT females, with the OTKO females displaying a markedly attenuated analgesia. These analgesic responses and the associated behavioural correlates of anxiety/fear facilitate the expression of a reduced interest in and avoidance of parasitized males by females. The OTWT and OTHT, but not the OTKO females, also distinguished between the odours of novel and familiar infected males and modulated their analgesic responses on the basis of prior familiarity, displaying reduced analgesia to familiar males and enhanced analgesia to novel males. Our findings indicate that a normal OT gene is an essential part of the central mechanism whereby females can, on the basis of odour, discriminate between parasitized and nonparasitized males and, thereby, both reduce the transmission of parasites to themselves and select for parasite-free males.