Investigations on the Olfactory Discrimination Exhibited by the Females in the Male-induced Implantation Failure (the Bruce Effect) in Laboratory Mice

Direct contact with the alien male pheromone for 7 days before mating significantly decreased the rate of male-induced implantation failure (the Bruce effect) in newly inseminated female mice. By contrast, females housed with alien males for 7 days before mating so that physical contact with the latter was prevented exhibited a high rate of implantation failure following exposure to alien males after mating. Exposure to an air-borne pheromone produced by alien males induced oestrus (the Whitten effect) in a significant number of grouped females. The results do not support the suggestion that the inability of the stud male to block implantation is due to his original induction of oestrus. The results also do not support the view that the key factor in the induction of the Bruce effect is the ability of the female to identify the stud as an individual which prevents her from responding to him but allows her to react to a new male with hormonal changes leading to implantation failure and return to oestrus. It is suggested that the olfactory discrimination exhibited by the female in the Bruce effect is influenced by her overall olfactory experience before and after mating. The results are consistent with the view that the male-originating pheromone involved in the Bruce effect is distinct from the one involved in the Whitten effect.     

Bromocriptine-induced implantation failure in mice: failure of the stud male to protect pregnancy.

The presence of the stud male failed to prevent implantation failure in newly inseminated females induced by administration of bromocriptine. This is in contrast with the ability of the stud male to prevent implantation failure in females induced by alien male exposure, and nutritional stress. Since bromocriptine is a potent inhibitor of hypophysial prolactin release by virtue of its stimulatory effect on hypothalamic dopaminergic activity, the results suggest that the stud male-originating luteotrophic stimulus is incapable of overriding the dopaminergic activity in bromocriptine-treated females.     

Stud male-induced protection of implantation in food-deprived mice: masking effect of an artificial scent on pheromonal odour

In contrast to unscented stud males, stud males anointed with a commercial perfume failed to protect implantation in food-deprived females. It is suggested that the failure of perfumed stud males to protect pregnancy in their coital partners is due to the masking effect of the perfume on the stud male-originating olfactory cue which stimulates luteotrophic activity in females. The results are also consistent with the view that the newly inseminated female mouse identifies the stud male as an individual through a pheromonal cue and this is involved in the protective effect on implantation in the food-deprived female.     

Involvement of contact stimuli in the male-induced implantation block (the Bruce effect) in mice

Confinement of newly inseminated female mice exposed to confined alien males significantly decreased the male-induced implantation failure (the Bruce effect). By contrast, free (unconfined) females exposed to confined alien males showed a high rate of implantation failure. The results suggest that the pheromone of male origin involved in the Bruce effect is non-volatile and acts on the female through contact. The vomeronasal organ appears to be involved in the perception of this pheromone.     

Effect of cyproterone acetate on the pregnancy-blocking ability of male mice and the possible chemical nature of the pheromone

Even though castration abolished the ability of alien males to induce implantation failure (the Bruce effect) in newly inseminated females, treatment of intact alien males with the steroidal antiandrogen, cyproterone acetate, for 14 days (short term) did not significantly depress their ability to induce the Bruce effect. However, prolonged treatment (42 days) with cyproterone acetate suppressed the pregnancy-blocking ability of alien males to some extent, possibly due to the antigonadotrophic properties of the drug. Ovariectomized alien females treated with implants of testosterone (androgenized females) exhibited the ability to block implantation in newly inseminated females, but concurrent treatment of androgenized females with cyproterone acetate did not depress this ability. The results strongly suggest that the pheromone involved in the male-induced implantation failure is not the product of an androgen-dependent tissue, but is likely to be a product of androgen metabolism.     

The Bruce effect in Norway rats

Intrauterine implantation of fertilized ova can be blocked by exposing recently inseminated females with an unfamiliar male. This selective pregnancy failure, designated as the Bruce effect (Bruce, Nature 1959; 184:105), is well studied in laboratory mice and has been confirmed in several other rodent species. However, no clear information exists concerning this phenomenon in the laboratory rat. The present study was conducted to investigate whether or not the Bruce effect exists in the rat. Females of two F1 hybrid strains (n(total) = 354) with different MHC genotypes (F344BNF1, RT1(lv1/n), and LEWPVGF1, RT1(l/c)) were mated with males of their own strain and subsequently exposed during the first 4 days postcoitus either to a male of the other hybrid strain or to an unfamiliar male of the same strain as the stud. The litter rate of each treatment group was determined. As a control, mated females of both strains were reexposed to the stud male to determine baseline litter rates. Female rats of both F1 hybrid strains showed a significantly lower litter rate when exposed to males of a different strain than their stud male, compared to the expected values of birth rates observed in control females (F344BNF1: P = 0.017; LEWPVGF1: P = 0.019). In contrast, there was no difference between expected and observed litter rates in females of both F1 hybrid strains after exposure to an unfamiliar male of the same strain as their stud. Our results demonstrate for the first time that the Bruce effect, well documented in mice, occurs in the Norway rat.     

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.     

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      

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。     

Novel male mice show gradual decline in the capacity to disrupt early pregnancy and in urinary excretion of testosterone and 17 beta-estradiol during the weeks immediately following castration.

Novel male mice can disrupt intrauterine implantation of fertilized ova in inseminated females. Evidence indicates mediation by androgen-dependent excretions. This study was designed to examine the time course of males' ability to disrupt pregnancy following castration and relate this to their urinary excretion of testosterone and 17 beta-estradiol. During days 1-5 of pregnancy, previously inseminated females were housed underneath castrated novel males at various intervals after the surgery. Castrated males generally continued to disrupt pregnancy during the initial weeks after surgery. Progressively, the probability of retention of pregnancy increased as a linear function of time since castration. There was an apparent asymptote, where the majority of females remained pregnant, beginning at about 6 weeks following surgery. Males' excretion of testosterone and 17 beta-estradiol in urine, measured via ELISA procedures, diminished gradually during the weeks after castration.     

Testosterone suppresses circadian responsiveness to social cues in the diurnal rodent Octodon degus

The diurnal, social rodent Octodon degus displays a robust sex difference in the ability to use social cues to facilitate reentrainment following a phase advance of the light cycle. Adult females housed with a female social cue donor reentrained 25% to 40% faster than did females reentraining alone. However, reentrainment rates of males were unaffected by exposure to female social cues during reentrainment. The authors hypothesized that males were less sensitive to the reentrainment-enhancing effects of social cues and that their higher threshold to the stimuli could be overcome if the social cues were either increased in strength or salience. Housing a male with two females significantly shortened the time to reentrain following a 9-h phase advance (p = 0.002). Housing with a sister had no effect on reentrainment. Therefore, male degus are able to respond to social cues but require the stimulus to be stronger than that for females. The effect of testosterone was tested by comparing reentrainment rates of castrated males before and after testosterone replacement both with and without a female social cue donor. Castrated males responded to a single female social cue donor, reentraining 35% faster than when housed alone (p = 0.006), whereas the time to reentrainment of intact males and males with testosterone capsule implants did not differ. Intact females were also implanted with testosterone and phase shifted with and without donors. Testosterone treatment eliminated the increase in reentrainment rates in the presence of social cues. The authors conclude that the rate of recovery from odor-enhanced phase shifts is modulated by activational effects of testosterone in male degus. Testosterone is also effective in suppressing social cue responsiveness in females, suggesting that testosterone's effects on responsiveness are not sexually dimorphic. This hormonal effect likely occurs by altering sensory system functions or CNS response to sensory information.     

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.     

Female Cowbird Song Perception: Evidence for Plasticity of Preference

The goal of the research reported here was to look for evidence of modifiability of preference for male song in female cowbirds, Molothrus ater. To this end, we investigated whether social experience affected the breadth and consistency of females’ playback preferences for geographic variants of male song. In three experiments, we varied female cowbirds’ exposure to males. Wild‐caught juvenile females showed a preference for local song in their first year when housed without males in sound‐attenuating chambers, as we had found previously with adult females. But we found that neither adult nor juvenile females showed a preference for local over distant song after they had been housed in large, outdoor aviaries with other females but without male residents. Aviary housing with local males did lead to preferences for local songs. These data represent the first unqualified evidence that adult and juvenile female cowbird preferences for song are modifiable. These data add to the growing body of literature suggesting that receivers, as well as signalers, rely on learning during development of their communication system.     

Genetic benefits of mate choice separated from differential maternal investment in red junglefowl (Gallus gallus)

Abstract Females may choose more attractive mates to obtain better viability or attractiveness genes for their offspring. A number of studies have demonstrated a positive relationship between paternal attractiveness and offspring quality. However, this pattern could be due to inheritance of paternal genes and/or it could be due to increased maternal investment in the offspring of more attractive males. To isolate female responses to male appearance from paternal genetic effects, I housed female red junglefowl ( Gallus gallus ) with vasectomized (sterile) males and artificially inseminated them. Male junglefowl with larger combs are more attractive to females. Females laid more eggs when housed with a large-combed, as opposed to a small-combed, vasectomized mate. Neither egg volume nor offspring body condition was associated with comb size of the mother's vasectomized mate. Paternal genetics appeared important. Body condition and comb size were greater for the sons of large-combed sperm donor males. This is consistent with the hypothesis that genetic benefits to offspring maintain female preference for the most ornate males. It is possible that greater body condition and comb size in sons of large-combed sires was not caused by genetic differences, but instead was due to compounds in the ejaculate of large-combed sperm donors inducing greater reproductive investment from females. However, females artificially inseminated by large-combed males did not produce more or larger eggs than females artificially inseminated by small-combed males, and thus there is no other evidence consistent with ejaculate-induced differential investment. Furthermore, only in older chicks was body condition significantly related to sire comb size, suggesting genetic rather than differential investment mechanisms.     

Pregnancy blockage and the memory of the stud male in the vole (Microtus agrestis).

When female voles were allowed contact with the stud male for only 1 h at the time of mating, 55% exhibited pregnancy failure when exposed to a strange male 48 h later. When females were made psuedopregnant by hormone treatment and vaginal stimulation (i.e. no stud male involved), 87% exhibited luteal failure when exposed to a strange male. It is suggested that the characteristics of the stud male are rapidly imprinted upon the female at the time of mating and that this imprinting is important in preventing the female showing a blocking response to this male upon any subsequent exposure.     

Is egg carrying attractive? Mate choice in the golden egg bug (Coreidae,Heteroptera)

In several species of fish, females select males that are already guarding eggs in their nests. It is a matter of debate as to whether a female selects a good nest site for her offspring (natural selection) or a male for his attractiveness (sexual selection). The golden egg bug, Phyllomorpha laciniata Vill, resembles fish in the sense that mating males carry more eggs than single males, but in the bugs, female mate choice is decoupled from egg site choice. The sexual selection hypothesis predicts that if females select males using male egg load as a cue for male quality, they should not mate with a male when eggs are removed, regardless of his mating attempts. When individual females were enclosed with an egg-loaded male and an unloaded male, they mated equally often with both males, although the loaded males courted more. In addition, when only successful males were used, females mated equally often with the loaded male and the unloaded male irrespective of sex ratio. Male choice rather than female choice affected mating frequency when sex ratio was equal. Therefore, females do not select the male by the eggs he carries, but successful males may receive many eggs due to egg dumping by alien females while they mate or as a consequence of mate guarding.     

Influence of male gonadal hormones and familiarity on pregnancy interruption in prairie voles

Pregnancy interruption (PI) was examined in female prairie voles, Microtus ochrogaster, exposed to stimuli from males 7 to 12 days after pairing. Urine from unfamiliar males interrupted pregnancy when placed directly on the external nares of newly mated females, but urine from familiar stud males was without effect. Castration of males did not reduce the efficacy of unfamiliar male urine in interrupting pregnancy. The neuroendocrine system of female prairie voles responded selectively to male urine as a function of its familiarity; the efficacy of male stimuli leading to PI was not dependent on gonadal hormones.     

Induction of dominant lethals in progeny of male CBA mice after pheromonal action

The inhibiting effect of pheromone 2,5-dimethylpyrazine of house mouse females on the reproductive function of the CBA male mice was studied. The mutagenic effect of six-day pheromonal effect was assessed by dominant lethal test. Analysis for the frequency of dominant lethals showed that the pheromonal effect results in an increased death rate of the progeny of the treated males. This is probably explained by implantation failure and is expressed in a reduced average number of the implantation sites and low live embryos per female. The proportion of females with live embryos decreased significantly. The implication of the effect of female mouse pheromone 2,5-dimethylpyrazine on the genetic processes in germ cells of male mice is discussed.     

Sperm influences female hibernation success, survival and fitness in the bumble-bee Bombus terrestris

We present evidence that in the absence of the transfer of male gland compounds in the ejaculate as well as of behavioural male traits, such as mate guarding or harming of females, sperm itself affects female life-history traits such as hibernation success, female longevity and female fitness. Using the bumble-bee Bombus terrestris, we artificially inseminated queens (females) with sperm from one or several males and show that sire groups (groups of brother males) vary in their effects on queen hibernation survival, longevity and fitness. In addition, multiply inseminated queens always had a lower performance as compared to singly inseminated queens. Apart from these main effects, sire groups (in situations of multiple insemination) affected queen longevity and fitness not independently of each other, i.e. certain sire group combinations were more harmful to queens than others. So far, the cause(s) of these effects remain(s) elusive. Harmful male traits as detected here are not necessarily expected to evolve in social insects because males depend on females for a successful completion of a colony cycle and thus have strong convergent interests with their mates.     

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.