Behavioral Selection of Odor Cues by Young Female Mice Affects Age of Puberty LEE C. DRICKAMER Department of Zoology Southern Illinois University Carbondale, Illinois
Female house mice were reared from weaning at 21 days of age until first vaginal estrus in 40 1 aquaria in which they were given a choice of exposing themselves to bedding placed on opposite halves of the aquarium floor and sprayed with water or urine containing puberty-influencing chemosignals. In Experimental I , mice housed with only male urine cues sprayed on the bedding matured significantly earlier and mice housed with only grouped female urine sprayed on the bedding matured significantly later than control mice where water was sprayed on the bedding for both halves of the aquarium. In Experiment 2, there were no significant differences in mean ages at vaginal introitus or first estrus for females reared with choices between (a) bedding sprayed with male urine versus bedding sprayed with water, (b) bedding sprayed with urine from grouped females versus bedding sprayed with water, (c) bedding sprayed with male urine versus bedding sprayed with urine from grouped females, or (d) the control condition where both sides of the aquarium contained bedding sprayed with water. Analysis of continuous video tapes of the locations of the females for Experiment 2 revealed that females chose initially to spend more time on the half of the floor with bedding that delayed puberty relative to the other side, but shifted their preference toward a more puberty-enhancing signal at about the time of first estrus. Female house mice appear to be able to exert some behavioral control over their own sexual maturation. 0 1992 John Wiley & Sons, Inc.
Sexual development and the onset of puberty are important both as key transition periods in the course of development and, in many species of rodents, as an indicator of the onset of reproduction. In many rodent species, puberty can be equated with generation time, certainly during that portion of the year when animals are sexually active. A variety of factors can influence the timing of puberty in mammals, particularly rodents (Bronson, 1979; Drickamer, 1986; Vandenbergh & Copola, 1987). These factors include genetics, ambient conditions, health and nutrition, and social influences such as urinary chemosignals (Drickamer, 1981; Laurie, 1946; Vandenbergh, 1983). For rodents, and house mice in particular, Reprint requests should be sent to Dr. Lee C. Drickamer, Department of Zoology, Southern Illinois University, Carbondale, I L 62901-6501 Received for publication 14 February 1992 Revised for publication 13 May 1992 Accepted at Wiley 18 May 1992
Developmental Psychobiology 25(6):461-470 (1992) 0 1992 by John Wiley & Sons, Inc.
CCC 0012-1630/92/060461-10
462
DRICKAMER
many aspects of the urinary chemosignal system influencing sexual development have been examined with respect to both the donors of puberty-influencing urinary signals and the young female recipients (Drickamer, 1986; Vandenbergh, 1983; Vandenbergh & Coppola, 1987). One area of investigation has involved behavioral responses of young females lo urinary chemosignals from different sources. Perpubertal female mice appear, in general, to avoid urine that contains acceleratory substances, whereas peripubertal and adult females are attracted to such urine (Drickamer, 1989a). Young female mice that are accelerated in their sexual development apparently have higher mortality rates and lower lifetime reproduction (Drickamer, 1988). In contrast, females whose puberty is delayed have larger litters and a greater lifetime reproductive output. These previous findings raise the issue of whether young female mice might not be able to influence their own sexual development via the odor preferences that they exhibit. Where possible, young females should behave in a manner to influence their own reproductive physiology. On the one hand it seems probable that in a shortlived rodent, reproduction should commence as early as possible and the prediction would be that the females should seek to expose themselves to puberty-accelerating substances, for example, male urine. On the other hand, the costs that are associated with early maturation suggest that females might be better off selecting their associations with odor cues in a manner that delayed the onset of reproductive activity. That female rodents can influence their own reproductive physiology is not a unique idea. Adult female rats may exert some behavioral control, via their odor preferences, with regard to their estrous cycles (McClintock, 1983), and pregnant female mice avoid odor from strange males for the critical days, early in pregnancy, before implantation (Drickamer, 1989b). Two experiments were designed to test whether young female mice select associations with odor cues, in the form of soiled bedding, in a manner that affects their sexual development. An initial experiment was conducted with the purpose of demonstrating that young female mice housed in the test apparatus, but presented with only one type of soiled bedding, would exhibit different ages for first vaginal estrus depending upon which urinary chemosignal cues or water were present. This was followed by the main experiment in which two major hypotheses were tested: ( I ) Young female mice provided with the opportunity to choose between soiled bedding of two types will spend their time in a manner that results in approximately the same age for puberty, as measured by first vaginal estrus, regardless of the possible combinations of odor cues from which they can select, and (2) Observations on the time spent by the young mice on soiled bedding of different types and the location of their sleepinghesting sites will shift during the course of development.
Methods General Methods The mice used for these studies were from a stock of IClUAlb mice maintained at Williams College in Massachusetts with infusions of new mice from the original supplier (Wards Scientific, Rochester, NY) at intervals of about every 2 years. All
BEHAVIOR AND PUBERTY IN MICE
463
colony mice were maintained in shoebox cages (28 cm x 15 cm x 15 cm deep) of opaque polypropylene with fitted wire lids and a bedding of ground wood shavings changed once per week. All mice were provided with water and fed Wayne Lab Blox ad libitum. The mouse colony and test aquaria described below were maintained in a room with a 12 : 12 hr light/dark cycle with the overhead fluorescent lights on from 0600-1800 hr. Test mice were placed into individual 40 l(25 cm x 50 cm x 30 cm deep) aquaria upon weaning at 21 days of age; six or eight aquaria were used at a time. Mice remained in the aquaria until attaining first estrus. Each aquarium contained a 2.5 cm high x 25 crn long x 0.7 cm thick Plexiglas partition glued to the floor across the short dimension, dividing the floor surface into two equal halves. Openings cut in the partition contained small stainless steel dishes, one filled with mouse chow and the other with water. Urine and water were sprayed onto the bedding using 2-mI hypodermic syringes with 28-gauge needles; separate syringes were maintained for each of the three substances sprayed. Prior to placing mice into the aquaria at the start of a test sequence, 2 ml of each of the appropriate substances were sprayed on 500 cc of clean bedding spread on each half of the aquarium floor. (The amount of bedding selected was small enough that little, if any, movement of bedding across the 2.5 cm high central partition occurred during the the course of any test.) The spraying process was repeated every day until the mouse attained first estrus; urine or water spraying was carried out at the time the mouse was removed as described below. Fresh urine was collected each day for spraying by holding donor mice over a Petri dish and gently stroking the flanks and belly. Adult male urine was collected from 15 to 20 individuals in each month; a minimum of 4 and maximum of 8 mice were used for any one collection. All males were between 100 and 220 days of age at the time of urine collection. Three cages of 8 adult females were used each month; a minimum of 8 and maximum of 16 mice were used for any one collection. Females were 70 to 200 days of age at the time of urine collection and had been caged together for at least 2 weeks prior to their use as urine donors (Coppola & Vandenbergh, 1985; Drickamer, 1983). Mice were weighed to the nearest gram at the start of each experiment in order to test whether there were any significant differences in mean body mass for the different treatments. During an experimental test, subject mice were removed briefly ( 0.25
15 5 p < 0.05
12 8 p > 0.25
6 14 0.05 < p < 0.10
9 11 p > 0.50
4 16 p < 0.01
19 1 p < 0.001
17 3 p < 0.005
16
4 p < 0.01
with grouped female urine on the first test day, did not exhibit a statistically significant preference on the 7th test day, and selected the side with male urine in significant numbers for their sleeping site on the day of first estrus.
Discussion The initial experiment revealed that there were significant differences in age of puberty for mice housed in the test apparatus and provided with the same substance, urine or water, on both sides of the aquarium. Mean body weights at the start of each experiment did not differ across treatments. Thus, the experimental manipulations performed did not, of themselves, produce any differences relative to the known puberty-influencing effects of the urinary chemosignals (Drickamer, 1986;Vandenbergh, 1983), nor did any significant differences in initial body weights affect the puberty results in either experiment. From the main experiment, two major conclusions emerge: (1) Young female mice, when given a choice, spend time with bedding samples that influence their puberty such that the mean age for sexual maturation is the same regardless of the urinary chemosignals that are on the bedding samples; and (2) the selection process by females begins by spending more time with bedding that is relatively more likely to retard puberty, but changes as the mice near puberty to a preference for soiled bedding that enhances onset of first estrus. The control treatment condition with water sprayed on both bedding samples resulted in no clear differential side bias by the mice in the test situation employed. This finding is important in that it indicates that choices made by mice in the other three treatment pairs were not influenced by some external condition(s), for example, a light or temperature gradient that was affecting all mice. The first conclusion is supported by data from all three treatment groups of Experiment 2. Mean ages at first estrus among these three groups did not differ from one another and they were not different from the control condition. It appears that young female mice behave in a manner that tends to produce an age for puberty that is relatively constant. One might expect that young mice, with short
BEHAVIOR AND PUBERTY IN MICE
469
life expectancies, would be selected for attaining puberty and beginning reproduction as soon as possible. Several lines of evidence argue against this notion. First, Bronson (1979) presented the view that young females are delayed in attaining puberty until they have dispersed. He supports this contention with evidence concerning chemosignals and socio-tactile cues that retard sexual maturation in females until they have left the natal area. Second, young female mice that mature early, due to exposure to male mice or male urine, tend to have lower survival rates and smaller litters than females that are delayed in reaching puberty (Drickamer, 1988). There may be some sort of balance in the effects of natural selection on the behavior of the females with respect to self-exposure to factors, for example, urinary chemosignals, that could influence their sexual development. For the treatment pair involving male urine and urine from grouped females, it is noteworthy that age at vaginal introitus did not differ from the other treatments. This may be due to the fact that the females did spend some portion of their time on the male urine side, possibly counteracting the retarding effects due to spending a majority of the time on the side with urine from grouped females. The second conclusion is in agreement with previous findings wherein young female mice given brief (10-20 min) tests, exhibited shifts in their odor preferences as they matured (Drickamer, 1989a). Near the time of first estrus females apparently switch from avoiding odors of males to a clear preference for male odors. In the present study, where female preferences were tested over a much longer period, they exhibited a similar time course for the shift in bedding preference. These data confirm the first conclusion above by demonstrating one external mechanism by which females’ behavior can effect a change in internal physiology. It should be noted, however, that it may be that the causal relationship is not fully established by these findings. That is, it may be that behavior changes internal physiology or conversely, internal physiological changes taking place as puberty approaches may affect behavioral preferences. Separating these two alternative explanations may be a difficult task.
Notes This research was supported in part by United States Public Health Service grant HD-08585. I thank Williams College for providing the facilities and animal care personnel for this research. Two anonymous reviewers provided very helpful comments on an earlier version of the manuscript.
References Bronson, F. H. (1979). The reproductive ecology of the house mouse. Quarterly Review of Biology, 54, 265-299. Coppola, D. M., & Vandenbergh, J. G. (1985). Effect of density, duration of grouping, and age of urine stimulation on the puberty delay pheromone in female mice. Journal ofReproduction and Fertilify, 73, 517-522. Drickamer, L. C. (1981). Selection for age of sexual maturation in mice and the consequences for population regulation. Behavioral and Neural Biology, 31, 82-89. Drickamer, L. C. (1983). Effect of period of grouping of donors and duration of stimulus exposure on delay of puberty in female mice by a urinary chemosignal from grouped females. Journal of Reproduction and Fertility, 69, 723-127.
470
DRICKAMER
Drickamer, L. C. (1984). Seasonal variation in acceleration and delay of sexual maturation in female mice by urinary chemosignals. Journal of Reproduction and Fertility, 72, 55-58. Drickamer, L. C. (1986). Puberty-influencing chemosignals in house mice: Ecological and evolutionary aspects. In D. Duvall, D. Muller-Schwarze, & R. M. Silverstein (Eds.), Chemical signuls in uertebrutes ZV (pp. 441-455). New York: Plenum Press. Drickamer, L. C. (1987). Seasonal variations in the effectiveness of urinary chemosignals influencing puberty in female house mice. Journal of Reproducrion and Ferrility, 80, 295-300. Drickamer, L. C. (1988). Long-term effects of accelerated or delayed sexual maturation on reproductive output in wild female house mice (Mus musculus). /014rna/ of Reproduction and Fertility, 83, 439-445. Drickamer, L. C. (1989a). Odor preferences of wild stock female house mice ( M u s musculus) tested at three ages using urine and other cues from conspecific males and females. Journal qfChemic,u/ E~oc-ol~gV, 15, 1971-1987. Drickamer, L. C . (1989b). Pregnancy block in wild stock house mice, Mus dome.sticus: Olfactory preferences of females during gestation. Animal Behauiour, 37, 690-692. Laurie, E. M. 0. (1946). The reproduction of the house mouse (Mus musculus) living in different environments. Proceedings of the Royal Society of London, Series B , 133, 248-281. Lenington, S. (1983). Social preferences for partners carrying “good genes” in wild house mice. Animul Behaviour, 31, 325-333. McClintock, M. K. (1983). Pheromonal regulation of the ovarian cycle: Enhancement, suppression, and synchrony. In J. G . Vandenbergh (Ed.), Pheromones and mammulian reproduction (pp. 113-149). New York: Academic Press. Rugh, R. (1968). The mouse, its reproduction and development. Minneapolis: Burgess. Sokal, R. R., & Rohlf, F. J . (1981). Biometry (2nd ed.). San Francisco: W. H. Freeman. Statview 11. (1990). Manual for the use of Statview I1 for the MacZntosh. Berkeley, CA: Abacus Concepts. Vandenbergh, J. G. (1969). Male odor accelerates female sexual maturation in mice. Endocrinology, 84, 658-660. Vandenbergh, J. G . (1983). Pheromonal regulation of puberty. In J. G . Vandenbergh (Ed.), Pheromone5 and mammalian reproduction (pp. 95-1 12). New York: Academic Press. Vandenbergh, J. G . , & Coppola, D. M. (1987). The physiology and ecology of puberty modulation by primer pheromones. Advances in the Study of Behavior, 16, 71-107.
Female house mice were reared from weaning at 21 days of age until first vaginal estrus in 40 1 aquaria in which they were given a choice of exposing themselves to bedding placed on opposite halves of the aquarium floor and sprayed with water or urine containing puberty-influencing chemosignals. In Experimental I , mice housed with only male urine cues sprayed on the bedding matured significantly earlier and mice housed with only grouped female urine sprayed on the bedding matured significantly later than control mice where water was sprayed on the bedding for both halves of the aquarium. In Experiment 2, there were no significant differences in mean ages at vaginal introitus or first estrus for females reared with choices between (a) bedding sprayed with male urine versus bedding sprayed with water, (b) bedding sprayed with urine from grouped females versus bedding sprayed with water, (c) bedding sprayed with male urine versus bedding sprayed with urine from grouped females, or (d) the control condition where both sides of the aquarium contained bedding sprayed with water. Analysis of continuous video tapes of the locations of the females for Experiment 2 revealed that females chose initially to spend more time on the half of the floor with bedding that delayed puberty relative to the other side, but shifted their preference toward a more puberty-enhancing signal at about the time of first estrus. Female house mice appear to be able to exert some behavioral control over their own sexual maturation. 0 1992 John Wiley & Sons, Inc.
Sexual development and the onset of puberty are important both as key transition periods in the course of development and, in many species of rodents, as an indicator of the onset of reproduction. In many rodent species, puberty can be equated with generation time, certainly during that portion of the year when animals are sexually active. A variety of factors can influence the timing of puberty in mammals, particularly rodents (Bronson, 1979; Drickamer, 1986; Vandenbergh & Copola, 1987). These factors include genetics, ambient conditions, health and nutrition, and social influences such as urinary chemosignals (Drickamer, 1981; Laurie, 1946; Vandenbergh, 1983). For rodents, and house mice in particular, Reprint requests should be sent to Dr. Lee C. Drickamer, Department of Zoology, Southern Illinois University, Carbondale, I L 62901-6501 Received for publication 14 February 1992 Revised for publication 13 May 1992 Accepted at Wiley 18 May 1992
Developmental Psychobiology 25(6):461-470 (1992) 0 1992 by John Wiley & Sons, Inc.
CCC 0012-1630/92/060461-10
462
DRICKAMER
many aspects of the urinary chemosignal system influencing sexual development have been examined with respect to both the donors of puberty-influencing urinary signals and the young female recipients (Drickamer, 1986; Vandenbergh, 1983; Vandenbergh & Coppola, 1987). One area of investigation has involved behavioral responses of young females lo urinary chemosignals from different sources. Perpubertal female mice appear, in general, to avoid urine that contains acceleratory substances, whereas peripubertal and adult females are attracted to such urine (Drickamer, 1989a). Young female mice that are accelerated in their sexual development apparently have higher mortality rates and lower lifetime reproduction (Drickamer, 1988). In contrast, females whose puberty is delayed have larger litters and a greater lifetime reproductive output. These previous findings raise the issue of whether young female mice might not be able to influence their own sexual development via the odor preferences that they exhibit. Where possible, young females should behave in a manner to influence their own reproductive physiology. On the one hand it seems probable that in a shortlived rodent, reproduction should commence as early as possible and the prediction would be that the females should seek to expose themselves to puberty-accelerating substances, for example, male urine. On the other hand, the costs that are associated with early maturation suggest that females might be better off selecting their associations with odor cues in a manner that delayed the onset of reproductive activity. That female rodents can influence their own reproductive physiology is not a unique idea. Adult female rats may exert some behavioral control, via their odor preferences, with regard to their estrous cycles (McClintock, 1983), and pregnant female mice avoid odor from strange males for the critical days, early in pregnancy, before implantation (Drickamer, 1989b). Two experiments were designed to test whether young female mice select associations with odor cues, in the form of soiled bedding, in a manner that affects their sexual development. An initial experiment was conducted with the purpose of demonstrating that young female mice housed in the test apparatus, but presented with only one type of soiled bedding, would exhibit different ages for first vaginal estrus depending upon which urinary chemosignal cues or water were present. This was followed by the main experiment in which two major hypotheses were tested: ( I ) Young female mice provided with the opportunity to choose between soiled bedding of two types will spend their time in a manner that results in approximately the same age for puberty, as measured by first vaginal estrus, regardless of the possible combinations of odor cues from which they can select, and (2) Observations on the time spent by the young mice on soiled bedding of different types and the location of their sleepinghesting sites will shift during the course of development.
Methods General Methods The mice used for these studies were from a stock of IClUAlb mice maintained at Williams College in Massachusetts with infusions of new mice from the original supplier (Wards Scientific, Rochester, NY) at intervals of about every 2 years. All
BEHAVIOR AND PUBERTY IN MICE
463
colony mice were maintained in shoebox cages (28 cm x 15 cm x 15 cm deep) of opaque polypropylene with fitted wire lids and a bedding of ground wood shavings changed once per week. All mice were provided with water and fed Wayne Lab Blox ad libitum. The mouse colony and test aquaria described below were maintained in a room with a 12 : 12 hr light/dark cycle with the overhead fluorescent lights on from 0600-1800 hr. Test mice were placed into individual 40 l(25 cm x 50 cm x 30 cm deep) aquaria upon weaning at 21 days of age; six or eight aquaria were used at a time. Mice remained in the aquaria until attaining first estrus. Each aquarium contained a 2.5 cm high x 25 crn long x 0.7 cm thick Plexiglas partition glued to the floor across the short dimension, dividing the floor surface into two equal halves. Openings cut in the partition contained small stainless steel dishes, one filled with mouse chow and the other with water. Urine and water were sprayed onto the bedding using 2-mI hypodermic syringes with 28-gauge needles; separate syringes were maintained for each of the three substances sprayed. Prior to placing mice into the aquaria at the start of a test sequence, 2 ml of each of the appropriate substances were sprayed on 500 cc of clean bedding spread on each half of the aquarium floor. (The amount of bedding selected was small enough that little, if any, movement of bedding across the 2.5 cm high central partition occurred during the the course of any test.) The spraying process was repeated every day until the mouse attained first estrus; urine or water spraying was carried out at the time the mouse was removed as described below. Fresh urine was collected each day for spraying by holding donor mice over a Petri dish and gently stroking the flanks and belly. Adult male urine was collected from 15 to 20 individuals in each month; a minimum of 4 and maximum of 8 mice were used for any one collection. All males were between 100 and 220 days of age at the time of urine collection. Three cages of 8 adult females were used each month; a minimum of 8 and maximum of 16 mice were used for any one collection. Females were 70 to 200 days of age at the time of urine collection and had been caged together for at least 2 weeks prior to their use as urine donors (Coppola & Vandenbergh, 1985; Drickamer, 1983). Mice were weighed to the nearest gram at the start of each experiment in order to test whether there were any significant differences in mean body mass for the different treatments. During an experimental test, subject mice were removed briefly ( 0.25
15 5 p < 0.05
12 8 p > 0.25
6 14 0.05 < p < 0.10
9 11 p > 0.50
4 16 p < 0.01
19 1 p < 0.001
17 3 p < 0.005
16
4 p < 0.01
with grouped female urine on the first test day, did not exhibit a statistically significant preference on the 7th test day, and selected the side with male urine in significant numbers for their sleeping site on the day of first estrus.
Discussion The initial experiment revealed that there were significant differences in age of puberty for mice housed in the test apparatus and provided with the same substance, urine or water, on both sides of the aquarium. Mean body weights at the start of each experiment did not differ across treatments. Thus, the experimental manipulations performed did not, of themselves, produce any differences relative to the known puberty-influencing effects of the urinary chemosignals (Drickamer, 1986;Vandenbergh, 1983), nor did any significant differences in initial body weights affect the puberty results in either experiment. From the main experiment, two major conclusions emerge: (1) Young female mice, when given a choice, spend time with bedding samples that influence their puberty such that the mean age for sexual maturation is the same regardless of the urinary chemosignals that are on the bedding samples; and (2) the selection process by females begins by spending more time with bedding that is relatively more likely to retard puberty, but changes as the mice near puberty to a preference for soiled bedding that enhances onset of first estrus. The control treatment condition with water sprayed on both bedding samples resulted in no clear differential side bias by the mice in the test situation employed. This finding is important in that it indicates that choices made by mice in the other three treatment pairs were not influenced by some external condition(s), for example, a light or temperature gradient that was affecting all mice. The first conclusion is supported by data from all three treatment groups of Experiment 2. Mean ages at first estrus among these three groups did not differ from one another and they were not different from the control condition. It appears that young female mice behave in a manner that tends to produce an age for puberty that is relatively constant. One might expect that young mice, with short
BEHAVIOR AND PUBERTY IN MICE
469
life expectancies, would be selected for attaining puberty and beginning reproduction as soon as possible. Several lines of evidence argue against this notion. First, Bronson (1979) presented the view that young females are delayed in attaining puberty until they have dispersed. He supports this contention with evidence concerning chemosignals and socio-tactile cues that retard sexual maturation in females until they have left the natal area. Second, young female mice that mature early, due to exposure to male mice or male urine, tend to have lower survival rates and smaller litters than females that are delayed in reaching puberty (Drickamer, 1988). There may be some sort of balance in the effects of natural selection on the behavior of the females with respect to self-exposure to factors, for example, urinary chemosignals, that could influence their sexual development. For the treatment pair involving male urine and urine from grouped females, it is noteworthy that age at vaginal introitus did not differ from the other treatments. This may be due to the fact that the females did spend some portion of their time on the male urine side, possibly counteracting the retarding effects due to spending a majority of the time on the side with urine from grouped females. The second conclusion is in agreement with previous findings wherein young female mice given brief (10-20 min) tests, exhibited shifts in their odor preferences as they matured (Drickamer, 1989a). Near the time of first estrus females apparently switch from avoiding odors of males to a clear preference for male odors. In the present study, where female preferences were tested over a much longer period, they exhibited a similar time course for the shift in bedding preference. These data confirm the first conclusion above by demonstrating one external mechanism by which females’ behavior can effect a change in internal physiology. It should be noted, however, that it may be that the causal relationship is not fully established by these findings. That is, it may be that behavior changes internal physiology or conversely, internal physiological changes taking place as puberty approaches may affect behavioral preferences. Separating these two alternative explanations may be a difficult task.
Notes This research was supported in part by United States Public Health Service grant HD-08585. I thank Williams College for providing the facilities and animal care personnel for this research. Two anonymous reviewers provided very helpful comments on an earlier version of the manuscript.
References Bronson, F. H. (1979). The reproductive ecology of the house mouse. Quarterly Review of Biology, 54, 265-299. Coppola, D. M., & Vandenbergh, J. G. (1985). Effect of density, duration of grouping, and age of urine stimulation on the puberty delay pheromone in female mice. Journal ofReproduction and Fertilify, 73, 517-522. Drickamer, L. C. (1981). Selection for age of sexual maturation in mice and the consequences for population regulation. Behavioral and Neural Biology, 31, 82-89. Drickamer, L. C. (1983). Effect of period of grouping of donors and duration of stimulus exposure on delay of puberty in female mice by a urinary chemosignal from grouped females. Journal of Reproduction and Fertility, 69, 723-127.
470
DRICKAMER
Drickamer, L. C. (1984). Seasonal variation in acceleration and delay of sexual maturation in female mice by urinary chemosignals. Journal of Reproduction and Fertility, 72, 55-58. Drickamer, L. C. (1986). Puberty-influencing chemosignals in house mice: Ecological and evolutionary aspects. In D. Duvall, D. Muller-Schwarze, & R. M. Silverstein (Eds.), Chemical signuls in uertebrutes ZV (pp. 441-455). New York: Plenum Press. Drickamer, L. C. (1987). Seasonal variations in the effectiveness of urinary chemosignals influencing puberty in female house mice. Journal of Reproducrion and Ferrility, 80, 295-300. Drickamer, L. C. (1988). Long-term effects of accelerated or delayed sexual maturation on reproductive output in wild female house mice (Mus musculus). /014rna/ of Reproduction and Fertility, 83, 439-445. Drickamer, L. C. (1989a). Odor preferences of wild stock female house mice ( M u s musculus) tested at three ages using urine and other cues from conspecific males and females. Journal qfChemic,u/ E~oc-ol~gV, 15, 1971-1987. Drickamer, L. C . (1989b). Pregnancy block in wild stock house mice, Mus dome.sticus: Olfactory preferences of females during gestation. Animal Behauiour, 37, 690-692. Laurie, E. M. 0. (1946). The reproduction of the house mouse (Mus musculus) living in different environments. Proceedings of the Royal Society of London, Series B , 133, 248-281. Lenington, S. (1983). Social preferences for partners carrying “good genes” in wild house mice. Animul Behaviour, 31, 325-333. McClintock, M. K. (1983). Pheromonal regulation of the ovarian cycle: Enhancement, suppression, and synchrony. In J. G . Vandenbergh (Ed.), Pheromones and mammulian reproduction (pp. 113-149). New York: Academic Press. Rugh, R. (1968). The mouse, its reproduction and development. Minneapolis: Burgess. Sokal, R. R., & Rohlf, F. J . (1981). Biometry (2nd ed.). San Francisco: W. H. Freeman. Statview 11. (1990). Manual for the use of Statview I1 for the MacZntosh. Berkeley, CA: Abacus Concepts. Vandenbergh, J. G. (1969). Male odor accelerates female sexual maturation in mice. Endocrinology, 84, 658-660. Vandenbergh, J. G . (1983). Pheromonal regulation of puberty. In J. G . Vandenbergh (Ed.), Pheromone5 and mammalian reproduction (pp. 95-1 12). New York: Academic Press. Vandenbergh, J. G . , & Coppola, D. M. (1987). The physiology and ecology of puberty modulation by primer pheromones. Advances in the Study of Behavior, 16, 71-107.
