Cross-Fostering of Male Mice Subtly Affects Female Olfactory Preferences

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.     

Brief exposure to the odour of a parasitized male alters the subsequent mate odour responses of female mice

Parasites can affect mate choice, with females preferentially selecting parasite-free males. Prior exposure to, or experience with, males has also been suggested to influence mate responses. Here, we examined the effects of an immediate, brief (1 or 15 min) pre-exposure to the urinary and associated odours of either an uninfected male house mouse,Mus domesticus , or a male infected with the natural murine nematode parasite, Heligomosomoides polygyrus, on the subsequent responses of female mice to the odours of infected and uninfected males. Using an odour preference test we found that females displayed a marked overall preference for the odours of uninfected males. Pre-exposure to the odours of a parasitized male decreased female preference for nonparasitized males and increased female preference for parasitized males. This ‘prior male’ effect was evident for both the total odour preference and initial odour choice. Females pre-exposed to the odour of a parasitized male displayed decreased choosiness and made no particular initial choice of a male, while still maintaining an overall preference for the odours of uninfected males. These shifts in initial choice and odour preference were not directly associated with either female stress responses or stress-related odour cues of the males. Our findings show that female mice can distinguish between parasitized and nonparasitized males on the basis of odour and suggest that a brief exposure to the odours of infected males influences females' immediate odour preferences, and their subsequent preference for and choice of males. This rapid, infection-associated ‘prior male’ effect may contribute to the reported variations in female mate preference and choice. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

Pheromonal Recognition of Females Takes Precedence over the Chromatic Cue in Male Iberian Wall Lizards Podarcis hispanica

Sex recognition is based on colour signals in many species of lizards. However, olfactory stimuli are also clearly involved, and many species might rely more on chemoreception. We aimed to examine whether colour pattern or odours, or both, are used in sex recognition and which cues elicit courtship of females by males of the lizard Podarcis hispanica . We experimentally manipulated the coloration and odour of female P. hispanica , thereby creating groups with all combinations between coloration and odour of males and females. Using data from staged encounters, we compared the responses of resident males to manipulated and unmanipulated individuals (males and females). Responding males reacted significantly more aggressively to female intruders with male odours, independently of their coloration. Nevertheless, coloration seemed to be important in long-distance sex recognition since, in the first minutes, females painted as females received a lower number of aggressive responses. Both colour and odour were important in eliciting male courtship. However, females painted as females and with female odours were preferentially courted. Comparisons with unmanipulated male and female intruders agreed with these expectations. Therefore, at close range, odoriferous cues seem to be more important than colour patterns in sex recognition, but female coloration is also useful at long range to deter the aggressive response of males and to elicit courtship in conjunction with odours.     

Smelling chemosensory signals of males in anxious versus nonanxious condition increases state anxiety of female subjects

The hypothesis of this experiment was that humans in an anxious state compared with a nonanxious state are able to increase anxiety levels in other humans via their body odors. Specifically, we hypothesized that male chemosensory anxiety signals compared with neutral chemosignals increase state anxiety of female subjects. Thirteen male subjects participated in 2 different sweat donation sessions: chemosignals were collected during participation in a high rope course (anxiety condition) and in an ergometer workout (neutral condition). State and trait anxiety were evaluated in 20 female odor recipients using Spielberger's state-trait anxiety inventory in a double-blind design. Comparison of state anxiety of odor donors between control and anxiety condition differed significantly indicating that our model of anxiety induction successfully led to the expected change in emotion. Comparison of state anxiety of odor recipients showed a trend toward higher state anxiety in the anxiety condition compared with the neutral condition after 5 min of odor exposure. After 20 min of odor exposure, state anxiety of female subjects was significantly higher during the perception of sweat collected during the anxiety condition in comparison with the perception of sweat collected during the neutral condition. This experiment gives evidence that male anxiety chemosignals compared with neutral chemosignals are capable of inducing an increased state anxiety in female subjects.     

MHC-correlated odour preferences in humans and the use of oral contraceptives

Previous studies in animals and humans show that genes in the major histocompatibility complex (MHC) influence individual odours and that females often prefer odour of MHC-dissimilar males, perhaps to increase offspring heterozygosity or reduce inbreeding. Women using oral hormonal contraceptives have been reported to have the opposite preference, raising the possibility that oral contraceptives alter female preference towards MHC similarity, with possible fertility costs. Here we test directly whether contraceptive pill use alters odour preferences using a longitudinal design in which women were tested before and after initiating pill use; a control group of non-users were tested with a comparable interval between test sessions. In contrast to some previous studies, there was no significant difference in ratings between odours of MHC-dissimilar and MHC-similar men among women during the follicular cycle phase. However, single women preferred odours of MHC-similar men, while women in relationships preferred odours of MHC-dissimilar men, a result consistent with studies in other species, suggesting that paired females may seek to improve offspring quality through extra-pair partnerships. Across tests, we found a significant preference shift towards MHC similarity associated with pill use, which was not evident in the control group. If odour plays a role in human mate choice, our results suggest that contraceptive pill use could disrupt disassortative mate preferences.     

Seasonal control of odour preferences of meadow voles (Microtus pennsylvanicus) by photoperiod and ovarian hormones

During the spring-summer breeding season, female meadow voles prefer odours of males over those of females, but in the autumn-winter season of reproductive quiescence this preference is reversed. Females housed in long (14 h light/day) and short (10 h light/day) photoperiods, respectively, had odour preferences comparable to those of spring and autumn voles, respectively. The preference of long-photoperiod voles for male over female odours was reversed by ovariectomy and restored by treatment with oestradiol. By contrast, neither ovariectomy nor oestradiol affected odour preferences of short-photoperiod voles. Long days appear to influence olfactory preferences by altering ovarian hormone secretion. The failure of oestradiol to affect odour preferences in short photoperiods suggests that the neural substrates mediating this behavioural response are refractory to oestrogens during the nonbreeding season.     

Odour–genes covariance within a natural population of subterranean Spalax galili blind mole rats

Previous research, using habituation techniques with multiple rodent species as subjects, has demonstrated (from kin to across species) the greater perceptual similarity in the qualities of individual odours of more closely genetically related individuals ('odour–genes covariance', abbreviated 'OGC'). This predictable relationship between individual genotypes and individual odours has only been assessed in rodents in which the genetic similarities and dissimilarities are known either through laboratory breeding or by selecting odour donors from different populations or species. To study OGC within a natural population of rodents, we genotyped Spalax galili blind mole rats using ten microsatellite markers, and conducted pairwise genetic distance comparisons to estimate genetic similarity and to calculate the relatedness coefficient between pairs of individuals. We then used habituation-generalization techniques to assess whether perceived odour similarities covaried with the genetic similarities we had identified. Indeed, animals treated odours from genetically closer donors as more similar than odours from less genetically similar donors. The results suggest an accurate and subtle ability to resolve genetically determined odour distinctions among familially unrelated animals within a population. Graded differential responses to conspecific odours based on degrees of similarity between other individuals' odours and one's own have been demonstrated in kinship and species discriminations and preferences. The evidence presented here provides the basis for hypothesizing a similar process that could promote optimal outbreeding and inclusive fitness within populations of conspecifics. The evolutionary implications of these findings are discussed.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 483–490.     

幼小鼠对种内几种化学信息的识别和反应

50年代以来,国际上相继开展了一些关于化学信息在小家鼠繁殖中作用的研究,并在实验室中揭示了一些反应:如集群雌鼠气味使雌鼠性周期延长的Lee-Boot效应,雌鼠气味能解除集群雌鼠对性周期的抑制、并促使它们同期发情的Whitten效应,以及陌生雄鼠气味中断妊娠的Bruce效应等等。但是,在成鼠间起作用的几种化学信息,是否能被幼鼠感受,对幼鼠的发育和性成熟是否产生影响,还是一个未知的问题。 影响小鼠发育的因素很多,除环境因子外,近来还出现了有关社群因素中外激素对小鼠性成熟影响的报道,发现雄鼠或给予雄激素的雌鼠有促进幼雌鼠性成熟的作用,范志勤发现父本气味和陌生雄鼠气味对幼雌鼠性成熟均有促进作用。但是,目前关于种内雌鼠气味、集群雌鼠气味、幼鼠气味影响性成熟的研究尚不多见。有关各种气味对性成熟效应的比较的报道亦少。本文的目的在于通过实验方法,阐明种内的几种化学信息,诸如父本、陌生雄性、雌性、集群雌性、幼雌等几种气味,对幼雌小鼠性成熟的影响,并据此了解幼鼠识别这几种信息的能力。     

Reliability of odour–genes covariance despite diet changes: a test in mound‐building mice

Odour–genes covariance (i.e. that individual odour similarities covary with genetic similarity) allows animals to assess their genetic relatedness to one another by comparing the similarities between their individual odours. The reliability of the odour–gene covariance phenomenon under environmental changes has not yet been explored. Using an innovative habituation‐generalization procedure, we tested whether the modifications of body odours induced by a change in diet interfered with the perceived similarity of individual odours of more genetically similar individuals. The effects of a change in diet, by adding aniseed flavour to the drinking water, was assessed in male mound‐building mice, a species in which odour–genes covariance has already been demonstrated. The results obtained indicate that mice perceive more similarities in the odours of sibling males than in those of nonrelatives, despite the effects of diet on body odours. We suggest that the reliability of signals arising from odour–genes covariance is likely a result of the independence between traits indicating genetic relatedness and indicator signals of biological states (e.g. diet) in body odours. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 682–688.     

Olfactory communication and the importance of different odour sources in the ferret (Mustela putorius f. furo)

Olfactory communication has a major role in solitary carnivores, particularly during the breeding season. Scent-marking behaviour in ferret (Mustela putorius f. furo) has been well studied, but not the significance of the deposited odours for the animal. We compared the interest in urogenital, anal and body odours of opposite-sex conspecifics between male and female ferrets and investigated both sexes’ discrimination ability (familiar vs. unfamiliar) for these three opposite-sex odours and the use of its ability by females during the breeding season. Males are more interested than females in the urogenital odour of the opposite sex. Male body odour probably did not interest females and males are somewhat interested in the female one. However, anal odour of the opposite sex is as interesting for males as for females and both sexes are able to discriminate familiar anal odour from an unfamiliar one. Moreover, females could use this ability when they must choose to have some sensory contact between olfactory familiar and unfamiliar males since they prefer to be in contact with the former. These results are coherent with behavioural differences observed between male and female solitary mustelids in the field and in captivity, and the consortship success of resident males compared to roaming males.     

Parasitized female mice display reduced aversive responses to the odours of infected males.

The present study showed that parasites influence both the responses of uninfected females to males and the responses of female hosts to infected males. In female laboratory mice one of the consequences of exposure to the olfactory cues associated with an infected male was a reduction of the reactivity to a thermal surface, i.e. pain inhibition or analgaesia. Uninfected oestrous and non-oestrous female mice displayed marked analgaesic responses after exposure to the odours of males infected with either the enteric single-host nematode parasite, Heligmosomoides polygyrus, or the protozoan parasite, Eimeria vermiformis. The uninfected oestrous females distinguished between infected and physically stressed males, displaying a greater analgaesic response to the odours of infected males. These analgaesic responses and their anxiety/ fearfulness-associated behavioural correlates could elicit either a reduced interest in, or avoidance of, parasitized males by females. Oestrous female mice infected with H. polygyrus displayed a reduced analgaesic response to the odours of the infected males and differentially responded to the odours of males infected with either the same (H. polygyrus) or a different parasite (E. vermiformis). An exposure time of 1 min elicited minimal responses to the odours of males infected with the same parasite, H. polygyrus, and an attenuated, though significant, non-opioid peptide-mediated analgaesic response to males infected with E. vermiformis. An exposure time of 30 min elicited similar markedly reduced endogenous opioid peptide-mediated analgaesic responses to the odours of both of the categories of infected males. The responses to the odours of a stressed male were, however, unaffected by the parasitic infection. The reduced analgaesic responses of the parasitized females to the odours of infected males may involve either enhanced odour familiarity and responses to group odour templates and/or neuromodulatory shifts resulting in reduced fearfulness and potentially greater interest in the infected males.     

Host odours enhance the responses of adult Rhyzopertha dominica to male-produced aggregation pheromone

The behavioural responses of adult male and female Rhyzopertha dominica (Coleoptera, Bostrichidae) to blends of host volatiles and male-produced aggregation pheromone were observed in a four-arm airflow olfactometer. The odour sources used were five pheromone-releasing males each on a single maize grain (lower maize-volatiles blend), five pheromone-releasing males on 500 g of maize (higher maize-volatiles blend) or the host volatiles emanating from 500g of maize (maize volatiles alone). Multiple-choice tests, in which volatiles from all three odour sources were presented in the exposure chamber at the same time, were used to study odour preferences of the males and females. Both sexes showed strongest attraction to the higher maize volatile blend but there were significant sex differences in response to the odour sources. Males spent significantly more time than females in the zone with only maize volatiles, and females spent significantly more time in the higher maize-volatiles zone. However, when odour sources were offered singly, females gave numerically greater responses than males to all sources although this difference was statistically significant for only the lower maize-volatiles blend. As males are more attracted than females to host odours alone it is suggested that they may be more highly adapted to seek out new hosts while females are more inclined to locate a food source by following the pheromone signals produced by males. However, both sexes responded most strongly to the odour source comprising aggregation pheromone with the higher proportion of maize volatiles.     

Balance hypothesis of action of socially significant volatile chemosignals on reactivity of chromosome machinery of the bone marrow dividing cells in the house mouse Mus domesticus L

Volatile chemosignals released by female CBA laboratory mice have been shown to produce action of different direction, depending on conditions of performance of experiment, on chromosome machinery of bone marrow cells in syngenic adult males. Thus, chemosignals secreted into environment by isolated adult females decrease frequency of mitotic disturbances in bone marrow dividing cells in male recipients as compared with spontaneous level in control animals. At the same time, 2,5-dimethylpyrazine - pheronome released only by high density caged females - increases frequency of mitotic disturbances. Preliminary 24-h-long action of chemosignals of isolated females decreases effect of the subsequent action of 2,5-dimethylpyrazine, although the level of disturbances exceeds that in control animals. The simultaneous action of used chemosignals neutralizes completely the 2,5-dimethylpyrazine action, the frequency of mitotic disturbances being not different from that after chemosignals of isolated females. The hypothesis is put forward about dependence of the revealed cytogenetic effects in male recipients on zoosocial conditions of maintenance of female donors of chemocommunication signals.     

鳄蜥对熟悉和陌生个体气味的辨别

个体辨别对于减少同种争斗以及配偶选择具有重要意义。我们用棉棒粘取鳄蜥(Shinisaurus crocodilurus)尿液作为气味源,以香水作为对照,测定鳄蜥对熟悉个体气味、陌生个体气味以及香水的舔舌次数和舔舌潜伏期,来探讨鳄蜥通过化学信息辨别熟悉和陌生个体的能力。结果显示,不论是雌性还是雄性,对不同个体尿液的舔舌次数均显著高于对香水的,舔舌潜伏期显著短于香水的;尽管雄性对陌生同性个体气味与熟悉同性个体气味的舔舌次数无显著差异,但对前者的舔舌潜伏期显著短于后者;雄性对陌生雌性气味的舔舌次数显著多于熟悉雌性气味的,对前者的舔舌潜伏期显著短于后者;雌性对陌生雄性气味的舔舌潜伏期显著短于对熟悉雄性气味的;雄鳄蜥对陌生雌性气味的舔舌次数显著多于雌鳄蜥对陌生雄性的。结果表明,鳄蜥能辨别同种个体的化学信息,并能通过化学信息来辨别熟悉和陌生个体,推测鳄蜥的这种辨别能力对其领域分配以及繁殖交配有重要作用。     

Confusing tastes and smells: how odours can influence the perception of sweet and sour tastes

This study investigated the relationship between perception of an odour when smelled and the taste of a solution to which the odour is added as a flavorant. In Experiment 1 (E1) sweetness, sourness, liking and intensity ratings were obtained for 20 odours. Taste ratings were then obtained for sucrose solutions to which the odours had been added as flavorants. Certain odours were found to enhance tasted sweetness while others suppressed it. The degree to which an odour smelled sweet was the best predictor of the taste ratings. These findings were extended in Experiment 2 (E2), which included a second tastant, citric acid, and employed four odours from E1. The most sweet smelling odour, caramel, was found to suppress the sourness of citric acid and, as in E1, to enhance the sweetness of sucrose. Again, odours with low sweetness suppressed the sweetness of tasted sucrose. The study demonstrated that the effects of odours on taste perception are not limited to sweetness enhancement and apply to sour as well as sweet tastes. The overall pattern of results is consistent with an explanation of the taste properties of odours in terms of prior flavour-taste associations.     

Human Gender Differences in the Perception of Conspecific Alarm Chemosensory Cues

It has previously been established that, in threatening situations, animals use alarm pheromones to communicate danger. There is emerging evidence of analogous chemosensory “stress” cues in humans. For this study, we collected alarm and exercise sweat from “donors,” extracted it, pooled it and presented it to 16 unrelated “detector” subjects undergoing fMRI. The fMRI protocol consisted of four stimulus runs, with each combination of stimulus condition and donor gender represented four times. Because olfactory stimuli do not follow the canonical hemodynamic response, we used a model-free approach. We performed minimal preprocessing and worked directly with block-average time series and step-function estimates. We found that, while male stress sweat produced a comparably strong emotional response in both detector genders, female stress sweat produced a markedly stronger arousal in female than in male detectors. Our statistical tests pinpointed this gender-specificity to the right amygdala (strongest in the superficial nuclei). When comparing the olfactory bulb responses to the corresponding stimuli, we found no significant differences between male and female detectors. These imaging results complement existing behavioral evidence, by identifying whether gender differences in response to alarm chemosignals are initiated at the perceptual versus emotional level. Since we found no significant differences in the olfactory bulb (primary processing site for chemosensory signals in mammals), we infer that the specificity in responding to female fear is likely based on processing meaning, rather than strength, of chemosensory cues from each gender.     

Individual Odour Similarity and Discrimination in the Coruro (Spalacopus cyanus, Octodontidae)

Previous studies of subterranean, fossorial and above‐ground rodents have demonstrated that similarities in individual odours covary with genetic similarities thus supporting the theory of odour‐genes covariance (i.e. the closer the individuals are genetically, the greater the similarities between their odours). We used the habituation‐generalization paradigm, where the subject is exposed to the same odour stimulus in three consecutive habituation trials followed by two test trials in which the odour from two other individuals are presented successively. Using this test design, we showed that the socially living coruros (Spalacopus cyanus) discriminate individuals on the basis of their ano‐genital odours and also respond to odour similarities between individuals. Male and female subjects treated ano‐genital odours of two same‐sex family members and also the odours of two sibling strangers as different to each other. At the same time, they treated the odours of siblings as similar compared with the odour of an unrelated individual. No gender differences were detected. Our results contrast with those from other rodent species that did not spontaneously discriminate between individual odours of siblings from a different family than their own. The polygyneous lifestyle may provide the selective background for that difference. Additional research will be necessary to explore this hypothesis and to rule out differences due to dietary preferences and due to the type of paradigm chosen for the tests.     

Calcium responses to pheromones and plant odours in the antennal lobe of the male and female moth Heliothis virescens

In male moths, the primary olfactory integration centre, the antennal lobe, consists of two systems. The macroglomerular complex processes pheromone information, while the ordinary glomeruli process plant odour information. Females lack a macroglomerular complex. We measured the spatial representation of odours using in-vivo optical recording. We found that: (1) pheromone substances elicited activity exclusively in the MGC. No response was found in female antennal lobes. (2) Plant odours elicited combinatorial activity patterns in the ordinary glomeruli in both males and females. No response was found in the MGC of male moths. (3) A clean air puff often led to activity, in both males and females, suggesting that mechano-sensory information is also processed in the antennal lobe. (4) With an interstimulus interval of 5 or 10 s, strongly activated glomeruli were able to follow the temporal structure of the stimulus, while others lost their phase-locking. Some glomeruli showed "off" responses. These properties were odour dependent. This confirms and extends previous studies, showing the functional significance of the two subsystems for processing olfactory information. Pheromones are coded in a combinatorial manner within the macroglomerular complex, with each glomerulus corresponding to one information channel. Plant odours are coded in an across-glomeruli code in the ordinary glomeruli.     

雌性根田鼠断奶后对亲本尿气味的记忆

为研究亲子分开后雌性根田鼠对亲本气味的记忆持续时间,分别在未分开(20日龄)、分开10d(30日龄)、20d(40日龄)、30d(50日龄)、40d(60日龄)时,以新鲜尿作气味源,在行为观察箱中记录雌性根田鼠对不同气味源的行为响应模式,结果表明(1)未分开时,雌鼠遭遇父本气味时自我修饰的频次极显著高于陌生雄鼠气味,在分开10d时,雌鼠接近父本气味的频次显著多于接近陌生雄鼠气味的频次,其对前者反标记显著少于后者;(2)分开20d后,雌鼠对父本和陌生雄鼠气味的行为响应无明显差异;(3)未分窝时,雌性根田鼠幼仔对母本和陌生雌鼠气味的行为响应无差异;(4)分开10—40d时,雌性根田鼠对母本和陌生雌鼠气味表现出不同的行为响应模式。以上结果表明,在亲子分开10d时,雌鼠仍能识别父本和陌生雄鼠的气味;分开20d后,雌鼠不再能够识别父本和陌生雄鼠的气味;在亲子分开40d时,雌鼠仍能识别母本和陌生雌鼠的气味。因此,雌鼠对父本气味的嗅觉记忆时间可以持续到亲子分开10—20d之间;而对母本气味的嗅觉记忆时间则可以持续到亲子分开40d以上。     

Scent-marking behaviour in response to conspecific odours by the rat, Rattus norvegicus

The scent-marking behaviour of male and female rats in response to conspecific odours was investigated in two experiments. The results of the first experiment indicated that exposure to conspecific odours generally led to an increase in marking rates. However, no sex differences were found, and large differences in marking responses according to the sex of the odour donor were only found for dioestrous females. These results do not suggest that the primary function of scent-marking in this species is sexual. In the second experiment, odour sources differed not only in the sex of the donor, but also in their relative familiarity to the animal being tested. This experiment showed that males marked more in response to odours from familiar (non-related) females. Females did not differ significantly on measures of marking but did display greater interest in odours from unfamiliar males. The results are discussed in relation to possible functions of marking in this species.