Abstract
The maternal environment has been shown to influence female olfactory preferences through early chemosensory experience. However, little is known about the influence of the maternal environment on chemosignals. In this study, we used two inbred mouse strains, C57BL/6 (C57) and BALB/c (BALB), and explored whether adoption could alter male chemosignals and thus influence female olfactory preferences. In Experiment 1, C57 pups were placed with BALB dams. Adult BALB females then served as the subjects in binary choice tests between paired male urine odours (BALB vs. C57, BALB vs. adopted C57 and C57 vs. adopted C57). In Experiment 2, BALB pups were placed with C57 dams, and C57 females served as the subjects in binary choice tests between paired male urine odours (C57 vs. BALB, C57 vs. adopted BALB, and BALB vs. adopted BALB). In both experiments, we found that females preferred the urine of males from different genetic backgrounds, suggesting that female olfactory preferences may be driven by genetic compatibility. Cross-fostering had subtle effects on female olfactory preferences. Although the females showed no preference between the urine odours of adopted and non-adopted males of the other strain, the BALB females preferred the urine odour of BALB males to that of adopted C57 males, whereas the C57 females showed no preference between the urine odour of C57 and adopted BALB males. Using gas chromatography-mass spectrometry (GC-MS) and stepwise discriminant analysis, we found that the ratios of volatile chemicals from urine and preputial gland secretions were altered in the fostered male mice; these changes may have resulted in the behavioural changes observed in the females. Overall, the results suggest that female mice prefer urine odours from males with different genetic backgrounds; this preference may be driven by genetic compatibility. The early maternal environment influences the chemosignals of males and thus may influence the olfactory preferences of females. Our study provides additional evidence in support of genotype-dependent maternal influences on phenotypic variability in adulthood.
Highlights
In nature, alloparental care and adoption have been documented in hundreds of mammalian and avian species [1]
We investigated whether BALB female olfactory preferences between BALB male urine and control C57 male urine were the same as those between the urine of BALB males and adopted C57 males, or vice versa
In Experiment 1, the BALB female mice were more attracted to control C57 male urine than to BALB male urine; in Experiment 2, the C57 females were more attracted to BALB male urine
Summary
Alloparental care and adoption have been documented in hundreds of mammalian and avian species [1]. Maternal effects are plastic, and maternal provisioning is often influenced by the genotype of the offspring [2,3,4,5,6,7,12]. Males are more susceptible to maternal effects than females [8,13]. Olfactory-mediated kin recognition is affected by the maternal environment, such that genotypic cues are learned through early chemosensory experiences. Females avoid mating with males carrying the major histocompatibility complex (MHC) alleles of their foster family rather than of their natural family, suggesting that familial imprinting determines their preferences [2,14]. Female olfactory preferences primarily rely on the assessment of male chemosignals, but whether the maternal environment can alter the chemosignals of males and influence female choice remains unknown
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