Physiology & Behavior 89 (2006) 133 – 138
Effects of prenatal stress on sexual partner preference in mice
Leslie R. Meek a,⁎, Kalynn M. Schulz b , Courtney A. Keith c
a
Division of Social Sciences, University of Minnesota, Morris, 600 E. 4th St., Morris, MN 56267, United States
b
Michigan State University, E. Lansing, MI, 48824, United States
c
University of South Dakota, Medical School, Vermillion, SD, 57069, United States
Received 23 March 2005; received in revised form 28 April 2006; accepted 1 May 2006
Abstract
Three-month old, male Swiss Webster mice were born to either control dams or dams who had been prenatally stressed with light, heat, noise
and handling during the last week of gestation. As adults, male offspring were tested on sexual partner preference and sexual behavior (mounting,
intromissions and lordosis) with a sexually experienced male stimulus animal and a stimulus estrous female. In comparison to males born to
control dams, prenatally stressed males showed a sexual partner preference for the sexually active male as demonstrated by a negative partner
preference score, more and longer visits to the male's compartment, fewer and shorter visits to the female's compartment and longer latencies to
and lower frequencies of mounts and intromissions of females. In addition, stressed males showed a greater frequency of lordosis and a higher
lordosis quotient than did control males. This study is the first to investigate the effects of prenatal stress alone, without hormonal manipulation, on
sexual partner preference using both a partner preference paradigm and measures of sexual behavior such as mounting, intromissions and lordosis.
These findings support the suggestion that prenatal stress alone is enough to significantly affect sexual partner preference in male mice.
© 2006 Elsevier Inc. All rights reserved.
Keywords: Mice; Sexual partner preference; Sexual orientation; Homosexuality; Prenatal stress
It has been unequivocally demonstrated that prenatal stress
during the last week of gestation in rats results in marked
deficits in adult male mating behavior, with males showing
fewer attempts to copulate, fewer successful ejaculations and
longer latencies to mounts, intromissions and ejaculations (e.g.,
[1–3]), without accompanying alterations in sexual organs [4].
It was subsequently determined that stress during gestation
shifts the typically high concentration of testosterone released
on gestational day 17 to gestational days 18 and 19 [5]. This
shift in the timing of the peak of testosterone is positively
correlated with decreased steroid aromatase activity in the brain
during gestational days 17–21 [6] and a markedly smaller adult
SDN-POA [7,8].
The SDN-POA of adult male rats is typically significantly
larger than that of females [9,10]. In sexually naïve male rats,
bilateral lesions of the SDN-POA have been shown to
⁎ Corresponding author. Tel.: +1 320 589 6213; fax: +1 320 589 6117.
E-mail address: meeklesr@morris.umn.edu (L.R. Meek).
0031-9384/$ - see front matter © 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.physbeh.2006.05.006
decrease the number of animals ejaculating and to increase
latencies to mounts, intromissions and ejaculations [11].
However, others have found no relationship between the size
of the SDN-POA and adult ejaculatory performance [8].
Instead, it is possible that the volume of the SDN-POA is
related to the probability that an adult male rat will
demonstrate lordosis when mounted. Thus, a smaller nucleus
predicts the increased likelihood of lordosis when a male is
mounted by another male [8,12,13].
The conclusion that has been drawn from the above evidence
is that by shifting the timing of the peak of testosterone, a
critical period of brain sexual differentiation is missed so that
brain nuclei involved in the expression of male sexual behavior
are demasculinized, resulting in a decrease in the expression of
male-typical sexual behaviors as an adult. Concomitantly, there
is a failure to defeminize central mechanisms, resulting in an
increase in the probability of the expression of female-typical
sexual behaviors in the adult male (e.g., [1,4,14]).
Since these discoveries have been made, many have
questioned whether the shift in the timing of the gestational
134
L.R. Meek et al. / Physiology & Behavior 89 (2006) 133–138
testosterone surge and the resultant effects on central control
mechanisms might not also affect sexual partner preference in
adult male rodents. Studies have indicated that in a sexual
partner preference test, adult males, even with no prior sexual
experience, show a strong preference for an estrous female over
a non-estrous female or an intact, adult male [15–17]. Studies
using a partner preference paradigm, where animals have a
choice between an intact, sexually experienced male and an
intact (or hormonally induced) estrous female have shown that
male rats who have been treated pre- and/or post-natally with
anti-estrogens or anti-androgens or who receive a bilateral
lesion of the MPOA–AH changed their partner preference from
that of an estrous female to an intact, sexually experienced male
[18–23] lending support to this suggestion.
To date, while a number of studies have investigated the
effects of pre- and/or post-natal anti-androgens and antiestrogens on sexual partner preference (e.g., [21,22,24,25]
there have been no investigations of the effects of prenatal stress
on sexual partner preference in gonadally intact male rodents
without manipulating hormones during development or adulthood. In addition, unlike other partner preference studies, this
study evaluated direct measures of sexual behavior such as
mounting, intromissions and lordosis along with standard
partner preference measures.
1. Methods
1.1. Animals
Three-month old, male, Swiss Webster mice were used in
this experiment. All animals were bred at the University of
Minnesota, Morris, from breeding stock obtained from Taconic
Farms, Inc. Food (Purina Mouse Chow # 5015, Ralston-Purina
Co., St. Louis, MO) and water was available ad lib. All animals
were maintained in a reversed light–dark cycle of 14 h light and
10 h dark, with a temperature of 20° ± 2 °C. Animals were cared
for according to the standards published by the University of
Minnesota Animal Care and Use Committee and in accordance
with federal regulations as detailed in the National Institutes of
Health Guide for the Care and Use of Laboratory Animals.
1.2. Procedure
1.2.1. Mating and stress
Swiss Webster dams were paired with sexually experienced
males for 1 week. During this time, animals were videotaped to
determine the date and time that mating occurred. On day 12
after mating, dams were randomly assigned to either a stressed
(n = 20) or a non-stressed (control; n = 20) group (gestation
length is 19 d in Swiss Webster mice). Dams were singly housed
in 45 × 26.5 × 20 cm opaque polycarbonate cages.
Stressed dams were exposed to stress 3 times daily for
45 min each time during the last week of pregnancy. All stress
occurred during the light portion of the light–dark cycle. Stress
occurred at random times so that dams could not predict when
stress would occur [26]. A record of when stress occurred each
day was kept to ensure that stress did not occur at the same time
each day and that it occurred roughly equally across the 14 h
light period. Stress sessions occurred a minimum of 2 h apart.
Stress consisted of handling (being picked up by the tail), noise
(being moved to a different room on a noisy cart), light
(180.5 L/ft2) and increased temperatures (34° ± 2 °C). All stress
procedures occurred in the same room. Food and water were not
available during stress. Non-stressed dams remained in their
cages in a separate room while stressed animals were stressed in
another, sound-proofed room. Stressed and non-stressed
animals were housed in separate rooms.
Following birth, pups were housed with their birth-dams and
littermates in 45 × 26.5 × 20 cm cages until weaning at 21 d of
age. They were then singly housed in 27 × 17 × 13 cm cages until
testing at the age of 3 months. All animals were sexually naïve
at the time of testing. One pup from each litter was used in
sexual partner preference testing (n = 20 in each group) and one
pup from each litter was used in lordosis testing to eliminate
litter effects (n = 20 in each group; 27).
1.2.2. Sexual partner preference testing
For 4 d prior to sexual partner preference testing, males were
habituated to the testing arena for 30 min each day. During
habituation, the same stimulus animals that were used during
testing for each individual experimental animal were present (a
3-month old sexually intact, experienced male and a 3-month
old sexually experienced behaviorally estrous female) but were
confined to wire-mesh cages on opposite sides of the arena.
Their position in the testing chamber was randomly alternated
during each habituation session. On the fifth day, the
experimental animal was simultaneously exposed to the two
stimulus animals, each of which was tethered at opposite ends
of the arena. The tether consisted of a plastic tie (Radio Shack)
as a collar with a fishing swivel attached. A 36 cm length of
flexible cord was attached by one end to the fishing swivel and
by the other end to the top of the aquarium. This apparatus
allowed the stimulus animals to move freely and engage in
sexual behavior, but confined them within a small portion of
their compartment.
The arena consisted of a 75 × 30 × 28 cm glass aquarium that
was visually divided into 3 equal areas with tape. The test male
was placed into the middle compartment and separated from the
stimulus male and estrous female by partitions for a 15-minute
period. Once the partitions were removed, a 60-minute
preference test ensued. All animals received exposure to one
of 20 stimulus males and one of 20 stimulus females. Each
stimulus animal was used in a test with a stressed male and a
non-stressed male. All habituation and testing occurred at
random times during the dark portion of the reversed day–night
cycle and under red light. Each test was videotaped with a
Panasonic Low-Light Videorecorder and no experimenters were
present during testing.
Behavioral estrous in the female stimulus animal was
determined by daily vaginal smears, stained with thionin and
examined microscopically to determine whether a smear was
classified as proestrous. Smears were rated as proestrous if most
of the cells were nucleated. Only females rated as being in
proestrous were used as stimulus females.
L.R. Meek et al. / Physiology & Behavior 89 (2006) 133–138
Table 1
Partner preference variables
Stressed versus non-stressed males
Behavior
Frequency in
female compartment
Frequency in
male compartment
Time spent in female's
compartment (sec)
Time spent in male's
compartment (sec)
Preference score
Latency to mount
female (sec)
Frequency of
mounting female
Latency to
intromissions
with female (sec)
Frequency of
intromissions
Stressed males
Non-stressed males
64.45 ± 4.0
131.8 ± 5.35
153.2 ± 3.68
81.65 ± 4.22
1535.85 ± 62.88
2692.4 ± 66.75
1843.45 ± 68.07
596.0 ± 31.27
− 307.01 ± 128.36
+2096.4 ± 95.41
3163 + 128.77
2165.0 + 83.40
0.66 + 0.54
3449.84 + 58.56
1.0 + 0.35
23.38 + 1.60
2175.47 + 47.87
15.55 + 1.19
t statistic
t = 9.95,
P < 0.0001
t = 15.42,
P < 0.0001
t = 13.15,
P < 0.0001
t = 18.75,
P < 0.0001
t = 16.25,
P < 0.0001
t = 5.92,
P < 0.0001
t = 11.78,
P < 0.0001
t = 11.81,
P < 0.0001
t = 10.74,
P < 0.0001
All values expressed as mean ± standard error of the mean.
P ≤ 0.05 considered significant.
There were 20 animals in each group that were tested on each dependent
variable.
The following behaviors were scored from the tape for
sexual partner preference testing:
1. Frequency and duration of visits to the female's or male's
compartment: A visit was scored as occurring when the
test male's entire body (excluding tail) had crossed the
tape marker and was inside the stimulus animal's
compartment.
2. Latency to first mount and frequency of mounts by the
experimental animal: A mount of a stimulus animal was
recorded when the test male oriented himself on top of the
caudal part of the stimulus animal's body with his hind feet
positioned on the flanks of the stimulus animal.
3. Latency to first intromission and frequency of intromissions:
An intromission was scored if the test male inserted his penis
into the vagina of the stimulus female or attempted to insert
his penis into the stimulus male.
4. Preference score: Time spent in the compartment containing
the sexually active male was subtracted from the time spent
in the compartment containing the estrous female; a positive
score indicates a preference for the estrous female; a negative
score indicates a preference for the sexually active male
[18,22,28].
1.2.3. Lordosis testing
Forty, 3-month old, Swiss Webster mice (one from each
litter; not the same animals as used in sexual partner preference
testing) were tested for lordosis behavior for 1 h or until 10
mounts had occurred, whichever occurred first. Frequency of
lordosis and lordosis quotient (number of lordosis responses /
number of mounts × 100) were both measured; 29). Each animal
135
was habituated to the testing arena as above and then placed in
the testing arena with an untethered, sexually active male.
Lordosis was defined as the experimental animal demonstrating
a concave back, tail deviation and neck extension in response to
being mounted by the stimulus animal [29].
1.3. Statistics
Student's t-tests were used for all comparisons between
stressed and control animals. Variability was expressed as
standard error of the mean and P ≤ 0.05 was considered
significant.
2. Results
2.1. Sexual partner preference
Stressed males made significantly fewer visits to the
female's compartment (t = 9.95, P < 0.0001) and significantly
more visits to the male's compartment (t = 15.42, P < 0.0001)
than did control males. Stressed males also spent significantly
less time in the female's compartment (t = 13.15, P < 0.0001)
and significantly more time in the male's compartment
(t = 18.75, P < 0.0001) than did control males. Stressed males
had a significantly lower mean preference score than did control
males. See Table 1.
Stressed males showed a significantly longer mean latency
to mount the estrous female (t = 5.92, P < 0.0001) and showed
significantly fewer mounts than control males (t = 11.78,
P < 0.0001). Similarly, stressed males had a significantly
longer mean latency to intromissions with the female
(t = 11.80, P < 0.0001) and showed significantly fewer mean
intromissions than did control males (t = 10.74, P < 0.0001).
See Table 1.
2.2. Lordosis frequency and quotient
Stressed males showed significantly more mean incidences
of lordosis than did control males (t = 4.50, P = 0.0002) when
paired with an experienced male. See Fig. 1. For those animals
Fig. 1. Mean frequency of lordosis (±SEM) in stressed and non-stressed males.
⁎ indicates significantly different from non-stressed animals, P < 0.05.
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L.R. Meek et al. / Physiology & Behavior 89 (2006) 133–138
Fig. 2. Mean lordosis quotient (±SEM) of stressed and non-stressed males.
⁎ indicates significantly different from non-stressed animals, P < 0.05.
that received 10 mounts, the lordosis quotient for stressed males
was significantly higher than for control males (t = 5.16,
P < 0.0001). See Fig. 2. Thirteen of twenty stressed males
showed lordosis when paired with another male, while only 3 of
20 control males did.
3. Discussion
Stressed males behaved significantly different than control
males on several definitive measures of sexual partner
preference. For example, when paired with a sexually active
female, stressed males demonstrated longer latencies to mounts
and intromissions and lower frequencies of both behaviors than
control males. When paired with a sexually active male, 65% of
stressed males exhibited lordosis, in contrast to 15% of control
males. Stressed males who received 10 mounts had a lordosis
quotient of 52.3% in comparison to that of 12.8% for control
males. This sexual partner preference by stressed males for a
sexually active male partner was corroborated and supported by
their negative partner preference score (indicating a male
partner preference) and the finding that they visited the male's
compartment more frequently and spent more time there than
did non-stressed control males. They also made fewer visits to
the female's compartment and spent less time there than did
control males. Overall, the above pattern of behavior on the part
of prenatally stressed male mice shows a marked shift in sexual
partner preference from estrous females to sexually active
males. This pattern of behavior is astonishing in Swiss Webster
mice, a highly aggressive species that is normally characterized
by intense inter-male aggression. In this study, inter-male
aggression was absent and appeared to be replaced by sexual
interest and behavior.
In addition to sexual interest, partner preference can also be
motivated by social attraction, curiosity or aggression on the
part of the experimental animal [30]. At least some of the
behavior that is expressed when an animal meets an unfamiliar
conspecific can be assumed to be motivated by curiosity.
However, we believe that our lengthy habituation period
before testing should have attenuated much of that curiosity,
so that true sexual partner preferences were expressed by our
animals.
In addition, since Swiss Webster mice, unlike rats, are not a
social species, few if any of the interactions between animals
should be mediated by social attraction. Swiss Webster mice, in
particular the males, are quite aggressive when they meet, and
social interaction between males would normally consist of
brief risk assessment behavior followed by fierce aggression.
During our partner preference tests, however, we saw no
aggressive interactions, so aggression can also be discounted as
a motive for approaching another animal, particularly the male
stimulus animal.
Vasey [31] notes that in order to determine true partner
preference, behaviors measured as dependent variables must be
sexual, at least in part. One way of demonstrating that nonheterosexual behaviors are sexual is to show that they are
similar to male–female sexual behaviors [31]. For this reason,
we included sexual behaviors such as mounting, intromissions
and lordosis in our study in addition to relying on partner
preference score to indicate choice of sexual partner. When
partner preference data is combined with data indicating that
stressed males are mounted by non-stressed stimulus males and
show lordosis in response, a stronger argument for same-sex
sexual partner preference can be made.
Previous studies have suggested that inexperienced males
show no preference for an estrous female over another stimulus
animal such as a sexually active male [32,33], but others have
found that even inexperienced males will show a preference for
an estrous female [15–17]. One author has suggested that
habituation to the testing arena prior to a sexual partner
preference test allows an inexperienced animal to express its
sexual attraction to an estrous female [17]. Since our study
allowed for adequate habituation to the testing arena and to the
stimulus animals, our sexually inexperienced animals can be
assumed to have expressed their real sexual partner preferences.
Stressed males almost never mounted stimulus males or
females. In contrast, as evidenced by the lordosis data, they
were mounted by the stimulus males. This suggests that
stressed males were not perceived by the stimulus males as a
typical male. When male Swiss Webster mice meet, aggressive
fighting usually occurs quickly. In contrast, in this study,
stimulus males treated the stressed males as if they were
receptive females and mounted them. It would be interesting to
determine whether stressed males were behaviorally mimicking
estrous female posture in any way, thus disarming the
aggression response and triggering sexual behavior on the
part of the stimulus male. Previous studies have demonstrated
that even without the use of exogenous hormones during
adulthood, some male rats will demonstrate lordosis as adults
in response to pairing with another male or manual stimulation
by an experimenter [34,35]. In our study, 15% of control males
displayed lordosis, indicating that some inexperienced male
mice that have not been exposed to any manipulation will
demonstrate female-typical sexual behavior as adults and show
lordosis when paired with a sexually active adult male. It is
possible that this is a facultative response, seen in some young,
inexperienced males in response to being paired with another
L.R. Meek et al. / Physiology & Behavior 89 (2006) 133–138
male. This response may occur as part of a constellation of
submissive behaviors that forestalls aggressive interactions and
functions to protect the submissive mouse from injury or death.
Thus, it appears as though there may be two functions of male–
male mounting, one of which occurs to forestall aggression and
one that actually indicates male–male sexual interest, as in our
study. If so, this suggests that each may arise from different
developmental events, but result in the same behavioral
endpoint.
While the majority of stressed males exhibited lordosis in
response to being paired with a sexually active male, none of
them displayed female-typical proceptive behaviors such as
dart-hopping or ear-wiggling. It is possible that different aspects
of female-typical mating behavior differentiate during different
critical perinatal periods, and had we disrupted testosterone
beyond the day of birth, at least some males would have
exhibited the full range of female mating behavior, as has been
demonstrated in rats (e.g., [4,22]).
The evidence of the partner preference data plus the sexual
behavior data indicates that 3-month old prenatally stressed
males showed a marked sexual partner preference for same-sex
partners. However, it remains possible that stress merely
delayed the development of the expression of full-blown male
sexual behavior. Had we tested animals at an older age, this
sexual preference may have been attenuated or reversed.
Further research needs to be done to determine whether age is
a factor in the expression of sexual partner preference
following prenatal stress. Thus, future studies could be
conducted in which adult stressed males could be tested for
sexual behavior with non-stressed males and females separately to determine the pattern of sexual behavior that occurs
with each stimulus animal. It would also be interesting to place
two prenatally-stressed males together in an arena to determine
the pattern of behavior they might express towards one
another. It seems unlikely that they would express either
aggressive or sexual behavior towards one another, since
neither will be perceived by the other to be a sexually active
heterosexual male. However, it would be interesting to observe
what behaviors they do engage in and compare that to intact
males interacting, intact females interacting and a male–female
dyad interacting.
This study supports the previous findings in rats that prenatal
stress alone can result in deficits in male sexual behavior and the
expression of female sexual behavior in adult rodents (e.g., [1–
5,7]) and extends those findings to show that prenatal stress
alone can also alter sexual partner preference in mice. In
addition, since the litter effect was controlled for in this study, it
also disputes the previous suggestion that prenatal stress effects
are mainly due to a litter effect [27].
In summary, this study suggests that prenatal stress alone,
without post-natal stress or hormonal manipulations can
significantly change sexual partner preference in mice, so
that males prefer sexually active males to an estrous female.
These findings have implications for sexual orientation
studies in non-humans. A number of studies have documented
that some species (e.g., rams) typically have a small number
of males who are unequivocally uninterested in females and
137
show male-typical behavior directed towards other males [36].
This study suggests that maternal stress might mediate such
sexual partner preferences. Vasey [31] has suggested that
trying to fit non-human male–male preferences into an
adaptationist framework is not feasible for every species,
and that for some species, it is reasonable to suppose that a
shift in sexual partner preference is maladaptive or functionally neutral, while for others it may actually serve an adaptive
function. Such determinations must be made based on the
evolutionary history and current ecology of each individual
species [31]. Thus far, human studies have not been able to
document any association between prenatal stress and human
male homosexuality (e.g., [37–40]), suggesting that rodent
and human responses to prenatal stress are not similar. Further
investigations may determine whether the rodent response to
prenatal stress is functional or maladaptive, although at least
one recent study suggests that this response is adaptive in that
it prepares offspring for the environmental and social
conditions they will encounter as adults [41].
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