Behavioral Ecology Vol. 13 No. 3: 408-418
© 2002 International Society for Behavioral Ecology
Reproductive skew, costs, and benefits of cooperative breeding in female wood mice (Apodemus sylvaticus)
Fakultät für Biologie, Postfach 5560, Universität Konstanz, D-78434 Konstanz, Germany
Address correspondence to G. Gerlach, who is now at the Marine Biological Laboratory, Woods Hole, MA 02543-1015, USA. E-mail: ggerlach{at}mbl.edu .
Received 14 July 2000; revised 5 March 2001; accepted 14 August 2001.
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ABSTRACT |
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Two current models seek to explain reproduction of subordinates in social groups: incentives given by dominants for peacefully remaining in the group (reproductive skew model) or incomplete control by dominants. These models make different predictions concerning genetic relatedness between individuals for the distribution of reproduction and the stability of cooperative breeding associations. To test these models and to further explore the relationships between reproductive skew, genetic relatedness, and investment of each participant, we performed behavioral observations of female wood mice (Apodemus sylvaticus) raising pups communally. Our results do not support previous models. Differences in lifetime reproductive success were significantly greater within mother—daughter pairs than within pairs of sisters or unrelated females. Subordinate females of either breeding unit did not differ in their direct reproduction. Calculations of inclusive fitness based on our results lead to the following predictions: (1) Communal nests should occur only when ecological circumstances prevent solitary breeding. (2) Subordinate females gain the highest inclusive fitness joining their mothers; they also show the highest nursing investment. (3) Mothers should accept daughters, who have no opportunity for solitary breeding. (4) Dominant sisters and unrelated females should reject subordinate females because cooperative breeding reduces their reproductive success. However, breeding units of dominant sisters and unrelated females nevertheless occur and can be explained by our finding that such females significantly reduce nursing time, which may help them save energy for future breeding cycles. Our data demonstrate that both genetic relatedness and investment skew are important in the complex evolution of reproductive skew in cooperative breeding.
Key words: Apodemus sylvaticus, cooperative breeding, reproductive skew, wood mice.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Communal breeding involves several contradictory driving forces of a genetic, behavioral, and ecological nature. Social groups in which a single breeder monopolizes reproduction are described as having high reproductive skew, whereas low-skew groups are those in which reproduction is distributed more equally over some or all group members (Vehrencamp, 1983
). Several
recent studies have attempted to understand what drives this reproductive skew
(Bernasconi et al., 1997;
Cant, 2000;
Creel and Waser, 1997;
Komdeur, 1996). The results
have led to two different models. The (classical) skew model is based on the
assumption that reproductive sharing within social groups is the result of
reproductive incentives given by dominants to subordinates to keep them as
peaceful helpers in the group (Keller and
Reeve, 1994; Reeve and Keller,
1995; Reeve et al.,
1998; Vehrencamp,
1983). Most examples fitting this hypothesis have been found in
ants and other social insects (see Keller,
1991). An alternative model is based on the assumption that
reproduction by subordinates is the result of incomplete control by dominants
(Clutton-Brock, 1998;
Reeve et al., 1998). This may
be the case in the naked mole rat (Heterocephalus glaber), where
dominant females are sometimes unable to suppress the reproductive activity of
subordinates (Jarvis,
1991).
These two skew models make different predictions about the role of
relatedness between dominants and subordinates and about the regulation of the
subordinate's share of reproduction. The optimal skew model predicts that the
subordinate's reproduction is inversely proportional to its relatedness to the
dominant. Assuming that dominants are benefiting from the presence of
subordinates, they should try to keep subordinates as helpers in the group. It
follows that dominants should allow less related individuals to raise more of
their own offspring as an inducement to remain in the cooperative group,
whereas more related individuals might stay with less of their own
reproduction because they can increase their inclusive fitness by helping
relatives raise their offspring
(Vehrencamp, 1983). The
decision of subordinates to stay rather than to leave to breed
alone—that is, the assessment of dispersal risk—is based on
ecological factors such as food and nesting availability. The optimal skew
model further predicts that reproductive skew is great in breeding units with
asymmetrical relatedness such as in matrifilial associations (the daughter is
more related to the offspring of her mother than vice versa) and that
reproductive skew is small in units composed of individuals of the same
generation in which relatedness to offspring is symmetrical
(Keller and Reeve, 1994;
Reeve and Keller, 1995).
Assessing the degree of relatedness among communally breeding females is
complicated when females mate with different males during one estrous period;
this results in a decrease of relatedness among offspring and affects an
important component of the model (Reeve
and Keller, 1996). Increased frequency of multiple matings will
tend to decrease reproductive skew in both matrifilial and sibling
associations, but such that skews in the former still exceed skews in the
latter (Reeve and Keller,
1996).
The incomplete control hypothesis predicts just the opposite effect: when
relatedness is symmetrical among group members, reproductive skew should
decrease with, or be insensitive to, increasing genetic relatedness among them
because dominants should prefer to tolerate reproduction in more related
individuals (Cant, 1998;
Clutton-Brock, 1998;
Reeve et al., 1998). The
occurrence of subordinate reproduction in asymmetrical parent—offspring
associations is more consistent with the optimal skew than with the incomplete
control model where the subordinate is predicted to obtain no direct
reproduction (Reeve et al.,
1998).
Neither model predicts high levels of aggressive testing by subordinates
and assertion of status by dominants, but the optimal skew model predicts
higher aggression for parent—offspring associations than the incomplete
control model (Reeve and Ratnieks,
1993; Reeve et al.,
1998; see also review on queen—queen interaction in social
insects by Heinze, 1993; but
see also Cant and Johnstone,
2000). According to the incomplete control model both the dominant
and the subordinate will exert decreasing aggression effort to enhance their
shares of group reproduction as their relatedness increases. At all values of
relatedness the subordinate's aggressive effort will exceed that of the
dominant. This will increase the payoff for the subordinate's aggressive
testing of dominants.
The two models do not make clear predictions about division of work and
investment. Evidence from Polistes wasps suggests that foundress
associations in species with high reproductive skew have a more sharply
defined caste system than associations with low skew
(Heinze, 1993;
Reeve and Ratnieks, 1993). It
is not clear whether this varies with genetic relatedness between females.
According to the incomplete control model, dominants might tolerate less
investment of related subordinates better than of unrelated. One of the best
known examples in vertebrates is the cooperative breeding system of the pied
kingfisher, where less related secondary helpers invest less in feeding
hatchlings (Reyer, 1984).
To test which model best explains the relationships between reproductive
skew, genetic relatedness (symmetrical and asymmetrical), and investment of
effort, we performed behavioral observations on female wood mice (Apodemus
sylvaticus). Wood mice are an excellent model organism due to their
variable sociality. In addition to nests of solitary mothers, communal nests
of two reproductive females pooling their offspring were frequently observed
in a large outdoor enclosure (Musolf and Gerlach, in preparation) and
telemetry studies revealed communal use of nest sites of reproductive females
under natural conditions (Wilson and
Montgomery, 1992). Concurrent studies of the genetic structure of
wild-living wood mice show that strict family groups of related adult animals
living together within one territory do not exist and that the probability of
a female encountering related as well as unrelated individuals is high
(Gerlach, in preparation). Therefore, related and unrelated females might be
chosen as cooperative partners when raising offspring together. This provides
an important and interesting difference with previous studies on cooperative
behavior in species such as house mice
(König, 1994a) that live
in strict family units where access and choice of unrelated females is less
probable. A high degree of multiple mating of female wood mice was found under
natural conditions (Baker et al.,
1999) and in an enclosure experiment
(Bartmann and Gerlach, 2001),
indicating a promiscuous mating system in wood mice. In enclosure experiments
in which four females were living together with four males, the fraction of
daughters to share the same father within one litter was 0.44, and,
considering consecutive litters, only 20% of all daughters born by one mother
shared the same father (Bartmann and
Gerlach, 2001). Taking these multiple matings into account, the
relatedness of daughters to the offspring of their mothers ranges between 0.25
and 0.5, and the relatedness of a female to the offspring of her daughter
always equals 0.25. This causes an asymmetrical relatedness between
mother—grandchild and daughter—sib/half-sib.
In this study of reproductive skew and cooperative breeding in wood mice, we wanted to test the impact of relatedness on reproductive success, nursing investment, infanticide, and aggressive interactions between females raising offspring together. We included for comparison the reproductive success of solitarily breeding females. To quantify all parameters, we conducted a laboratory study where relatedness and dispersal could be controlled and where behavioral interactions could be observed. As it is likely that in nature ecological constraints determine the probability of dispersal and thus reproduction outside the familiar group, we prevented dispersal to enhance the effects on reproductive skew.
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MATERIALS AND METHODS |
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Experimental design
Experimental animals were the first and second filial generations of wood mice trapped from different places near Konstanz, southern Germany. All animals were kept at 20°C on a 10:14 h light:dark cycle (light on at 1000 h). Food and water were available ad libitum. At 4 weeks of age, experimental animals were separated from their parents and kept in groups of the same sex, with the exception of animals destined for mother—daughter (MD) breeding units. In that case, when a daughter was 4 weeks old, her father and littermates were removed and she was kept together with her mother for the next 4 weeks. The father had been separated before the mother gave birth to ensure that she was not becoming pregnant again. Other females were assigned to one of three additional experimental groups: one female alone (M), a breeding unit of two sisters of the same age who were never separated from each other (S), or a breeding unit of two unrelated, unfamiliar females of the same age (F).
At the beginning of each experiment, only mothers of experimental group MD were 16 weeks old and had given birth to one litter; all other females were 8 weeks old and sexually inexperienced. Both females of a breeding unit were marked individually by shaving fur in different places. One male (8-10 weeks old) who was unfamiliar and unrelated to the females was added to each of the experimental groups. In case of the MD associations, this was not the father of the daughter.
Experimental setup for groups MD, S, and F consisted of three cages in a line (each 42 x 26 x 15 cm) and two nest-boxes (each 15 x 15 x 15 cm) linked to either cage 1 or 3 by a tube; those for experimental group M consisted of two cages and one nest-box. Each experimental group was kept for 120 days, which is considered to equal the life span of wood mice under natural conditions (Gerlach, in preparation) and was checked daily for litters. We measured body weight of the young on the day after birth (corresponding to day 1 of lactation) and on day 28, when they were weaned and removed from the experimental group. Several times per week we conducted behavioral observations for 30 min, equally divided between day and night. Two activities of the females were recorded and analyzed: time spent nursing and number of aggressive interactions. We analyzed 595 observation periods; sample size for each breeding unit was M: n = 11, MD: n = 10, S: n = 10, and F: n = 9.
Data analysis
To compare differences in reproductive success (number of offspring and
litters and body weight of offspring) among the experimental groups, we used
ANOVA procedures of the program JMP (SAS
Institute, 1995) with further contrast analysis.
Both females of a breeding unit were suckling not only their own offspring,
but also the offspring of the other female. When evaluating whether the two
females invested different amounts of time in nursing, the age of her own and
the age of the other female's offspring had to be taken into account because
offspring of the two females within a breeding unit were of different age.
Thus, we calculated nursing times of dominant and subordinate females
separately and evaluated nursing times according to the age categories of a
female's pups. To examine the factors influencing the time a female spent
nursing, we used an ANOVA, Procedure Mixed
(SAS Institute, 1992) for
mixed linear models (models with both fixed and random effects). In the test
design, each female was considered a random effect to account for the repeated
measurement design. We started the analysis with a comprehensive model of
potentially relevant factors, preferring those models with a minimum
Schwartz's Bayesian criterion in the model-fitting information. Schwartz's
Bayesian criterion is a sensitive indicator of the goodness of fit that
compensates for the tendency of many goodness of fit indicators to increase
with an increasing number of factors.
When calculating direct and indirect reproductive success, we estimated the relatedness, r, of a mother to her own pups as r = 0.5; the relatedness of a mother to the offspring of her daughter as r = 0.25; a daughter to the offspring of her mother, due to different paternity in our experimental design, as r = 0.25; two sisters to each other's offspring as r = 0.25; and r = 0 for unrelated females to each other's pups.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Reproductive success
Females always put their young together in one nest and nursed them communally. But because their litters were of different age, it was easy to recognize to which mother the pups belonged. The reproductive success of a female was defined as the number of young reaching the age of 17 days within the experimental period of 120 days. (At 17 days, pups begin to eat solid food and are assumed to be capable of surviving on their own.) Figure 1 shows the number of offspring born and weaned in the four experimental groups. There were significant differences between experimental groups in number of offspring born (F = 9.29, df = 3, p =.0001) and weaned (F = 2.95, df = 3, p =.0455). On average, one mother alone (M) gave birth to 17.9 (± 1.5 SE) offspring and weaned 16.2 (± 1.3), whereas cooperatively breeding females gave birth to and weaned more joint offspring per breeding unit than solitary mothers (MD: born, 31.2 ± 1.9, weaned, 24.7 ± 2.1; S: born, 24.5 ± 1.9, weaned, 20.3 ± 2.0 SE; F: born, 28.5 ± 2.0, weaned, 20.6 ± 2.4; Figure 1). There was no statistical difference between the three breeding units in the number of pups born (F = 1.95, df = 2, p = 0.59) or weaned (F = 1.67, df = 2, p =.10).
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However, within a breeding unit, one of the two females always weaned far more offspring than the other (on average twice, see Table 1 and Figure 1). We defined the female with the larger number of offspring as the dominant and the other as the subordinate female (e.g., MDdom, MDsub, etc.). To analyze whether variances in number of young produced were higher in breeding units of cooperating females than in females raising offspring solitarily, we randomly distributed solitary mothers into two groups. Differences in number of offspring between these two groups of solitary mothers were significantly smaller than between dominant and subordinate females of the breeding units (young born: t = 2.11, p =.043; young weaned: t = 2.92, p =.007). Therefore, we concluded that differences in reproductive success between subordinate and dominant females cannot be explained by normal variance between females.
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Considering solitary mothers and dominant females in all breeding units, there was no difference in the number of offspring born, but both solitary mothers and MDdom weaned more offspring than Sdom or Fdom (Table 1). Considering solitary mothers and subordinate females, solitary mothers gave birth to more pups and weaned more pups than any of the subordinate females (Table 1). We did not compare number of offspring of dominants and subordinates because they were different by definition.
Reproductive skew
Differences between the number of offspring weaned by dominant and
subordinate females (reproductive skew) were significantly greater in MD
breeding units than in either of the other units (MD versus S, F breeding
units: t= 2.15, p =.038;
Figure 2). On average,
MDsub weaned 7.9 (± 1.4 SE) fewer pups than
MDdom, and Ssub had 4.9 (± 1.4) and
Fsub 4.8 (± 1.4) pups less than their dominant counterpart.
Therefore, we conclude that reproductive skew was greater within asymmetrical
breeding units than in symmetrical units, but no difference was evident
between breeding units consisting of sisters and unrelated females.
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Total reproductive success
Broadly generalized, Hamilton's concept of inclusive fitness (Hamilton,
1964a,b)
predicts that the evolution of cooperation is favored over solitary breeding
if r x b - c > 0, where r is the
coefficient of genetic relatedness between these individuals, b is
the benefit of cooperation in terms of additional reproduction, and c
is the cost in terms of a loss of reproduction
(Grafen, 1984). We calculated
inclusive fitness values for each female of a breeding unit according to this
formula to evaluate whether subordinate females of either breeding unit should
join the nest and whether dominant females should accept subordinate females
in the nest (Table 2). It
turned out that subordinate females should never join a nest when they have
the chance to breed solitarily. But they should always join a nest, even with
a nonrelated female, when they have no chance of finding a nest site for their
own. Only MDdom should accept a daughter in their nest when the
daughter had no chances to breed solitarily. According to this calculation,
neither Fdom nor Sdom should accept subordinate females
in their nest because the cost—benefit relation for Sdom
(-1.6) and for Fdom (-8.3) is > 0.
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Parameters determining reproductive success
Number of litters produced
Solitary females and MDdom had more litters than the dominant
females of the other two experimental groups
(Table 1). MDdom
produced more litters than MDsub. No difference in number of
litters was found between dominants and subordinates in any of the other
breeding units (Table 1). Thus,
the MDdom mother appears to have a special reproductive advantage
in producing litters.
Number of offspring per litter
Solitary mothers gave birth to an average of 5.6 pups per litter
(Table 1), similar to dominant
females of all breeding units, whereas subordinate females delivered
significantly fewer pups. In the MD and S (but not F) breeding units, dominant
females had a significantly larger number of pups per litter than subordinate
females. It could be argued that dominant females of the MD unit had more
offspring because they were older and more experienced at the beginning of the
experiment; they had already given birth to a litter. However, in solitarily
breeding mothers, litter size did not change with increasing number of litters
(ANOVA, F = 0.089, df = 3, p =.96), and there was also no
difference between the first and second litter (t = 0.62, p
=.54).
Interbirth intervals
On average, a solitary female gave birth to her first litter 31.9 days
(± 4.1 SE) after her first encounter with the male
(Table 3). Solitary and
dominant females in the different breeding units did not differ in the time
span until the first litter was born. However, dominant females gave birth to
their first litter significantly faster than subordinate females.
MDsub had the longest interval until she gave birth to her first
litter: 45 days (Table 3), but
differences among breeding units for subordinate females were not
statistically significant due to high variance.
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We suspected that communal nursing would decrease the time intervals between litters because mothers might save energy by not nursing the pups alone. Therefore, interbirth intervals were analyzed (ANOVA) using experimental group and individual female nested in experimental group (as a random factor) as independent variables. No difference was evident in interbirth intervals between solitary mothers and dominant females or between solitary mothers and subordinate females. Subordinate females had longer interbirth intervals than dominant females, but due to Bonferroni corrections the difference was no longer significant (Table 3).
Body weight of offspring
Body weight of weaned offspring did not differ significantly among the
experimental groups. Additionally, pups of subordinate females weighed as much
as pups of the dominant or solitary mothers
(Table 1).
Aggressive interactions
Aggressive interactions between females were rare. On average, females had
0.2 (± 0.06 SE) fights per observation period with other females, and
they were more aggressive against the male (0.72 ± 0.07). Agonistic
encounters were highest in F breeding units (0.3 ± 0.08), lower in S
(0.15 ± 0.09), and lowest in MD (0.09 ± 0.13); the differences
were not statistically significant due to high variance in the data. Dominant
females tended to be more aggressive against subordinate females than vice
versa (t = 1.87, p =.059). There was a trend that
Fdom were more aggressive against subordinates than
MDdom and Sdom (t = 1.753, p =.09),
while subordinates of all breeding units should equal aggressiveness against
dominants. In breeding units where dominant females were aggressive against
subordinates, the reproductive success of the subordinate partner was
significantly lower than when no aggression was observed (Fisher's Exact test,
2 = 17.901, p =.0002). Thus, overt aggression, rare
as it appears, seems to be involved in maintaining (and perhaps determining)
dominance.
Infanticidal behavior
To further evaluate how females in breeding units control each other's
reproduction, we analyzed the amount of infanticide in the experimental groups
(Table 1). On average, a
solitary mother weaned 1.7 offspring fewer than she gave birth to within the
experimental time period of 120 days. The difference in number of offspring
born and weaned was not statistically different among experimental groups or
between females of the same breeding unit
(Table 1). On average, 4
(± 0.7 SE) pups of dominant females and 2.5 (± 0.7) pups of the
subordinate did not survive until weaning. Deaths of pups of one female
occurred shortly before the other female gave birth to her next litter and
when her previous litter was already weaned. This would be a good strategy to
avoid killing one's own pups by mistake.
Comparison of nursing time between solitary and communally breeding
females
Solitary mothers spent similar amounts of time nursing (47%) as
MDdom (52%; Figure
3a), which was significantly more than either Sdom
(29%; Figure 3b) or
Fdom (32%; Figure
3c). Although no longer statistically significant after Bonferroni
corrections, MDsub spent more time suckling (57%) than solitary
mothers; whereas Ssub (26%) and Fsub (29%) spent
statistically significant far less time suckling than solitary mothers
(47%).
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The time a female spends nursing depends on the age of her offspring. For reference we used again solitary mothers, who spent about 63% of their time nursing until the pups were 19 days old; this time decreased significantly to 31% when the pups were 20-24 days old and to 20% when they were 25-28 days old. The number of offspring per litter had no influence on the nursing time of solitary mothers (ANOVA Procedure Mixed, F1,158 = 1.28, p =.25). We investigated whether nursing time of communally breeding females depends on the nursing effort of the female counterpart and how females allocate their nursing efforts when pups of different age (and thus parentage) were present. For this we calculated separately the nursing times of dominant and subordinate females according to the age categories of their own pups.
Nursing efforts of dominant females
In a first analysis the time a dominant female was nursing was used as the
dependent variable and the category age of own young as an independent
variable. Further independent variables were experimental group, time the
subordinate female spent nursing young, age difference between pups of the
dominant and subordinate female, and the interaction of experimental
group*age difference between pups of the dominant and subordinate
female (Table 4). The age of
their own pups had a significant effect on the mother's nursing time: with
increasing pup age, dominant females spent less time suckling them. Nursing
time of the subordinate female had no influence on nursing time of the
dominant. The experimental group had a significant effect: the MD breeding
unit spent more time nursing than the S or F unit. With increasing age
difference between her own pups and the pups of the subordinate female, the
dominant female spent less time suckling than solitary females. Otherwise the
results seem to indicate that nursing is a physiological process decreasing
with pup age and unaffected by other pups and other nursing efforts
(Table 4), indicating that
during times when offspring of the subordinate female were smaller and needed
more milk, the dominant female reduced her nursing time.
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Nursing effort of subordinate females
The same analysis was performed using time a subordinate female was nursing
as the dependent variable. Subordinate females also decreased their nursing
time with increasing age of their pups and were not influenced by the nursing
efforts of the other female (Table
4). But, in contrast to dominant females, differences between the
age of her own and the pups of the dominant mother had no significant effect.
A significant difference appeared in the interaction of experimental
group*age difference, indicating an increase of breeding effort in
the MD unit compared to S and F units. MDsub increased their
breeding effort by 4.2% per category of age difference. Thus, when younger
pups of the dominant female were present, MDsub spent more time
nursing than she would have done according to the age of her own pups.
The worst situation for communally breeding females was that in nine cases the whole litter of a subordinate female was killed. In six of those cases, the subordinate female stopped nursing completely, although there were pups of the dominant female present. This shows that begging behavior of pups is not the only stimulus that induces females to nurse; mothers also noticed whether their own pups were present or not. On average, such females decreased their breeding effort by 94%.
Investment in relation to the number of own and foreign pups
To compare breeding effort of each female according to the number of own
and foreign pups, we divided mean values of time spent nursing
(Figure 3) by the number of
pups of the communal nests, taking into account their genetic relatedness to
the offspring of the other female. We added the number of a female's own pups
(multiplied by r = 0.5) and the number of pups of the other female
(multiplied by the relatedness between either female and the pups). No
differences could any longer be revealed among females, with the exception
that Fsub showed the highest effort in relation to her reproductive
success. The Fsub spent significantly more time nursing pups in
relation to the number of own pups than Fdom. We concluded that the
revealed highest absolute breeding effort of MDsub was balanced by
a high number of related pups, even when we considered that the daughter was
only r = 0.25 related to the pups of her mother.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Two main results have emerged from this study: (1) a striking relationship between differences in investment and reproductive success among cooperatively breeding females that vary in relatedness and (2) convincing evidence for litter discrimination in communal nests, which is not affecting nursing investment. We discuss these results below in light of previous theories on reproductive skew.
Evolution of cooperative breeding units
According to our calculations of inclusive fitness, communal nests of
females raising pups together should not occur when ecological circumstances
permit solitary breeding. The costs for subordinate females joining a nest
always exceeded the benefits, regardless of their relatedness to the dominant
female (Table 2). In contrast,
when solitary breeding is impossible—as might be the case when
population density is high and appropriate nest sites are
limited—subordinate females should always join nests
(Table 2). They would gain the
highest inclusive fitness joining their mother. Our calculations show that the
mother (MDdom) should accept a daughter, who has no opportunity for
solitary breeding, whereas Sdom and particularly Fdom
should always reject subordinate females
(Table 2). Yet, this is not the
case. Here, nursing investment adds an interesting new twist to the story.
Our results on differences in nursing investment strongly emphasize the importance of maternal investment and degree of relatedness when trying to understand the occurrence of breeding associations. In comparison to solitary mothers, Sdom and Fdom reduced their nursing effort by 38% and 32%. Also Ssub and Fsub invested significantly less time nursing pups than solitary mothers. This result may explain why communal nests founded by sisters and unrelated females can still be advantageous despite a decrease in reproductive success compared to solitary breeding. By spending significantly less time nursing offspring than solitary mothers, both partners in the symmetrical relationships Sdom, Ssub and Fdom, Fsub save energy for future reproductive effort while still having moderate reproductive success. Comparing nursing time and total (direct and indirect) reproduction in S and F breeding units, we showed that Sdom and Ssub invested equally, whereas Fsub invested significantly more time nursing than Fdom relative to their total reproduction. Therefore, a subordinate female has the greatest disadvantage when breeding cooperatively with an unrelated dominant female. MDdom spent the same time nursing as solitary mothers, indicating again that she has no additional costs but also no measurable direct benefits. Subordinate females of the MD breeding units nursed more than solitary mothers, but the extraordinary effort by subordinate daughters breeding with their mothers pays off in gaining the greatest increase of inclusive fitness.
Time spent nursing as an investment in pups
Investment of effort can take several forms. Besides direct nursing, time
spent with offspring is likely to enhance nest temperature and protection of
young. This could result in costs such as females having less time for
activities such as foraging. Perhaps the more important question that arises
is to what degree our behavioral measure "time spent nursing" is
correlated with energetic expenditure. Although we cannot prove this point
directly because we did not quantify milk transfer, we offer the following
indirect evidence. In house mice, the amount of milk produced depends on the
suckling stimulus of young (Hall and
Williams, 1983) and increases with increasing litter size
(König et al., 1988).
Milk ejections are produced in the mother by pulsatile release of oxytocin
from the pituitary, which is in turn stimulated by suckling
(Wakerley and Lincoln, 1971).
Therefore, we assume that MDsub not only nursed longer but as a
result also gave more milk than any of the other females: nursing periods were
longer and more frequent, resulting in stronger suckling stimulation by pups.
In addition, we can speculate that the longer time span needed to produce the
next litter is indirect evidence for higher energetic investment of
MDsub because her longer lactation period delayed the next
reproductive cycle. Fuchs
(1981,
1982) showed this relationship
in house mice. The fact that longer nursing periods in the MD units did not
result in greater body weight of offspring than in other experimental groups
was probably the result of the greater number of pups in the MD nests. Our
results concerning body weight of offspring are different from previous
studies. House mice (Sayler and Salmon,
1969) showed greater pup weight in communal nests. Greatest body
weight of weaned offspring was found in females living with a sister compared
to monogamous females or to females communally nursing with an unrelated
partner (König,
1993).
Discrimination between own and foreign offspring
The second result from our study provides convincing evidence for litter
discrimination in communal nests. In our experiments, a mother's nursing time
was strongly related to the age of her own pups but not to the age of foreign
pups. This was seen clearly where dominant females of all breeding units spent
significantly less time suckling young when the offspring of the subordinate
females needed more milk than their own. Only subordinate females of the MD
breeding unit broke this rule and increased their nursing time when the
offspring of dominant females were younger and needed more milk than their own
litter. We interpret this higher investment as a result of the daughters'
greater relatedness to the offspring of the mother. All these results
demonstrate the ability of female wood mice to discriminate between pups of
mothers, sisters, and unrelated females. In addition, in cases where the whole
litter of a subordinate female was killed, she reduced her nursing time by 94%
regardless of the presence of other pups, indicating recognition of her own
litter. Thus, our experiments show that nursing is not simply a response
caused by the presence of unweaned pups. This ability of pup discrimination
appears not to be used in preferential suckling in mixed nests (e.g., by
removing foreign pups from their nipples). Coincidentally, as in the present
study on well-fed wood mice, female house mice under restricted feeding
conditions killed the same number of their own and foreign pups
(König, 1989).
Cooperative breeding units of wood mice in regard to reproductive
skew theories
Our data demonstrate an unequal distribution of reproduction between
cooperating females with a higher reproductive skew in asymmetrical MD than in
symmetrical S and F breeding units. This higher skew was not caused by a
smaller number of pups by MDsub but by a higher number of pups
produced and weaned by MDdom in comparison to breeding units of
dominant sisters and unrelated females. Indeed, number of pups did not differ
between subordinate females of either breeding unit. Therefore, neither
different incentives (Vehrencamp,
1983) nor different tolerance levels of the dominant female toward
subordinates (Clutton-Brock,
1998; Reeve et al.,
1998) differed according to genetic relatedness. Direct
reproductive success of all three categories of subordinates was reduced
equally, both by longer time intervals until and between litters and by a
smaller number of offspring born per litter. Therefore, neither of the two
models fit these data. Although there was a striking difference in
reproductive success between asymmetrical and symmetrical associations, we
found almost no difference between the two symmetrical associations
considering direct reproductive success. This result contradicts the
reproductive skew model, which predicts higher reproductive incentives for
unrelated females than for sisters
(Vehrencamp, 1983). And
considering total reproductive success, Fsub was even significantly
less successful and had a greater breeding effort in relation to total
reproduction than Ssub. Our results differ from results obtained on
communal nursing in house mice, where communally nursing sisters had higher
direct lifetime reproductive success than unrelated or solitarily breeding
females (König, 1994a).
In house mice, reproductive success was equally divided between cooperating
sisters (König, 1994b).
These differences may reflect the different social systems of house mice and
wood mice (Bartmann and Gerlach,
2001). Multiple and promiscuous matings of female wood mice within
one estrous period are common. Therefore, under natural conditions most of the
sisters within one litter are only maternal half-sibs, and the probability is
quite high that unfamiliar females are also half-sibs (paternal) because the
same males have also mated with their mothers. This might decrease behavioral
and reproductive differences between these breeding units.
Neither of the two models we considered originally makes clear predictions
about division of work and investment. The optimal skew model predicts that
subordinates should be most likely to engage in risky or energetically costly
tasks (Reeve and Ratnieks,
1993) but does not clearly specify whether this should be affected
by genetic relatedness. The overall results of this study do not fit the
predictions of either model in a satisfying way. Perhaps reproductive skew
models have been developed mainly for social insects, and their application to
mammals is difficult. In addition, the existing models do not sufficiently
consider the role of differential investment in raising offspring.
The predicted effect of relatedness on dominance interactions is complex.
At least, when it does not significantly reduce group productivity, optimal
skew models predict that the greater the reproductive skew (with increased
relatedness), the greater will be the subordinate's payoff for
"testing" dominant queens
(Reeve and Ratnieks, 1993).
Thus, the intensity and frequency of dominance interactions should increase
with increasing reproductive skew and increasing relatedness (but see also
Cant and Johnstone, 2000).
In our study, aggressive encounters were highest in associations of
unrelated females, but this was not statistically significant. Dominant
females, defined in our study as those with the greatest reproductive fitness,
tended to be more aggressive than subordinate females, which might indicate
that agonistic encounters were more likely dominant aggression to control
subordinates than subordinates challenging the dominant's fighting abilities.
Subordinates of all breeding units did not differ in their aggressiveness
against dominants, but there was a trend that Fdom were more
aggressive than MDdom and Sdom. In addition, higher
aggressiveness of dominant females was correlated with decreasing reproduction
of subordinates. This further supports the conclusion that this aggression may
be a mechanism to suppress subordinates. In several ant species, dominant
cofoundresses also grow intolerant of each other after emergence of the first
workers when the time of benefiting from a subordinate cofoundress is past
(see Heinze, 1993). Long-term
studies of naked mole rats (Heterocephalus glaber) have shown that
aggression by breeding females suppresses reproduction in other females,
primarily daughters (Faulkes et al.,
1991). These attacks might cause physiological stress for the
pregnant subordinate female, reducing her litter size and fertility. Urine
pheromones, which play an important role in female—female interactions
in small mammals (Jemiolo et al.,
1989; Labov, 1981;
Lawton and Whitsett, 1979;
Wolff, 1992), might cause
similar physiological changes, leading to fewer and smaller litters.
A further strategy to manipulate reproductive success of the cooperative
partner is infanticidal behavior (for review see
Hrdy, 1979). In our study,
infanticide occurred in litters of dominant and subordinate females. Similar
behavior was demonstrated in pregnant house mice killing each other's
offspring (Manning et al.,
1995). This was interpreted as a manipulation to invest less in
foreign offspring while raising pups communally. In our study, although not
quite significant at the 5% level, infanticidal behavior was highest in
unrelated females. It is not unexpected that unrelated females, both dominant
and subordinate, might have the least interest in investing in offspring of
the counterpart and engage in greatest infanticidal behavior. It is
interesting that in MD and S breeding units, infanticidal behavior of
subordinates was greater than that of dominants. This might be a subordinate
strategy, particularly for MDsub, to balance investment by reducing
the too numerous offspring of the dominant female. It could be excluded that
males performed infanticide (Gerlach, unpublished data). These results might
fit the incomplete control model better than the optimal skew model, which
predicts higher infanticide or oophagy in dominants
(Reeve and Ratnieks, 1993),
demonstrated in the ponerine ant Pachycondyla apicali
(Oliveira and Hölldobler,
1991).
Conclusion
Our results do not support previous models
(Clutton-Brock, 1998;
Reeve et al., 1998;
Vehrencamp, 1983). We show
that subordinates pay for being accepted rather than being paid (receiving
incentives) for being helpers. Dominant females have no advantage in terms of
increasing their reproductive success by breeding communally when ecological
circumstances do allow solitary breeding. Recently, Johnstone and Cant
(1998) added to the complexity
of cooperative breeding the interesting behavioral observations that, in many
species, dominant group members forcibly evict or exclude subordinates from
the group, and subordinates are reluctant to leave (Gerlach,
1990,
1996; see review on rodents:
Anderson, 1989). This is also
true in wood mice (Gerlach, unpublished data), and it fits the predictions
based on our calculations of inclusive fitness of either breeding unit.
Ecological circumstances, such as nest site availability and food limitation,
are supposed to be the crucial factors determining the occurrence of communal
breeding units. If nest sites are limited, MDdom should accept a
daughter who has no other chances for reproduction. If ecological conditions
are so harsh that saving time and energy with nursing would pay off,
Fdom, and even more Sdom, should accept subordinate
females because this allows them to reduce their nursing investment.
Subordinates should make the best of their situation. Daughters could and did
increase their inclusive fitness by helping their mothers to wean offspring.
Subordinate sisters or unrelated females did not increase their fitness so
effectively. Their reduced investment might be an appropriate response.
We predict that under natural circumstances, mother—daughter breeding
pairs should be more common and stable than those of sisters or unrelated
females. Kokko and Johnstone's model
(1998) showed that stable
breeding units are possible even if they lead to a decrease in immediate
reproductive success as long as subordinates can gain long-term success
through inheritance of territory, which may be more efficient than attempting
to establish a new territory. Recently, Queller et al.
(2000) showed that
subordinate, unrelated helpers in the social wasp Polistes dominulus
gain through inheritance of a territory. This might be an additional factor
for MDsub to accept her role because she might have a greater
probability to take over the maternal territory than Ssub and
Fsub, who are of the same age as their dominant counterparts. Our
observations in a large outdoor enclosure give first evidence that this is
indeed the case (Musolf and Gerlach, in preparation).
|
ACKNOWLEDGEMENTS |
|---|
We express our gratitude to J. Atema, L. Keller, and two anonymous referees for valuable criticism of the manuscript and to W. Nagl for statistical advice. We also thank R. Hellmann for laboratory help and H. Markl for generously supporting the project. This study was supported by the University of Konstanz, Verband der Chemischen Industrie, and by the Deutsche Forschungsgemeinschaft DFG (Ge 842/1-3).
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