Behavioral Ecology
doi:10.1093/beheco/arj012
Advance Access publication 23 November 2005
The large-male advantage in brown antechinuses:
female choice, male dominance, and delayed
male death
Diana O. Fisher and A. Cockburn
School of Botany and Zoology, Australian National University, Canberra ACT 0200, Australia
Male-biased dimorphism in body size is usually attributed to sexual selection acting on males, through either male competition or
female choice. Brown antechinuses (Antechinus stuartii) are sexually dimorphic in size, and heavier males are known to sire more
offspring in the wild. We investigated four possible mechanisms that might explain this large-male reproductive advantage. We
tested if there is a female preference for large males, a female preference for dominant males, if larger males compete more
effectively for mates, and if there is a survival advantage for large males during the mating season. We established nesting groups of
males in captivity and conducted mate choice trials in which males from nesting groups either could or could not interact. We
assessed male dominance rank and recorded survival times after mating. Females did not prefer larger males directly. The results
suggest that the other three mechanisms of sexual selection tested account for the large-male advantage: large males competed
more successfully for mates, so were socially dominant; females rejected subordinates (males they saw losing twice in contests to
previous mates); and dominant males survived for longer after their first mating. Females judged male rank based on direct observation of male competitive interactions at the time of mating and apparently could not distinguish rank from male scent. Effects
of size and dominance on male reproductive success are not confounded by age because male antechinuses are semelparous.
Key words: Dasyuridae, dominance, mate choice, sexual selection, sexual size dimorphism. [Behav Ecol 17:164–171 (2006)]
exual dimorphism in body size can evolve as a result of
natural selection (e.g., the sexes use different resources;
Selander, 1966) or sexual selection (one sex gains a greater or
a reduced reproductive advantage from large size; Andersson,
1994). Sexual selection in the form of males either fighting or
competing to be most attractive to females is traditionally seen
as the main cause of male-biased sexual size dimorphism. If
larger males produce more or competitively superior sperm,
postcopulatory sexual selection could cause male-biased sexual size dimorphism (Kraaijeveld-Smit et al., 2002b). A fecundity advantage in smaller females can also lead to male-biased
sexual size dimorphism, although this is rare (Lindenfors,
2002), and selection on size in one sex can drag the size of
the other sex in the same direction through genetic correlation, reducing sexual dimorphism (Lande and Arnold, 1985).
Evidence from recent comparative studies of fish, primates,
ungulates, macropods, birds in general, seals, reptiles, and
shorebirds supports the hypothesis that male-biased dimorphism is associated with sexual selection acting on males,
although much variation remains unexplained (Cox et al.,
2003; Dunn et al., 2001; Fisher and Owens, 2000; Lindenfors
and Tullberg, 1998; Lindenfors et al., 2002; Loison et al.,
1999; Pyron, 1996; Szekely et al., 2000).
In most mammals, body size is correlated with age. Contests
of strength between males often lead to stable dominance
hierarchies, in which the largest and oldest males in a group
have priority access to females (Fisher and Lara, 1999). However, younger males sometimes use tactics that avoid confrontation but still gain a high proportion of matings (e.g., in Soay
sheep and bighorn sheep; Isaac, 2005). In most species, it is
S
Address correspondence to D.O. Fisher. E-mail: diana.fisher@anu.
edu.au.
Received 24 September 2004; revised 4 October 2005; accepted 5
October 2005.
The Author 2005. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
difficult to separate the effects of size-based male competition,
age-based male competition, female choice of large males,
and female preference for older males. Females can often
choose males on the basis of dominance rank even if they
do not observe fights. For example, in many small mammals
with social systems governed by olfactory signaling, females
can tell the dominance rank of a male by other cues, such
as his scent or that of his urine, without direct observation of
contests (Hoffmeyer, 1982; Horne and Ylonen, 1996; Huck
and Banks, 1982; Rolland et al., 2003).
Brown antechinuses have male-biased sexual dimorphism
but no niche separation between the sexes (Lazenby-Cohen
and Cockburn, 1988). Males are likely to be the targets of
sexual selection; litter size is fixed by the number of teats
(eight), so there is no fecundity advantage in being a small
female. Antechinuses have an extremely unusual life history,
which precludes age-dependent mating tactics or female
choice of old males. All males die at 11 months of age, after
a single, brief mating season. Consequently, all males that
compete in the rut are the same age, providing a unique
opportunity to analyze dominance independently from the
confounding effects of age.
Microsatellite analysis of paternity has shown that larger
males and males with larger testes sire more offspring in the
wild (Holleley, 2003). In the agile antechinus, KraaijeveldSmit et al. (2002b, 2003) also found a greater share of paternity for larger males in the field, even though larger males
were not more likely to sire offspring in controlled laboratory
matings where two mates varied in size. The largest mate does
not sire more offspring in laboratory matings of brown antechinuses either (Fisher DO, unpublished data), so postcopulatory sexual selection cannot explain the large-male
advantage. Behavior in the wild might facilitate female choice
because males aggregate in nests that females visit during the
mating season (Lazenby-Cohen and Cockburn, 1988). Two
scenarios of male competition have also been proposed: either males fight for mates using contests of strength and the
Fisher and Cockburn • The large-male advantage in brown antechinuses
largest ones dominate or males that are able to grow largest
before the breeding season survive for longer and thus mate
more often (Braithwaite, 1979; Kraaijeveld-Smit et al., 2003;
Woollard, 1971).
In this study, we use mating trials in the laboratory to determine if the large-male reproductive advantage in brown
antechinuses is likely to result from female choice or male competition. We test four specific hypotheses: (1) females prefer to
mate with larger males, (2) females prefer to mate with more
dominant males (winners of contests), (3) larger males within
nesting groups are dominant, and (4) larger or more dominant
males survive longer after mating. We also explore the possibility that females can tell which males are dominant using
olfactory cues.
METHODS
Study animal
Radio tracking studies on the south coast of New South Wales,
where this study took place, have shown that brown and agile
antechinuses (Antechinus agilis) form mixed sex aggregations
in nests within tree hollows prior to and during the mating
season. Maximum aggregation size is 6–18, depending on the
study, and many nests contain fewer than five individuals
(Lazenby-Cohen, 1991; Lazenby-Cohen and Cockburn, 1988;
Lorch, 2004; McNee and Cockburn, 1992). Aggregation size is
fluid because males move frequently between nests, especially
late in the mating season (Lazenby-Cohen, 1991). Females visit
these aggregations for up to 19 consecutive hours (LazenbyCohen and Cockburn, 1988; McNee and Cockburn, 1992).
Mating in captivity takes 5–14 h (Shimmin et al., 2002).
Antechinuses use scent for intersexual communication;
they make several sex-specific chemicals in their glandular
secretions and urine, and both sexes possess specialized sensory systems to detect these (Toftegaard and Bradley, 2003).
Agile antechinuses have also been seen apparently following
scent trails in the wild during the mating season (LazenbyCohen, 1990).
Wild male antechinuses die as a result of escalating blood
corticosteroid concentrations causing immune collapse. Normal male social organization (communal nesting) seems to
facilitate this. Two studies have found that allowing social interactions between captive males during the breeding season
elevates stress hormones and accelerates death, even though
interactions involved chases and threats rather than overt
fighting (Scott, 1987; Wood, 1970).
Both the brown antechinus and the closely related agile
antechinus are polyandrous in the wild (Holleley, 2003;
Kraaijeveld-Smit et al., 2002a). Males are variable in size, despite being uniform in age (Kraaijeveld-Smit et al., 2003).
Male size is probably both genetically and environmentally
determined. Head length of agile antechinus fathers and
daughters raised in captivity are correlated, indicating a genetic component (sons could not be tested, Kraaijveld-Smit,
2001). An environmental component has been demonstrated
in dusky antechinuses (Antechinus swainsonii), as offspring of
fathers from populations of large individuals and small individuals are the same size when born in captivity (Cockburn A,
unpublished data). Endurance is expected to be important in
breeding males, because wild males forage in a much smaller
area during the mating season than before it, and males metabolize muscle during the mating period (Lazenby-Cohen
and Cockburn, 1988; Woollard, 1971). Some males also show
rapid weight gain just before breeding starts, followed by
weight loss during the mating period as energy reserves are
used (Kortner and Geiser, 1995).
165
Animal capture and maintenance
Thirty-five female and 34 male adult antechinuses were initially trapped at Kioloa, New South Wales, during late June
and July 2003. Elliott traps waterproofed with plastic bags were
placed in lines, 10 m apart, and lines were set 25 m apart. Trap
locations were permanently marked and numbered. Traps
contained Dacron fiber for bedding and were baited with
peanut butter and oats. We set traps before dusk for two
nights in a row in any one section of the sites and checked
them at dawn. Each captured animal was microchipped
(Trovan, Keysborough, Victoria, Australia, ID-100 transponder, 11 3 2.2 mm), dusted with insecticide powder to remove
ectoparasites (pestene), and wormed (Aristopet small animal
wormer [piperazine]). Antechinuses were maintained in singlesex groups of three in captivity (nesting groups) in 30-l plastic
containers (45 3 35 cm, 20 cm high, clear polyurethane) with
wire mesh lids and wood shavings on the floor. Each container
had a wooden nest-box (22 cm3 with a 3-cm-diam entrance
hole) containing shredded paper and a mouse running wheel.
Nest-boxes were similar in size to hollows containing antechinus nests in the wild (Cockburn A, unpublished data). A constant supply of water was provided in an inverted drip bottle.
Minced beef and kangaroo mixed with calcium powder, pentavite vitamin drops, and dog chow was given once a day and
frozen mouse pups and mealworms once a week. Animals
were kept at 18C during the day and 14C at night in a natural
light regime, with a child’s night-light (to prevent total darkness, which would otherwise occur in the windowless climatecontrolled room).
We checked the estrous status of females every day by looking for cornified epithelial cells in a drop of urine on a microscope slide, using 403magnification (Shimmin et al., 2000).
Females were mated beginning on the third day after cornified epithelial cells outnumbered other cell types (from 27
July). Females and males that mated multiple times were given
a day’s rest between each mating.
After mating, females were kept in individual containers to
give birth (for another study). Males were initially kept in the
same nesting groups as before. We checked which males had
died, once per day, and removed them. We attempted to keep
the remaining males at close-to-constant density by moving
them together into larger containers (40 3 65 cm, 35 cm
high, clear polyurethane) as their nest mates died. In case
of disagreements between individuals that had not previously
been nesting together, we provided several nest-boxes in the
larger containers, but we saw only minor, occasional threats
between males. All males in a container always nested together
in the same nest-box. After 66 days, males remaining alive
were released back into the wild.
Mating experiments
We used two types of choice trials. The first type (without male
interaction, n ¼ 14 females) was designed to test if females
prefer larger or more dominant males as mates when males do
not interact with each other, i.e., using visual or olfactory cues.
To be consistent with the conditions of the second type of
choice trial (see below), three males from one nesting group
(container) were offered. For each trial, the three males inside separate nest-boxes were first placed next to each other in
an arena (a clear polyurethane container of the same sort
used to house antechinuses, with wire mesh lid) between
0700 h and midday. Male nest-boxes were new wooden finch
boxes with a single 50-mm-diam entrance hole at the front. A
female in an open cloth bag was then placed at the other end
of the arena, about 10 cm from the front of the boxes. Males
almost always remained in their own nest-boxes: trials in which
a male emerged were discarded from the analysis. A small
Behavioral Ecology
166
surveillance camera was put on the mesh lid of each arena,
with a connection to time-lapse video recording equipment
and a split-screen monitor in the next room. Real time was
displayed on the video monitor and recorded. Once a female
entered a nest-box, we moved the camera to inside the nestbox, in order to monitor mating. The unsuccessful males were
returned to their container immediately.
The second type of choice trial (with male interaction) was
designed to test if direct competition advantages larger males
and if females assess male dominance interactions and reject
subordinate or smaller males as mates. Trials were filmed as
above. Dominance was defined as the outcome of competitive
interactions between males; the male with the highest priority
access to a resource (in this case a female) was designated the
most dominant (Dewsbury, 1982). We also tested for correlations between priority access to food and to mates and between priority access to food and male weight. We devised
two treatments that differed in terms of female opportunity
for direct assessment of dominance: ‘‘group’’ and ‘‘random.’’
(1) Group treatment (n ¼ 9 females). On the first mating day
we put a female with a group of three males from the same
nesting group (container). When a pair had been mating for
3–4 h, we checked the identity of the successful male by opening the nest-box and passing the microchip scanner over him,
making sure that the unsuccessful males were out of the way
(unsuccessful males were not removed from the arena during
the trial). This did not disrupt mating as pairs were in a mating
tie by then. The first male to mate was recorded as the dominant male in that container in terms of access to mates. On
the second mating day, we removed the previously successful
male from the container and offered only the two as yet unsuccessful males to the same female. On the third mating day,
we offered only the last remaining unsuccessful male from the
nesting group. (2) Random treatment (n ¼ 10 females). On
the first mating day, we presented the female with a group of
three males from the same nesting group (container), as in
the group treatment above. On the second mating day, we
offered two randomly selected males from a container different from that offered on the first mating day (i.e., the two
males were familiar with each other, but the female had never
seen them before). On the third mating day, we offered a single randomly selected male from a different container again
(i.e., the female had never seen him before). Under this regime, females from both treatments were offered a choice of
three, then a choice of two, and then a single male. Males in
the group and random treatments had virtually the same mean
weight and variance in weight (34 6 0.75 g versus 34 6 0.55 g).
Dominance and body weight
Males were weighed immediately before and after all mating
trials had been completed. We used the mean weight in analyses. We used priority access to mates as the main measure of
dominance in all tests. We also determined priority of access to
food between males in a nesting group, as an additional measure. After all mating trials had been completed, each of the
three males in a container were distinguished from each other
by dots of white correction fluid on one ear or neither ear. We
then recorded which male gained first and second access to
the food (in a single dish) at normal feeding times (1700 h)
for 5 days. The male that had first priority the most often was
scored as dominant in terms of food access in the container.
Data analysis
Videos of mating behavior in the mate choice trial ‘‘with male
interactions’’ were analyzed by scoring behaviors of the males
and female each minute for the first hour after the trial
began. We scored the following behaviors: female evasion of
mounting (running away or avoiding a position where the male
could achieve intromission), female walking (moving a short
distance inside the nest-box, while dragging the mounted male
along), rolling sideways and kicking males while mounted
(Shimmin et al., 2002), nonmating males making vocal threats,
and physical contact with the mounted male.
We used Spearman rank tests to find correlations between
male dominance ranks determined by mating priority and
body weight and paired t tests to determine if body weight
of males that mated and did not mate differed in mate choice
trials ‘‘without male interaction.’’ In mate choice trials without
male interaction, we used a chi-square test to find if the proportion of females that mated with the dominant male (as
assessed during the mate choice trials with male interaction)
was greater than expected at random. For the mate choice
trials involving nesting groups of males that could interact,
we used Fisher’s Exact test to find if the proportion of females
that rejected the last male offered differed between the group
and random treatments. Linear regression was used to find
associations between female activity and subordinate male attempts to disrupt mating by dominant males. Cox proportional
hazards regression was used to test if the time between first
mating and death varied according to social rank, weight rank,
or absolute weight in males. Statistical analyses were carried
out in Statview (Caldarola et al., 1999).
RESULTS
Effect of male body weight and dominance on female choice
in the absence of male interactions
Females did not choose mates on the basis of body weight.
There was no difference in body weight between males that
did or did not mate when they were presented to females
in the arena in separate nest-boxes (paired t test, t ¼ 0.80,
p ¼ .44, df ¼ 12). Females typically took between 1 and 5 min
to emerge and enter a male’s nest-box and then commenced
mating immediately. They did not overtly assess both males
visually. Females could not have been choosing mates by assessing rank via olfactory cues before they entered a nest-box;
they did not mate with the dominant male from the container
more often than by chance (v2¼ 0.33, p ¼ .96, df ¼ 1).
Mating behavior in nesting groups
When a female entered a nest-box containing three males
from the same nesting group, mating always ensued straight
away, with no obvious courtship or evasion of females by males
(Figures 1 and 2). The largest male almost always mounted
the female. In contrast to the minimal day-to-day aggression
between males in their containers, we saw prolonged confrontations when males interacted in the presence of estrous females. In the first hour of mating, generally one of the other
two males in the nest-box was aggressive toward the mating
male, and the other nonmating male retreated outside the
box. Occasionally, both unsuccessful males retreated without
further confrontation, or both attempted to dislodge the mating male from the female.
We saw two types of aggressive behavior toward the mating
male. The harassing male either raised his head and forepaws
and gave a vocal threat close to the mating male’s head without physical contact or grappled with the mating male using
his forepaws, sometimes attempting to kick him off. Often, a
nonmating male approached from behind, bit the mounted
male on the foot, and pulled. The mating male retaliated
with vocal threats and bites, usually without releasing his grip
on the female. On two occasions, attacks by subordinates
Fisher and Cockburn • The large-male advantage in brown antechinuses
167
Figure 1
Results of the female choice experiment with male interaction,
showing the proportion of matings accepted when the male was the
first, second, and third mate offered, in the group (n ¼ 9) versus the
random (n ¼ 10) treatment. Females rejected subordinate males
(males that lost twice) when they were able to see those males
competing.
dislodged the mating male, but in both cases, the original male
recommenced mating and not the subordinate.
Females reacted to these attacks by increasing their walking
activity within the nest-box (while still mounted) for several
minutes afterward. There was a strong correlation between
the number of physical contacts per hour to the mounted
male and female walking activity for both the group and random treatments (group: F1,24 ¼ 19, p ¼ .0002, r2 ¼ .44; random: F1,19 ¼ 23, p ¼ .0001, r 2 ¼ .54). There was also a strong
correlation between the number of vocal threats to the
mounted male and female walking activity for both treatments
(group: F1,24 ¼ 46, p , .0001, r2 ¼ .66; random: F1,19 ¼ 12,
p ¼ .003, r2 ¼ .38). Both types of aggression were intermittent,
with the nonmating male retreating between bouts. Eventually, the nonmating male usually retreated somewhere away
from the mating pair and slept.
Female choice and assessment of male dominance when
males could interact
The results of the female choice experiment with male interactions showed that females pay attention to male contests,
they later use the information to discriminate against subordinate males, and they are capable of rejecting unwanted
mates. Females in both the group and random treatments
always accepted the first mating when they were put in a container with three males from the same nesting group (Figure 1)
and did not evade male advances (Figure 2). One female in
the group treatment (in which the female was offered two
losers after mating with the overall winner in a container)
rejected the second mating. Many second-mating females in
the group treatment did not mate straight away but spent
12% of the first hour on average evading males (Figure 2).
No female in the random treatment (in which the female was
Figure 2
Female behavior during the first hour after females were put in the
mating arena, when the male was the first, second, and third mate
offered, in the group versus the random treatment. Evasion was
when females avoided being mounted by running away from the
male until he stopped approaching her. Resisting intromission was
when the female curled her hindquarters in a way that did not allow
the male to put his tail under hers and achieve intromission. This
was usually temporary. Rolling sideways did not result in any interruption to mating. Occasionally, a female that had been gripped
under the forearms by a male resisted intromission by rolling sideways and kicking him vigorously until the male let go. Females behaved most evasively in the presence of subordinate males (males
that lost twice) when they were able to see those males competing.
n ¼ 26 matings in the group treatment and 21 matings in the
random treatment. Error bars are standard errors.
Behavioral Ecology
168
offered two males she had not seen before, from a nesting
group different from that of her first mating) rejected the
second mating or evaded any males offered (Figures 1 and 2).
There was a striking difference in female behavior between
treatments during the third pairing. Only one female in the
group treatment out of nine accepted the third male offered,
compared to 9 out of 10 females in the random treatment.
The difference between treatments in the proportion of females accepting third matings was significant (Fisher’s Exact
test, p ¼ .0029). Females usually rejected matings by running
away and occasionally rolled over to kick off a male that managed to mount (Figure 2). Therefore, the proportion of time
spent evading males was much greater in the group than in the
random treatment for the third mating (Figure 2, F1,13 ¼ 6.4,
p ¼ .03).
Females rejected the last male offered only in the group
treatment, despite the fact that males were of similar sizes in
both treatments, and the last male to be chosen was smaller
on average than the first two males to mate in both treatments
(mean weight of first, second, and third males in the group
treatment: 35 6 1.1 g, 36 6 1.3 g, and 31 6 0.8 g; in the
random treatment: 35 6 0.7 g, 34 6 1.1 g, and 33 6 1.0 g).
This confirms the result from our female choice trials without
male interaction that females do not discriminate against
small males.
Effect of body weight on dominance and male
social relationships
Males cohabited in containers without obvious aggression and
huddled as a group in the nest-box during the day. Larger
males were more likely to be dominant in access to mates,
and there was a strong correlation between priority access to
food and mates and between priority access to food and male
weight (Figure 3, Spearman rank test for mating priority versus absolute weight, q ¼ 0.53, p ¼ .002; for mating priority
versus weight rank per nesting group, q ¼ 0.58, p ¼ .001; for
mating priority versus food priority, q ¼ 0.81, p , .0001; and
for food priority versus absolute weight, q ¼ 0.64, p ¼ .0002).
If more than one male emerged from the nest-box at once
when food was offered, there was usually vocalization by both
Figure 3
The effect of male body weight on dominance status (priority access
to a female for mating in a competitive situation within the nesting
group). Larger males obtained more matings. n ¼ 12 nesting
groups.
males at the food dish before one started eating but no physical contact. Subordinate males generally picked up food in
their mouths and retreated to a corner to eat.
Effect of male dominance and body weight on
postmating survival
Male dominance rank within nesting groups had a strong
effect on survival rate after mating (Figure 4). Dominant
males survived longer than second- or third-ranking males
(Wald v2¼ 10.3, p ¼ .006, df ¼ 2). Virtually, all subordinate
males were dead by 66 days after their first mating; two (17%)
of the second-ranked males and none of the third-ranked
males lived long enough to be released. Eight of the dominant
males (67%) survived. Neither body weight nor weight rank
within nesting groups had a significant effect on survival
(Wald v2 for weight covariate ¼ 0.4, p ¼ .53, df ¼ 1; Wald
v2 for weight rank ¼ 1.7, p ¼ .43, df ¼ 2).
DISCUSSION
Female choice
We found no direct preference for large males in female
brown antechinuses. These results agree with the findings of
Kraaijeveld-Smit et al. (2002b), who noted that female agile
antechinuses did not reject small males offered as mates after
large ones.
Females in our study discriminated between dominants
(they mated straight away), second-ranking males (females
with opportunity to judge that the male was ranked second
resisted for a short time but mated), and third-ranking subordinates (females with opportunity to judge that the male was
ranked last refused to mate with him). There was no evidence
of female choice on the first contact with a particular male.
When the female was introduced to a group of males, she
quickly mated with the first to mount (by definition, the dominant male). On later exposure to the unsuccessful (subordinate) males, she rejected them, even though the dominant
male was absent. Thus, female choice was involved in the
large-male reproductive advantage because smaller males
were more likely to be subordinates (Figure 3) and females
rejected them.
There are several potential selective advantages for female
animals that choose dominant mates (i.e., reject subordinates). Fighting ability can signal genetic quality to females
(Qvarnstrom and Forsgren, 1998). Dominance is usually related to size, and large sires may produce larger, fitter offspring (this is the case in at least one species of moth and
one lizard: Calsbeek and Sinervo, 2002; Iyengar and Eisner,
1999). There is some evidence that offspring size is also correlated with paternal size in agile antechinuses (KraaijeveldSmit, 2001), suggesting that dominant males would have
larger offspring.
Other potential advantages to females are that dominant
males better protect females from injury inflicted by rival
males and dominant males might be healthier and less likely
to transmit disease (Berglund et al., 1996; Qvarnstrom and
Forsgren, 1998). Both these benefits could apply to brown
antechinuses. Subordinate males seemed to be more aggressive; the only injuries to females during mating trials came
from last-mating, subordinate males biting them on the neck
when they attempted to end copulation. Dominant males gripped females under their forearms and rested their chin on
the female’s neck, rather than biting. Dominant males seemed
to be healthier because they survived longer (Figure 4).
Consistent with this, larger wild males in our study site had
fewer ectoparasites (Lorch, 2004). Dominant males might be
Fisher and Cockburn • The large-male advantage in brown antechinuses
169
healthier because of previous access to better resources as well
as genetic quality. In the subtropical antechinus (Antechinus
subtropicus), dominant males apparently occupy more productive microhabitats (Braithwaite, 1979).
A preference for high-ranking males is often associated with
female olfactory assessment of dominance status in small
mammals (Hoffmeyer, 1982; Horne and Ylonen, 1996; Huck
and Banks, 1982; Rolland et al., 2003). However, we found no
evidence that female brown antechinuses recognize dominant
males by scent, even though they prefer such males as mates.
Females were no more likely to enter the nest-box of isolated
dominant males than subordinate males to mate and did not
discriminate against subordinates offered in isolation after
matings in which males from different nesting groups competed (Figure 1).
Female brown antechinuses apparently relied solely on direct observation to identify male dominance status (Figure 1).
Once a female entered a nest-box containing interacting
males, the dominant male mounted her and then had to repel
subordinate rivals as they tried to displace him. Females had
plenty of opportunity to assess which males were dominant
during these intense and aggressive interactions in close proximity. A reason why females use direct observations rather
than scent could be the fluid nature of male mating aggregations in the wild (Lazenby-Cohen, 1991; Lazenby-Cohen and
Cockburn, 1988). As the composition of male nests changes
virtually daily and many males are in body contact in nests, it
may be impossible for males to accurately signal their dominance status relative to all other males in a nest using scent.
The reasons why females did not use body size as a cue for
dominance are unclear.
Females reacted to attacks on the mounted male by increasing their activity for several minutes afterward, and they were
more active in first matings, when there were more males in
the nest-box. There are two possible explanations for this. It
might be that females were disturbed or physically uncomfortable as a result of fighting between males, one of whom was
copulating with them. Alternatively, females might have been
testing the mounted male’s strength and ability to maintain
his grip. If he had failed to stay on, she might have accepted
the intruding male instead. Such tests of strength and encouragement of male contests are common mechanisms of female
choice in promiscuous vertebrates (e.g., Fisher and Lara,
1999; Lott, 1981; Pizzari, 2001). We saw only two cases where
a nonmating male managed to dislodge a mating male, and
in both cases the original male recommenced mating rather
than the intruder. This could be partly because antechinuses
develop a mating tie, which makes it difficult to separate them
(Shimmin et al., 2002). However, increased female activity
(e.g., walking and sideways rolling) is associated with the
end of mating sessions in agile antechinuses, indicating that
females have some control over the duration of copulation
(Shimmin et al., 2002).
Male competition
Figure 4
(a) Cox proportional hazards regressions showing survival times
of first-ranking (dominant in terms of mating priority), secondranking, and third-ranking males. After 66 days, the surviving males
(eight dominant and two second ranking) were released into the
wild. (b) Cox proportional hazards regressions showing survival
times of first-ranking, second-ranking, and third-ranking males in
terms of body weight within each container. The most dominant
males survived longest, but body weight alone did not influence
survival time.
We found male competition for mates in two forms in brown
antechinuses. First, large males have priority access to mates
(Figure 3). Dominant males are larger and were better able to
repel attacks from subordinates during copulation. This mechanism of sexual selection is traditionally associated with malebiased dimorphism (Darwin, 1871) and supported by many
recent comparative studies of other vertebrates (Cox et al.,
2003; Dunn et al., 2001; Fisher and Owens, 2000; Lindenfors
and Tullberg, 1998; Lindenfors et al., 2002; Loison et al., 1999;
Pyron, 1996; Szekely et al., 2000). Male size was directly related
to dominance, so mating success was not confounded by agespecific tactics or relationships between age and size.
170
Second, dominant males survive for longer after the first
mating (Figure 4). If this applies in the field, it is likely that
dominant males gain more mates by surviving in a relatively
healthy state for a greater part of the mating season. It has
been suggested that large male agile antechinuses might have
better survival during the mating season because their greater
energy reserves give resilience against starvation and cold
(Lazenby-Cohen and Cockburn, 1988; Woollard, 1971). However in our study, dominant males were larger and survived
longer, even though all males were well fed and not cold
stressed. Even low-intensity contact between male antechinuses during the breeding season increases the circulating
corticosteroids that lead to death (Scott, 1987; Wood, 1970).
Stress hormones seemed to have a more severe effect on subordinate males. In other social mammals with dominance hierachies but no cooperative breeding, subordinates usually
suffer greater corticosteroid levels than dominant individuals
(Creel, 2001). Our results suggest that large male antechinuses in the wild might survive longer because their social
dominance delays death and because they have better endurance to fasting and cold.
CONCLUSION
Our results show that precopulatory sexual selection can explain the large-male reproductive advantage in brown antechinuses, but the mechanisms are much more complex and
subtle than previously imagined. There is no direct female
preference for large males and no apparent assessment of
male rank based solely on olfactory cues by females. Three
types of sexual selection account for the large-male advantage:
large males compete more successfully for mates, so are socially dominant; females reject subordinates (but only if they
have the opportunity to assess male dominance rank directly
by observing contests); and dominant males survive for longer
after their first mating.
We are extremely grateful to Owen and Christina Carriage for their
hospitality and for allowing us to trap on their land. We also thank
Steve and Robin Berkhout for generous help at Kioloa Australian
National University field station. Thanks to Ben Moore, Jessica
Stapley, Dagmar Lorch, Simon Blomberg, Golo Maurer, Junko Kundo,
Thomas Polden, Anastasia Dalziell, Suzanne Morrison, Zak Pierce,
Christine Young, Michelle Shackleton, Grant Robinson, Bronwen
Jones, Tom Strang, Jacqui Devereux, Geoff Kay, and Ellie Sobey for
helping with fieldwork and/or antechinus handling in the laboratory.
The manuscript was greatly improved by comments from two anonymous reviewers. This study was supported by the Australian Research
Council.
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