Analysis of a genetic recognition system in wild house mice

Wild female house mice have strong preferences for odors of male mice whose t-complex genotype is +/+ rather than for males carrying deleterious mutations (+/t) at the t complex. In this review of a large number of studies examining the basis for this preference, we suggest the following: first, preferences of +/+ females are greatly influenced by environmental factors and probably do not have a large genetic component: second, preferences of +/t females are less dependent upon environmental factors and hence may have a strong genetic component: third, the lethal factors within the t complex are involved in both the production of the cue by males and the expression of the preference in females: and fourth, there may be a second gene or genes within the t complex involved in the expression of female preference.     

Responses of male mice to odors of females: Effects of T- and H-2-locus genotype

Male wild house mice (Mus musculus) were given a choice of odors of females whose T-locus genotype was +/ + or +/t. Males showed strong preferences for the odors of +/ + females. However, when males were tested with odors of recombinant females whose genotype differed at the T locus but which carried similar haplotypes at the H-2 locus, the preference for odors of +/+ females was not manifested. Consequently, differences in female odor production that are responsible for male odor preference are not due specifically to the female genotype at the T locus.This work was partially supported by NIH Grant HD R01 1997 and a BRSG Grant from Rutgers University.     

Factors modulating preferences of female house mice for males differing in t-complex genotype: Role of t-complex genotype,genetic background,and estrous condition of females

The present study investigates factors mediating odor and social preferences in female house mice (Muc domesticus) based on the t-complex geontype of males. Previous studies in this laboratory showed that females prefer the odors of wild-type (+/+) males over those that carry lethal genes (+/t). The purpose of this study was to determine the genetic, hormonal, and environmental factors that regulate these preferences. The variables examined include t-complex genotype, genetic background, estrous condition of test females (+/+ or +/t), and genotype of the test female's parents. Results indicate that female preferences for +/+ males are dependent upon the t-complex genotype and estrous condition of test females. Only +/t females in estrus showed preferences for +/+ males. Estrous cycle condition effects were seen in both wild (+/+w ⁵) and inbred (129 +/tw ⁵)females. Homozygous females (+/+) and diestrous females of both geno-types did not demonstrate preferences for either +/+ or +/t males.     

Female discrimination of male odors correlated with male genotype at the T locus: A response to T-locus or H-2-locus variability?

Female house mice (Mus musculus), derived from several populations of wild-caught mice, were tested for their ability to discriminate between males whose genotype at the T locus was +/+ and those whose genotype was +/t, using odor cues alone. Females spent more time near the odors or +/+ males than near the odors of +/t males. This preference was independent of the T-locus genotype of the female and the particular type of t allele carried by either the male or the female. A female's preference, however, did appear to be related to the genotype of her parents. Females with one +/t parent were more likely to prefer +/t males than were females whose parents were both +/+. In a second experiment 18 females were tested with odors from soiled bedding of recombinant males whose genotype varied at the T locus but who were similar at the H-2 locus. As a control, these 18 females were also tested with bedding of wild-derived +/+ and +/t^{w semilethal} males. Females tested with recombinant males preferred odors of males not carrying lethal t alleles over those of males carrying two lethal t alleles, indicating that T-locus variability, not H-2-locus variability, is responsible for odor differences between +/+ and +/t males. Female responses to odors of recombinanat males did not differ from those to odors of +/+ and +/t^{w semilethal} males. Responses of mice to odor differences associated with T-locus variability may have evolved independently of responses to odor variability associated with the H-2 locus.This work was supported by NIH Grant HD 15997-01.     

Preferences of pre- and post-weanling long-evans rats for nest odors

Three experiments were conducted on the preferences of infant rats for nest odors. Pre-weanling rats preferred their own nest odor to nests of strange litters and showed low preferences for the nest odors of virgin females. Nest odors of unmated males were investigated less than the pup's own nest odor but more than the odors of virgin females. Male and female rats did not differ in odor preferences. Rats reared with both their dam and sire did not differ in their odor preferences from rats reared with their dam alone when tested at 16–20 days of age, but when tested at 33–38 days of age they showed a greater preference for male odors. Post-weanling rats did not show a preference for the nest odors of lactating females and began to show sex differences in their preferences.     

Cross-species rearing influences urine preferences in wild guinea pigs

Urine preferences of adult wild male guinea pigs reared with domestic female guinea pigs were studied. Subjects were removed from the mothers at birth and each was reared with a domestic female for either the first 3 or the first 16 weeks of life; each control group male was reared with a wild female for the first 3 weeks of life. Following rearing experience, males were reared in social isolation. A series of urine preference tests was conducted beginning when the subjects were 17 weeks of age. Whereas males in the control group preferred urine of wild animals to urine of domestic animals, individuals reared with a domestic female generally preferred domestic female urine to wild female urine and were equally attracted to male urine of the two species. It is concluded that postnatal prepubertal experience influences urine odor preferences in wild male guinea pigs.     

A role of female preputial glands in social behavior of mice

Female mice reared by mothers with preputial glands preferred females with preputial glands over females deprived of preputial glands (p<0.02). Furthermore, such females preferred odors from males with preputial glands to odors from males without such glands (p<0.01). Females reared by mothers without preputial glands showed greater preferences for the odor of preputialectomized males (p<0.02) and females (p<0.01) than nonpreputialectomized animals. Odors common to males and females, emanating from preputial glands of the mother apparently influence early postnatal mice and determine their preferences in later life.     

Photoperiod and gonadal hormones influence odor preferences of the male meadow vole, Microtus pennsylvanicus.

Male meadow voles housed in a long photoperiod (14 h light/day, LP) preferred female to male odors, whereas males maintained in a short photoperiod (10 h light/day, SP) did not display preferences for odors of either sex. These odor-preference patterns matched those of free-living males during spring and autumn, respectively. The preference of LP male voles for female over male odors was eliminated by gonadectomy and reinstated by treatment with testosterone. In SP males, although gonadectomy did not affect odor choices, a preference for female odors was induced by testosterone treatment. Treatment with estradiol did not alter odor preferences of LP or SP males. In conjunction with previous result, the present findings suggest that hormonal responsiveness of neural substrates that control odor preferences are sexually dimorphic and may reflect sex differences in reproductive strategies.     

Effect of vomeronasal organ removal from male mice on their preference for and neural Fos responses to female urinary odors

Four experiments were conducted to determine whether vomeronasal organ (VNO) inputs in male mice mediate the rewarding properties of estrous female urinary odors. Sexually naive male mice with either an intact (VNOi) or lesioned (VNOx) VNO preferred to investigate female urine over water in Y-maze tests. Subsequently, VNOi males ran significantly more quickly and remained in nasal contact longer with estrous female urine than with male urine, whereas VNOx males investigated these odors equally. In home-cage habituation-dishabituation tests, VNOi males also investigated female urine significantly longer than did VNOx males, although both groups investigated female urine longer than other non-body odors. Finally, female urinary odors induced Fos in the nucleus accumbens core of VNOi males but not of VNOx males. Our results suggest that female urinary odors retain some incentive value in VNOx males. However, once direct nasal contact is made with female urine, VNO inputs further activate forebrain mechanisms that amplify the reward salience of this stimulus for the male mouse.     

Parental environment: effects on survival, growth and aggressive behaviors of 2 rodent species

The influence of the parental environment on the development of aggressive behaviors was studied in 2 muroid rodent species. Litters of southern grasshopper mice and northern white-footed mice were reared by the natural parents or were reciprocally cross-fostered soon after birth to parents of the opposite species. After weaning at 24–26 days, mice of both species were isolated and observed at 10-day intervals from 30 to 100 days of age in one of the following tests: (1) predation on house crickets; (2) interspecific aggression toward Swiss-Webster laboratory mice; and (3) intraspecific aggression toward opponents of the same gender and approximate age. Naturally reared grasshopper mice males and females displayed extremely high levels of aggressive and predatory behaviors whereas white-footed mice controls were passive and defensive in all tests. Rearing by white-footed mice foster parents resulted in a significant decrease in the aggression of grasshopper mice males and females toward laboratory mice. During intraspecific encounters, fostered grasshopper mice initiated fewer social interactions than naturally reared controls. The predatory behavior of grasshopper mice was not altered by the fostering procedure. The behavioral measures of fostered white-footed mice showed no systematic changes when compared to controls. These results indicate that the postnatal parental environment contributes to the naturally high levels of aggressive behaviors of grasshopper mice. In contrast, the limited aggressive behaviors of a naturally passive species, white-footed mice, were not increased by fostering at birth to parents of a highly aggressive species, grasshopper mice.     

Effect of bilateral accessory olfactory bulb lesions on volatile urinary odor discrimination and investigation as well as mating behavior in male mice

Previous research raises the possibility that urinary volatiles from estrous female mice activate mitral cells in the accessory olfactory bulb (AOB) of male mice following detection via the main olfactory epithelium as opposed to the vomeronasal organ. We asked whether bilateral lesions of the AOB would disrupt the ability of male mice to discriminate between urinary volatiles from mice of different sexes or endocrine states, or affect their interest in investigating these odors when they were presented sequentially in home-cage habituation/dishabituation tests. Males with either partial or complete bilateral lesions of the AOB resembled sham-operated control males in their ability to discriminate between ovariectomized and estrous female urinary volatiles as well as between male and estrous female urinary volatiles. However, males with either complete or partial AOB lesions spent significantly less time than sham-operated control males investigating urinary volatiles from estrous females, especially during tests when the alternative stimulus presented was male urine. Placement of AOB lesions failed to disrupt males' mating performance. Our results suggest that the incentive value of opposite-sex (female) volatile urinary odors which are initially detected by the main olfactory system is enhanced when they are further processed by the male's AOB.     

Inhibition of infanticide after mating by wild male house mice

The effect of mating on the behavior of male house mice (Mus musculus) toward young has been examined in numerous domestic stocks of mice, and the somewhat contradictory results led us to examine the effects of mating on the behavior of wild male mice toward young. The wild mice were the F1-F4 offspring of mice trapped in Missouri. Virtually all wild males exhibit infanticide prior to mating, but virrually all wild males were inhibited from exhibiting infanticide 3 weeks after mating whether they were placed into the cage of their former mate and her litter or into the cage of an unfamiliar female and her litter, similar to the effect of mating on the behavior of CF-1 male mice toward young. In contrast, wild males that had exhibited infanticide prior to mating were inhibited from exhibiting infanticide 3 weeks after mating when placed with their former mates and their 2-day-old young but not when placed with unfamiliar females and their 2-day-old young. When wild males were tested for their behavior toward young using the procedure of placing a single pup into each male's home cage, mating did not result in an inhibition of infanticide (about 90% of the males exhibited infanticide). Cohabitation with a female without mating also did not influence the behavior of wild males toward young. Wild males that exhibited infanticide when placed with a lactating female produced their own young more rapidly than did noninfanticidal males, thus providing further support for the hypothesis that under some conditions, infanticide can be an adaptive trait.(ABSTRACT TRUNCATED AT 250 WORDS)     

Lesions centered on the medial amygdala impair scent-marking and sex-odor recognition but spare discrimination of individual odors in female golden hamsters.

The medial amygdala (Me) has been implicated in various social behaviors that depend on chemosensory cues, but its precise role in discriminating and learning social odors is not known. Female golden hamsters (Mesocricetus auratus) received electrolytic lesions of the Me or sham surgery and were tested for their ability to (a) discriminate between odors of individual males in a habituation-discrimination task, (b) show preferences for male over female odors in a Y maze, and (c) scent-mark in response to male and female odors. All females discriminated between scents of individual males. In contrast, Me lesions eliminated female preferences for male odors in a Y maze. Females with Me lesions also showed a substantial reduction in vaginal marking and virtually no flank marking in response to odors. Thus, the Me in female hamsters is critical for differential investigation of opposite-sex odors and for scent-marking behavior but is not involved in discrimination between odors of individuals.     

Hormonal control of odor preferences and urine-marking in male and female rats

Gonadectomized male and female rats show no preferences for the odors of conspecifics of the opposite sex and no urine-marking. Castrated males given testosterone propionate (TP) injections showed preferences for female odors over no odor as did males given estradiol benzoate (EB). Males given EB plus progesterone (P), P only, or oil (controls) showed no preferences for female odors. No group of ovariectomized females (TP, EB, EB+P, or oil injected) showed a preference for male odors over no odor. Males given TP, EB, or EB+P injections showed an increase in urine-marking while males given P or oil showed no marking. Females given TP injections showed an increase in marking but those given EB, EB+P or oil showed no marking. These results are discussed in relation to studies on the hormonal control of scent-marking in gerbils and sexual behaviour in rats.     

A competitive effect of androgen signaling on male mouse attraction to volatile female mouse odors

Olfaction plays an important role in animal communication. We hypothesized that males recognize the attractive volatile odors attributed to female reproductive ability. We measured the period during which a male mouse spent sniffing volatile odors from a sham-operated female mouse or an ovariectomized mouse without visual or tactile contact. Intact male mice spent more time sniffing volatile odors from proestrous, estrous or metestrous females than from ovariectomized females. There was no difference in castrated male mice. To investigate the involvement of sexual hormone in this behavior, castrated male mice were treated with 17 alpha-estradiol (E), dihydrotestosterone (DHT), or both. E-treatment did not affect sniffing behavior. Regardless of the estrous stages, DHT-treated castrated males spent less time sniffing the volatile odors from sham-operated than from ovariectomized female mice. Both E- and DHT-treated castrated males spent less time sniffing the volatile odors from proestrous or estrous females than from ovariectomized females. These results suggest that neither androgen nor estrogen is sufficient for reproducing male attraction to volatile female mouse odors, and that androgen signaling has a competitive effect against the attraction.     

Preferences of pre-weanling Long-Evans rats for anal excreta of adult males and females

Long-Evans hooded rat pups were reared with their dam alone, their dam and sire or their dam 12 hrs per day and their sire 12 hrs per day and tested for preferences for anal excreta from adult male and female rats when they were 18 to 20 days of age. In all rearing conditions the anal excreta of the rat's own dam was preferred to that of strange dams and the excreta of both own and strange dams was preferred to that of virgin females. Anal excreta from virgin females was preferred to no odor as was anal excreta of unmated males, strange sires and the rat's own sire. Only rats reared with their dam and sire preferred the odor of their own sire to that of other males. The results suggest that pre-weanling rats may attend to different dimensions of the odors of conspecifics, such as the species odor, maternal odor, and individual odor and that different rearing conditions may influence the odor dimension to which the rat attends.     

Effects of the sex-linked prenatal lethal gene tortoise (Moto) on reproduction and growth in the mouse

The sex-linked prenatally lethal gene tortoise (Moto), an animal model for the human disorder known as Menkes' Kinky Hair Syndrome (MKHS), was studied in the mouse (Mus musculus). The genetic effects upon reproductive performance, birth weight, preweaning growth, and mortality were evaluated to characterize the debilitating effects of the disorder. Reproductive performance of mice were evaluated in two mating types (dam X sire), mutant female (To/+) X normal male (+/Y) and normal female (+/+) X normal male (+/Y). Litter size was reduced in the To/+ X +/Y mating type as expected due to the death of To/Y offspring in utero. Adjusted birth weight of To/+ and +/Y offspring were identical, and both were greater (P less than 0.05) than +/+ offspring. Within one day, however, the To/+ littermates were smaller (P less than 0.05) than +/+ and +/Y and remained consistently inferior in growth through day 30. Normal females and normal males were similar (P greater than 0.05) in growth from day 1 through day 21. Thereafter, +/Y mice were consistently heavier (P less than 0.05) than +/+ mice through day 30. The To/+ genotype had the greatest (13.8%) preweaning mortality rate; +/+ and +/Y genotypes were comparable as were overall comparisons between parity 1 and 2. It is apparent from this study that the copper deficiency and lethality occurring in the progeny of mottled mice were primarily the result of the gene actions in the heterozygote animals. Progression of the disorder may be prevented by experimental determination of both the timing and targeting of in utero therapy in mottled mice and MKHS fetuses.     

Infanticide by virgin CF-1 and wild male house mice (Mus musculus): effects of age, prolonged isolation, and testing procedure

The frequency of infanticide by juvenile, young-adult, and adult male house mice (Mus musculus) was compared in CF-1 albino mice and the F1-F4 male offspring of wild mice trapped in Missouri. When tested in their home cages for their behavior toward a single 2-day-old pup after being individually housed for 5 days, juvenile CF-1 and wild males were equally likely to exhibit infanticide (about 35%). But, adult wild males were significantly more likely to exhibit infanticide (about 90%) than were adult CF-1 males (about 45%). We propose that differences in exposure to testosterone during fetal life may contribute to the difference in the incidence of infanticide between CF-1 and wild males. Prolonged isolation (45 days) significantly reduced the proportion of wild male mice that exhibited infanticide when the males were tested in their home cages, but not when the males were tested by being placed into the cage of lactating females and their 2-day-old young. Virtually all adult wild males exhibited infanticide when they were tested in their home cages (with either a 2-day-old or 7-day-old pup) or when they were placed into the cages of lactating wild female mice and their 2-day-old young. But, when adult wild males were placed with lactating wild females on Day 7 postpartum, the females attacked the males and most males were prevented from exhibiting infanticide.     

Assortative mating in mice. III. Genetic determination of female mating preference

Females from the inbred strains BALB/Ibg and DBA/Ibg and females from the reciprocal crosses between these strains, which were fostered by BALB/Ibg and DBA/Ibg males, were tested for mating preference between BALB/Ibg and DBA/Ibg males. The tests included the use of both the standard and the tubetechnique methods. In these strains, it was found that the main determinant of female mating preference was the genotype of the foster father. Females reared by DBA/Ibg males had a tendency for negative mating preference, whereas females reared by BALB/Ibg did not. The genotype of the mothers had some effect on the degree of the preference. Females reared by BALB/Ibg mothers had somewhat lower preference for BDA/Ibg males than did daughters' of BDA/Ibg females. The effect of the female's own genotype on mating preference was found to be only minor in a comparison done between these strains and their F ₁ crosses which had been raised by foster parents of the same genotype.This work was supported by NIGMS grant GM- 14547.     

Attraction of beagles to conspecific urine, vaginal and anal sac secretion odors

Attraction of male and female Beagles to conspecific urine, vaginal and anal sac secretion odors was examined in four experiments. Males spent more relative time investigating female urine odors than odors of vaginal or anal sac secretions. Sexually experienced males, but not sexually inexperienced ones, spent more time investigating estrous than diestrous female urine and vaginal odors. Anal sac secretions from estrous bitches were not more attractive to males than those from diestrous bitches. Estrous females spent no more time than diestrous ones in the investigation of male anal sac secretion and urine odors. Male urine and anal sac secretions elicited little investigation from male conspecifics. Females spent more time investigating female urine odors than female anal sac or vaginal secretion odors, and exhibited a slight general preference for diestrous over estrous stimuli. A positive correlation between the odor investigation times of this study and investigation times of comparable animals to conspecifics in a social situation suggests odor preferences are relatively good indicators of social preferences, and vice versa, in this breed.