Scent-marking by male mammals: Cheat-proof signals to competitors and mates

Abstract

Scent-marking is a ubiquitous form of olfactory signaling in male mammals and both territorial males in resource-defense mating systems and dominant males in dominance mating systems scent-mark. A large body of evidence suggests a link between scent-marking by male mammals and intrasexual competition. Resource holders appear to mark to help establish and maintain their status. They may do this because scent marks allow potential opponents to assess the status or RHP of the signaler. Nonresource holding competitors benefit because they can adjust the level of escalation in relation to potential costs and benefits and avoid risky contests. Resource holders benefit through reduced costs because many nonresource holders withdraw to avoid escalated contests. Three basic mechanisms allow receivers to make decisions after detecting scent marks. Receivers may (1) detect intrinsic properties of scent marks (e.g., concentrations of androgen-dependent volatiles), (2) remember past contests and the odor of each individual involved and associate these with the odor of scent marks, and (3) remember the smell of marks recently encountered and match this smell with potential opponents that they meet subsequently. It is now known that all of these mechanisms are used, sometimes within one species (e.g., mice) and we argue that the mechanisms are used conditionally, depending on information available and potential costs and benefits to receivers. Game theoretical analysis has recently shown how territorial intruders may switch from using intrinsic properties of marks to scent-matching when making decision about whether to remain in a territory. Scent-marking may be a uniquely cheat-proof signal of status because males must be able to defend their territory or dominance status over the time taken to mark it. A pattern of marks is thus a signal of status that has been tested in intrasexual competition. It also seems likely that marks are intrinsically costly both in energetic terms and by increasing predation risk. Mice can detect whether urine is from a parasitized or nonparasitized individual and these odors could potentially signal immunocompetence if mediated by variation at the MHC region of the genome. This remains to be tested. It is known that mice can detect relatedness via urine volatiles mediated by the MHC and it has been predicted that males should modify their competitive behavior in the light of this information. Again this remains to be tested. Information about disease status and genetic relatedness does not explain why males maintain patterns of scent marks. Most, perhaps all, territories are scent-marked. This may be because most intruders are of lower RHP than resource holders and these males should usually withdraw after assessing the resource holder by its scent marks. The costs of defending a territory may thus be substantially reduced. The obligate link between scent-marking and territoriality suggests that resource-defense polygyny in mammals may not be economically viable without this reduction in the costs of area defense. A little information is available to show that females use information from patterns of scent marks and a great deal of information shows that they use intrinsic information. It is not known whether males signal to females to enable mate choice or if females eavesdrop on signals sent between male competitors. Most known responses are to male urine by female rodents. For example, females show physiological (priming) responses to male odors (e.g., advancing and synchronizing estrus, inducing abortion). Other research has identified factors responsible for female mate preferences in choice tests. For example, the dominance status of the signaling male is a predictor of female interest and such studies have identified androgen-dependent volatiles responsible for the response. More recently, females have been shown to use odor mediated by the MHC locus to choose mates in relation to their genetic relatedness and to use odor to distinguish healthy and diseased mates. Most of these studies have been on mice and most use male urine, but the effect of patterns of urine scent marks has not been investigated. The only studies that explicitly use scent marks are those showing that females match the odor of potential mates with marks previously found in the environment to select mates. Future research should aim to clarify how information about the quality of potential mates is transmitted and how females trade-off such information against genetic relatedness.