Encoding choosiness: female attraction requires prior physical contact with individual male scents in mice

Abstract

Scents, detected through both the main and vomeronasal olfactory systems, play a crucial role in regulating reproductive behaviour in many mammals. In laboratory mice, female preference for airborne urinary scents from males (detected through the main olfactory system) is learnt through association with scents detected through the vomeronasal system during contact with the scent source. This may reflect a more complex assessment of individual males than that implied by laboratory mouse studies in which individual variation has largely been eliminated. To test this, we assessed female preference between male and female urine using wild house mice with natural individual genetic variation in urinary identity signals. We confirm that females exhibit a general preference for male over female urine when able to contact urine scents. However, they are only attracted to airborne urinary volatiles from individual males whose urine they have previously contacted. Even females with a natural exposure to many individuals of both sexes fail to develop generalized attraction to airborne male scents. This implies that information gained through contact with a specific male's scent is essential to stimulate attraction, providing a new perspective on the cues and olfactory pathways involved in sex recognition and mate assessment in rodents.

Figure 1

Preference for male (M) over female (F) urine when naive females can contact urine stimuli. Females were either (a) familiar with urine from the same individuals from pre-exposure prior to the test or (b) unfamiliar with the stimuli after pre-exposure to urine from different individuals. The response is broken down into time spent sniffing the stimulus, time under the stimulus not sniffing and total time under the stimulus urine (mean+s.e., n=16). The p-values indicate Wilcoxon signed-rank tests. The log ratio of total time under the male/female stimulus did not differ between familiar and unfamiliar tests (matched-pair t-test, t₁₅=−0.89, p=0.39).

Figure 2

Preference for airborne male (M) over female (F) urinary odours according to prior exposure to urine stimuli. Prior to the preference test, naive females had pre-exposure to either airborne urinary odours (a,b) or contact with urine stimuli (c,d), where pre-exposure and test stimuli were either from the same individuals ((a,c) familiar) or from different individuals ((b,d) unfamiliar). The p-values indicate Wilcoxon signed-rank tests. Females preferred male over female airborne odours only in test (c) when they had contact with urine from the same individuals prior to the test (interaction term for log ratio in total time: F_1,30=4.16, p=0.050). The preference in test (c) differed strongly from that following contact with urine from different individual donors ((c) versus (d), matched-pair t-test of log ratio in total time, t₁₅=3.20, p=0.006), and more weakly from that following pre-exposure to airborne scent from the same individual donors ((c) versus (a), t-test: t₃₀=1.78, p=0.085).

Figure 3

Preference of socially experienced females for airborne male (M) over female (F) urinary odours. Experienced females were either (a) familiar with soiled bedding from the same individual male prior to the test or (b) unfamiliar after pre-exposure to bedding from a different individual male. The p-values indicate Wilcoxon signed-rank tests. The log ratio of total time under the male/female stimulus differed between familiar and unfamiliar tests (matched-pair t-test, t₉=3.08, p=0.013).