Unformatted text preview: A NIMAL BEHAVIOUR, 2000, 59, 801–806
doi:10.1006/anbe.1999.1365, available online at http://www.idealibrary.com on Why some male Mongolian gerbils may help at the nest:
testosterone, asexuality and alloparenting
MERTICE M. CLARK & BENNETT G. GALEF, JR Department of Psychology, McMaster University
(Received 14 June 1999; initial acceptance 15 August 1999;
final acceptance 11 November 1999; MS. number: A8517) In previous studies we have shown that those male Mongolian gerbils, Meriones unguiculatus, that as
fetuses resided in intrauterine positions (IUPs) located between two female fetuses (2F males) have lower
circulating levels of testosterone, less well-developed genital musculature, and lower reproductive success
than males gestated in IUPs between two male fetuses (2M males). We have also found that such 2F males
spend more time caring for conspecific young than do 2M males, and that presence of a 2F male, but not
of a 2M male, with a lactating female and her litter decreases the cost to a dam of suckling one litter while
gestating a second litter conceived in postpartum oestrus. Here we show that some 2F males, those with
circulating levels of testosterone similar to those seen in females of their species, show no interest in
females in oestrus and fail to impregnate females with which they are paired. Such ‘asexual’ 2F males
spend 30–50% more time caring for nestlings than do sexually active 2F males. We suggest that such
asexual, highly parental 2F males are incapable of direct reproduction and are obligate helpers at the nest
that can contribute to their own fitness only by assisting to rear collateral kin. uterine exposure of male fetuses to exogenous testosterone as a consequence of their intrauterine positions
(IUPs) relative to members of the same and opposite sex is
an important correlate of variance in testosterone titres of
adult male Mongolian gerbils (vom Saal 1989; Clark et al.
1991, 1992b; Even et al. 1992). When adult, male gerbils
that had gestated in IUPs between females (2F males)
have, on average, circulating levels of testosterone half
those of conspecific males gestated in IUPs between males
(2M males; Clark et al. 1992b).
Fetal IUP predicts not only adult male gerbils’ testosterone titres, but also the development of some of their
reproductive anatomy. The bulbocavernosus muscle of
adult male gerbils gestated in 2M IUPs are 50% heavier
than those of their 2F brethren (Forger et al. 1996).
As might be expected, given that circulating levels of
testosterone and weight of the bulbocavernosus muscle
both correlate positively with sexual performance in male
rodents (Sachs 1982; Hart & Melese-d’Hospital 1983),
adult male gerbils from 2F IUPs show abnormalities in
their mating behaviour (Clark et al. 1990), and are significantly less likely than are adult 2M males to impregnate
unfamiliar females with which they are housed for several
weeks (Clark et al. 1992a).
In male Mongolian gerbils, circulating levels of testosterone mediate variance not only in sexual behaviour, but
in parental behaviour as well. Most male gerbils huddle
over and groom young, generally engaging in the same More than 90% of female mammals rear their young
without assistance (Kleiman & Malcolm 1981). However,
in some mammalian species, males assist conspecific
females to raise dependent juveniles (Alexander et al.
1991; Jennions & Macdonald 1994; Woodroffe & Vincent
1994; Carter & Roberts 1997; Moehlman & Hofer 1997).
Sometimes such parental males are potential fathers of
those they assist in rearing (Sussman & Garber 1987), but
more often they are not (Woodroffe & Vincent 1994).
Nonpaternal male helpers are generally assumed to be
temporarily unable to breed and to contribute indirectly
to their own fitness by rearing collateral kin while awaiting a more promising environment in which to father
offspring (Faulkes et al. 1989; Creel & Waser 1991). Here
we provide evidence of testosterone-mediated variation
in both the sexual and parental behaviour of male
Mongolian gerbils, Meriones unguiculatus, that may have
resulted in some male gerbils being permanent, rather
than temporary, helpers at nests whose only contribution
to fitness lies in rearing collateral kin.
Testosterone titres of adult male Mongolian gerbils vary
by a factor of more than 10, from less than 0.35 to more
than 3.72 ng/ml (Clark et al. 1992b; see also Probst 1985;
Probst et al. 1987). Although this variance in testosterone
titres has many potential causes, differing levels of intraCorrespondence: M. M. Clark, Department of Psychology, McMaster
0003–3472/00/040801+06 $35.00/0 2000 The Association for the Study of Animal Behaviour 801 2000 The Association for the Study of Animal Behaviour 802 ANIMAL BEHAVIOUR, 59, 4 parental behaviours displayed by lactating females,
except, of course, for lactation (Elwood 1975). However,
2F male gerbils (that have relatively low circulating levels
of testosterone) are significantly more parental than are
2M male gerbils (Clark et al. 1998). Castration in either
adulthood or adolescence significantly increases parental
behaviour in male gerbils, and when testosterone titres
of castrated males are returned to normal levels using
Silastic implants of testosterone, parental behaviour
decreases significantly (Clark & Galef 1999).
Differences in the parental behaviours of 2F and 2M
male gerbils appear to affect the fecundity of females with
which these males reside. At least under the relatively
stress-free conditions of the laboratory, the parental
activities of 2F males, but not those of 2M males,
are correlated with subsequent increase in female
reproductive success (Clark et al. 1997b).
Our previous results thus suggest that developmental
history results in some male gerbils being unable to
reproduce directly, some being exceptionally good
alloparents, and some having exceptionally low circulating levels of testosterone. Here, we directly assess the
correlation between testosterone level, parental behaviour, mating behaviour and reproductive competence in
In the first experiment, we determined the ability of 18
male Mongolian gerbils gestated in 2F IUPs to impregnate
females with which they were paired. We then observed
both the mating and parental behaviours of each of these
18 subjects. In a second experiment, we determined
circulating levels of testosterone in a second group of 14
male gerbils from 2F IUPs whose fertility and mating
behaviours we also measured. Thus, we could determine
whether fertility, adequacy of mating behaviour and
variation in frequency of parental behaviours were
correlated with testosterone titres.
We first determined the reproductive competence of each
of 18 male gerbils from 2F IUPs, then examined both the
mating behaviour and frequency of parental behaviour of
each subject. Methods
Eighteen 2F male and 144 virgin female Mongolian
gerbils that were third- or fourth-generation descendants
of stock animals acquired from Tumblebrook Farm
(Brookfield, Massachusetts) served as subjects. We had
delivered the 18 male subjects, each taken from a different dam on the last day of pregnancy, by Caesarean
section, and thus knew the IUP each had occupied during
Immediately following Caesarean delivery, we toeclipped each male subject and his littermates for permanent identification, and then placed the entire litter with
a foster mother that had delivered vaginally during the
24 h preceding delivery of the litter she was to rear (see Clark & Galef 1988 for details of Caesarean section and
We weaned subjects when they reached 32 days of age,
after which we kept them in same-sex groups of three or
four siblings until they were 60 days old, sexually mature
and therefore, ready to participate in the experiment. The
housing conditions we used after weaning not only
assured that all subjects had equal sexual experience
before the experiment started, but also allowed comparison with subjects that we had treated similarly in
Throughout the experiment, we maintained all subjects
with ad libitum access to food (Purina Rodent Laboratory
Chow 5001) and tap water in polypropylene shoebox
cages, measuring 35 30 cm and 15 cm high, housed in a
single colony room on a 12:12 h light:dark cycle, with
controlled temperature and humidity. Procedure
Measuring reproductive success. When each male subject was 60 days old, we paired him with a succession
of three unrelated, sexually mature, vaginally delivered,
virgin females from our colony. To start, we placed each
male in a shoebox cage, measuring 35 30 cm and 15 cm
high, with a virgin female, but separated from her by a
screen partition. Twenty-four h later, we removed the
partition and left the pair undisturbed (except for weekly
examination and twice weekly cage cleaning) until a
female was conspicuously pregnant or 30 days had
elapsed. We have reported previously that 95% of 2M
males impregnate females with which they are paired
within 20 days (Clark et al. 1992a). Measuring mating behaviour. One week after we had
examined the male’s reproductive competence, we
observed his behaviour when placed briefly with the first
of five females in artificially induced oestrus. We brought
each female into oestrus by anaesthetizing her (Metofane;
Janssen Pharmaceutica, North York, Ontario) and then
implanting subcutaneously at the back of her neck a
Silastic capsule (Dow-Corning Silastic tubing, 0.125 cm
outside diameter, 0.06 cm inside diameter, capped at
both ends with Dow-Corning Type A adhesive) that
contained a 5 mm column of oestradiol benzoate
(Ulibarri & Yahr 1996). In validating this procedure for
inducing oestrus, Ulibarri & Yahr (1996) found, during
30 min observation periods, that each member of a random sample of 10 adult male gerbils paired with a treated
female mounted and intromitted and that 9 of 10 ejaculated. We found similarly (unpublished observations)
that each of 20 2M male gerbils placed with females in
artificial oestrus induced using Ulibarri & Yahr’s technique, mounted and 18 of the 20 both intromitted and
ejaculated twice in 2 h.
Once each week, for 5 consecutive weeks, we placed
each male subject in the home cage of a female in
induced oestrus, but separated from her by a screen
partition. Twenty-four h later, we removed the partition
that separated the male and female. Then an observer,
unaware of the previous reproductive success of subject CLARK & GALEF: WHY SOME MALES MAY HELP AT THE NEST Table 1. Reproduction and parenting by 18 males in experiment 1 each tested with five females in induced oestrus,
then observed for 20 days while with a litter and female
Mean number of mounts
Mean number of intromissions
Latency to first ejaculate (min)
%Intervals with pups/mate absent Yes
67.2 (5.6) Yes
66.2 (4.3) No
87.8 (3.0) Numbers in parentheses=1 SEM. males, noted his behaviour towards the female until he
either achieved two ejaculations or 2 h had passed. We
used two ejaculations as a criterion for ending observation periods because Agren (1990) reported that
two ejaculations from a single male is sufficient for
impregnation. Measuring parental behaviour. To measure the parental behaviour of each of the subjects whose reproductive
success and mating behaviour we had observed, we
placed each male individually in the cage of a female
from our breeding colony when she was in the last week
of her 25 day pregnancy. On each of the first 20 days
postpartum, an observer who was unaware of the reproductive performance of the male, recorded, once every
20 s for 15 min, whether: (1) the male was crouched over
the young in a nursing posture (‘brooding the young’);
and (2) the male was present in the nest and in contact
with the young while the female was away from the nest
and young (e.g. Clark et al. 1997, 1998). We have used
the same procedures to sample parental behaviours
of male and female gerbils in previous studies (e.g. Clark
et al. 1997, 1998).
To equate the probability that females rearing young
with potent and with asexual foster fathers from 2F IUPs
would be both lactating and pregnant, on the day of
parturition of each female we briefly returned her to the
cage of the male that had sired her litter. Each female and
her original mate remained together until the male
achieved three ejaculations, which invariably occurred
within 30 min. We then returned the female to the cage
containing her litter and its foster father.
Eight of the 18 male subjects succeeded in impregnating one or more of the virgin females with which they
were paired; 10 failed to impregnate even one female. genital area of females, as they would have done to any
unfamiliar conspecific, they did not pursue females about
the cage and they did not attempt to mount them.
The remaining six males that failed to impregnate
females mounted and intromitted frequently, and
showed normal sexual interest in females, continually
sniffing their anogenital areas and pursuing the females
about the cage. During the five 2 h tests, one of these six
males failed to ejaculate, four achieved one ejaculation on
one or more of the five tests, and one achieved two
ejaculations on two tests. Presumably, any male that
mounted females and ejaculated had some chance of
direct reproduction. Parental behaviour
Males that failed to mount females in oestrus were
significantly more likely than were males that mounted,
both to assume a brooding posture over the pups
(ANOVA: F2,17 =4.57, P< 0.03; Table 1) and to remain with
the pups when the dam was away from the nest
(F2,17 =5.15, P< 0.02; Table 1). Males that failed to mount
females in oestrus and to impregnate females were significantly more parental than were either males that
mounted females but failed to impregnate them or males
that both mounted females and impregnated them (LSD
test: both P <0.05). Discussion
The results suggest a subset of 2F male Mongolian
gerbils that fail to respond to oestrous females and are
thus unable to reproduce; these males might be described
as ‘asexual’ in that they show no interest in females in
oestrus, fail to mount, intromit or ejaculate and are
effectively sterile. Such asexual males spend almost 50%
more time brooding young than do potentially fertile
males and are almost one-third more likely than are
sexually active males to stay in the nest with young when
a lactating female leaves her young and nest site. Mating behaviour
The mating behaviour of four of the 10 males that had
failed to impregnate females was severely compromised;
none of these males mounted any of the five females in
induced oestrus with which he was paired, and of course,
none achieved intromission or ejaculation (Table 1).
These four males also failed to show sexual interest in
females in oestrus. Although the males sniffed the ano- EXPERIMENT 2
To examine hormonal correlates of mating and parental
behaviours in 2F male gerbils, we determined the testosterone titres of a second sample of 14 2F males whose
reproductive performance and mating behaviour we had
measured following the same methods used to measure 803 804 ANIMAL BEHAVIOUR, 59, 4 Table 2. Reproduction and testosterone titres of 14 males in experiment 2
Mean number of mounts
Mean number of intromissions
Latency to first ejaculate (min)
T (ng/ml) Yes
1.52 (0.13) Yes
0.77 (0.12) T: Testosterone. Numbers in parentheses=1 SEM. parental behaviour of the 18 2F males participating in
experiment 1. Methods
Our subjects were: 14 Caesarean-delivered male Mongolian gerbils from 2F IUPs, each born to a different dam;
42 unmanipulated, sexually mature, vaginally delivered
virgin females; and 70 females brought into induced
oestrus with subcutaneous Silastic implants of oestradiol
Between 1400 and 1600 hours, 2 weeks after we had
finished evaluating each male’s reproductive success and
mating behaviour as in experiment 1, we anaesthetized
each male by intraperitoneal injection with sodium
pentobarbital (40 mg/kg) and collected a sample of blood
by cardiac puncture. Testosterone levels of serum samples
were then determined by radioimmunoassay (see Clark
et al. 1993 for details of the bioassay). Results
Reproductive and mating behaviour
Five of the 14 male subjects both failed to impregnate
any of the three females with which they were paired and
failed to mount any of the five females in induced oestrus
with which they interacted; one male failed to impregnate any female but mounted and mated with four of five
females in induced oestrus; and eight male subjects both
sired litters and mated with females in induced oestrus. Testosterone titres
Subject males that had failed to both mount females
and sire litters had testosterone titres significantly lower
than those males that had either sired litters, or mated
with females in induced oestrus but failed to sire litters
(Student’s t test: t11 =3.88, P< 0.03; Table 2). Indeed, the
testosterone titres of the four asexual males examined
were at the upper end of the range we have previously
observed in female Mongolian gerbils (Clark et al. 1991).
The results of experiments 1 and 2 indicate that, as a
sequela of prenatal development in IUPs between two
females, some male gerbils have circulating levels of testosterone in adulthood comparable to those seen in
adult females of their species. Such 2F males are essentially asexual; they failed to either mate or reproduce, and
such asexual males were significantly more responsive to
conspecific young than were sexually active male gerbils
that matured in 2F IUPs.
Integrating the present data with those reported in our
previous studies (Clark et al. 1997, 1998; Clark & Galef
1999) shows that there is great variation in the frequency
with which male gerbils engage in parental behaviour.
For example, in a situation comparable to that used in the
present experiment, 2M males spent an average SE of
57.8 3.6% of observation periods in contact with young
and 54.7 2.6% of the time their partner was away from
the nest with the pups, whereas 2F males did so on
70.2 2.8 and 67.8 3.7% of observation periods,
respectively (Clark et al. 1998). As in the present experiments, even within 2F males there is considerable variability in parental responsiveness; asexual 2F males have
unusually low testosterone titres and are significantly
more parental than are sexually active 2F males.
An interesting question, though one on which our
experiments cast no light, regards the selective pressures
that might have resulted in the evolution of asexual male
Mongolian gerbils. Given the current lack of evidence of
the distribution of asexual, highly parental males among
rodent species that occupy different ecological niches in
nature, speculation as to the evolutionary causes of asexuality in male gerbils would be entirely post hoc and,
therefore, not particularly compelling. It is, however,
relevant to note that those who breed laboratory rats and
mice find the occasional ‘dud’ male (Craig et al. 1959;
Whalen et al. 1961) that fails to mate with any of a
succession of females with which he is paired. We are not
aware of any assessment of the parental behaviour of such
sterile males, but their existence suggests that M. unguiculatus may not be the only rodent species with asexual
males that can enhance their fitness only by helping to
rear collateral kin.
For asexual males to enjoy reproductive success comparable to that of sexually active competitors, males’
probability of direct reproduction would have to be relatively low and their probability of increasing their inclusive fitness by helping to rear kin would have to be
relatively high. We know that: (1) gerbil dams can affect
the level of prenatal exposure to testosterone received by
their fetuses (Clark et al. 1991); (2) varying levels of
prenatal exposure to testosterone effects testosterone
titres in adulthood (Clark et al. 1992b); (3) adult circulating levels of testosterone effect the frequency with which CLARK & GALEF: WHY SOME MALES MAY HELP AT THE NEST males act parental. If having some asexual sons that care
for their dam’s or sisters’ offspring contributes more to a
dam’s fitness than having only sons that reproduce
directly, then selection might modulate the internal
milieu of gerbil dams to produce some sons that develop
as asexual, highly parental males.
In reviews of the literature on avian reproductive
behaviour, Ketterson & Nolan (1994) discuss correlational
evidence that testosterone increases sexual behaviour of
birds while depressing their parental effort (Wingfield
et al. 1990). For example, male pied kingfishers, Ceryle
rudis, that help at the nest have significantly lower testosterone titres than do breeding males (Reyer et al. 1986).
The present results suggest that in Mongolian gerbils, as
in birds, circulating levels of testosterone may mediate a
trade-off between sexual and parental behaviours (Clark
& Galef 1999).
The correlations between intrauterine exposure to testosterone, testosterone titres in adulthood (Clark et al.
1992b), mating behaviour (Clark et al. 1992a) and expression of parental behaviours (Clark et al. 1998) revealed in
the present and previous experiments suggest a relatively
straightforward hormonal basis for both development
and evolution of helping behaviour in male Mongolian
We thank Fred vom Saal for performing radioimmunoassays and Jenifer Vonk, Dorothy DeSousa, Paul Ramos
and Elaine Whiskin for technical assistance. This work
was supported by the Natural Sciences and Engineering
Research Council of Canada. The research presented here
was described in Animal Utilization Proposal Nos 98-1051, 97-11-55 and 96-11-88, approved on 1 December
1998, 6 January 1998 and 30 January 1997, respectively,
by the McMaster University Research Ethics Board.
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