Behavioral Ecology Vol. 10 No. 2: 178-184
© 1999 International Society for Behavioral Ecology
Costly young and reproductive skew in animal societies
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
Address correspondence to M. A. Cant, Department of Biology, University College London, Wolfson House, 4 Stephenson Way, London NW1 2HE, U.K. E-mail: mcant{at}galton.ucl.ac.uk
Received 2 March 1998; revised 3 August 1998; accepted 12 August 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Many recent models of reproductive skew explain subordinate reproduction as a staying incentive offered by dominants, who can produce more young with a helper present than without. Here, we present a new, alternative explanation for subordinate reproduction, which applies whenever the fitness cost to a parent of producing young is an accelerating function of the number produced (as commonly assumed in optimal clutch size theory). Under these circumstances, a dominant individual may be selected to offer a share of reproduction to a related subordinate, not as an incentive to stay, but because additional offspring that would be expensive for the dominant to produce are cheap for the subordinate. "Beneficial sharing" of this kind is more likely the more closely related the subordinate is to the dominant, so that the model predicts a negative relationship between skew and relatedness. This result runs directly counter to the positive relationship predicted by previous incentive-based models. We explore the interaction of these contrasting effects by developing an integrated model that allows for both beneficial sharing and staying incentives. When offspring are cheap to produce, this integrated model predicts that the incentive effect will dominate, and skew will increase with relatedness. When young are costly, in contrast, beneficial sharing will be of greater importance, and skew will decrease with relatedness.
Key words: cooperative breeding, cost of reproduction, dominance, reproductive skew, subordinate.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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A current focus of behavioral ecology is to identify what factors determine the distribution of reproduction, or the degree of reproductive skew, in social groups. In high-skew animal societies, one or a few individuals monopolize reproduction, whereas in low-skew societies breeding is distributed more equally (Keller and Reeve, 1994
; Vehrencamp,
1983a, b). The
level of reproductive skew varies widely, even between closely related
species. For example, in dwarf mongooses (Helogale parvula) usually
only one female breeds (Creel and Waser,
1991; Keane et al.,
1994; Rood, 1990),
whereas in banded mongooses (Mungos mungo) it is the norm for all
adult females in the group to give birth together
(Rood, 1975; Cant M,
unpublished data). Similarly, in social insects there is often great variety
within genera in the number and relative contribution of queens to colony
reproduction (Keller and Vargo,
1993; Spradberry,
1991).
Vehrencamp (1979,
1983a,
b) introduced a simple optimal
skew model to explain the division of reproduction in groups of cooperative
breeders. This and extended versions of the model (e.g.,
Johnstone et al., in press;
Reeve, 1998;
Reeve and Keller, 1995;
Reeve and Ratnieks, 1993) make
the assumption that the distribution of reproduction within a group is under
the control of a single dominant animal. The dominant offers reproductive
"staying incentives" to subordinates who might otherwise do better
to leave, perhaps because they have a high chance of dispersing successfully
or because they are unrelated to the dominant's young and therefore accrue no
indirect fitness benefit by helping her to raise offspring. Thus,
incentive-based models predict that high skew will be associated with severe
ecological constraints on independent breeding and high relatedness between
group members.
Incentive-based models of skew have generated a great deal of interest
because they potentially provide a framework to account for variation in skew
across all sorts of taxa, from social insects to communally breeding mammals
(see Keller and Reeve, 1994;
Reeve et al., 1998). Moreover,
there is some empirical support for their predictions. For instance, in
leptothoracine ants high skew is found associated with strong ecological
constraints, and possibly with high relatedness, although data regarding the
latter are scarce (Bourke,
1997; Bourke and Heinze,
1994; Heinze,
1995). Similar associations have also been reported in a few
vertebrate species (reviewed by Emlen,
1997). Clutton-Brock
(1998), however, points out
that few of these vertebrate studies are able to rule out alternative
explanations for the observed patterns of skew and concludes that there is a
need for more sophisticated models. This is particularly the case if we expect
the models to be applicable to social organisms with radically different
biology.
Here, we develop a new optimal skew model that incorporates a hitherto
neglected factor, the cost of producing young. This cost is of great
importance because it can potentially provide a novel explanation for
subordinate reproduction. When, as commonly assumed in classical optimal
clutch size models (e.g., Charnov and
Krebs, 1974; Daan et al.,
1990; Kacelnik,
1989; Trivers,
1972, 1974), it
becomes increasingly costly for a dominant individual to add each successive
offspring to a brood, it may pay to yield a share of reproduction to a related
subordinate, even if the latter does not help with offspring care (following
Trivers, 1972, we define cost
in terms of the decrement to the future reproductive value of the parent).
This is because additional offspring would be expensive for the dominant to
produce but are cheap for the subordinate. Previous models of reproductive
skew have not explicitly dealt with the costs of offspring production (e.g.,
Reeve and Ratnieks, 1993) or
else have assumed that such costs are linear
(Johnstone and Cant, in press)
and thus have overlooked this possibility.
To explore the consequences of accelerating costs of producing young on the stable partitioning of reproduction, we first consider the simplest possible case in which a subordinate must remain in association with the dominant but contributes nothing to offspring care. Under these circumstances, the dominant will never offer a staying incentive and will only give up a share of reproduction as a means of defraying the costs of offspring production. We then integrate this approach with existing incentive-based models by incorporating a subordinate contribution to care and allowing the subordinate the decision of whether to disperse or to stay and help in an association with the dominant. We show that the predictions of this integrated model are highly sensitive to the magnitude of the cost of young. Consequently, we suggest that patterns of skew are likely to differ markedly between the societies of insects, birds, and mammals because the costs of offspring production differ markedly among these different taxa.
The model
A basic model incorporating accelerating costs of young
We consider a situation where offspring fitness depends on brood size and
ask how reproduction will be shared between two females, referred to as Alpha
and Beta, who contribute to a communal brood. Alpha is dominant to Beta and
has full control over the distribution of reproduction. She produces
n young herself and allows Beta to produce f young. The
total brood size is denoted t (=n + f).
For simplicity we assume that individual offspring fitness,
s(t), declines linearly with brood size, t, so that
s(t) = 1 - kt, where k is a measure of the
sensitivity of offspring to increasing brood size (the results are
qualitatively similar for a nonlinear decrease in offspring fitness with brood
size). The total productivity of a brood of size t is given by
 | (1) |
Producing young entails an accelerating fitness cost (sensu
Trivers, 1972) to the
individual parent. To be more precise, we assume that the cost of producing
n young is equal to xn2, where x is some
constant (we use this particular function for reasons of tractability; other
accelerating functions yield qualitatively similar results). Note that we are
concerned with personal costs incurred solely by the breeder that produces the
n offspring, rather than shared costs involved in rearing young to
independence.
We can readily find the optimum clutch size for a single breeder: this will
be the brood size that maximizes F(n), the net benefit of
producing n young. F(n) is given by
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Solving for n, a single female's optimum clutch size, we obtain
 | (2) |
(see Figure 1).
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To analyze what happens when two females contribute to the brood, we find an expression for the inclusive fitness payoff to Alpha as a function of n and f. Because in this model Alpha has full control over the distribution of reproduction, the evolutionarily stable individual brood sizes n* and f* are those for which Alpha's inclusive fitness payoff from the breeding attempt is maximized.
Assuming that the total productivity of a combined brood, T
(n + f), is shared according to the relative contributions
of the two breeders, we can write Alpha's inclusive fitness payoff,
, as follows:
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The first two terms on the right-hand side of this expression represent Alpha's direct fitness payoff, the term in brackets represents Beta's direct fitness payoff, and r is the coefficient of relatedness between Alpha and Beta.
Rearranging we obtain:
 | (3) |
To find n* and f* we calculate the
partial derivatives of with respect to n
and to f, set both equal to zero, and then solve simultaneously for
n and f. The solution is
 | (4a) |
 | (4b) |
(it is easy to show that these are fitness maxima). This solution, however,
is biologically meaningful only if f* 
0 and
n* 0. For
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this requirement is not met, indicating that Alpha does best not to allow Beta any direct reproduction. Under these circumstances, f* = 0 and n* is equal to a single female's optimal clutch size, given in Equation 2.
Results of the basic model
In a previous model (Cant,
1998) that assumed linear costs of producing young, it never paid
Alpha to allow any subordinate reproduction: if there was any benefit to
having extra young in the brood, Alpha did better to produce them herself.
However, when the cost of producing young is an accelerating function of
number produced, additional offspring are expensive for Alpha, while Beta can
produce her first few young at relatively low cost. If the two breeders are
related, Alpha's payoff can thus be maximized by allowing Beta some share of
reproduction (this argument will hold for postproduction costs associated with
rearing young to independence only in cases where each parent cares
disproportionately for its own young).
The basic model predicts that when relatedness is zero, Alpha never shares
reproduction with Beta. When Alpha and Beta are related, Alpha grants a larger
share of reproduction to Beta the higher the cost of young
(Figure 2). We can summarize
this trend using Pamilo and Crozier's
(1996) index of skew
(S):
 |
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where NT is the total number of potential breeders, and
QE is the effective number of breeders, defined as
QE = 1/
pi2, where
pi is the reproductive contribution of the ith
breeder. As shown in Figure 3,
the stable level of skew falls rapidly from 1 (monopolization by Alpha) at low
levels of relatedness, to 0 (equal sharing of reproduction) at r = 1.
The threshold value of relatedness above which this decline begins is lower
the higher the cost of young (Figure
3). This predicted relationship between relatedness and skew runs
directly counter to previous skew models (e.g.,
Cant, 1998;
Reeve and Ratnieks, 1993).
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An integrated model: incorporating options for the subordinate
So far, we have analyzed the stable level of skew as if Beta had no option
but to produce the number of young, f*, permitted by
Alpha. In contrast, optimal skew models (e.g.,
Reeve and Ratnieks, 1993;
Vehrencamp, 1983a,
b) make two important
assumptions concerning the options available to subordinates. First,
subordinates may choose to leave the group and have some probability of
dispersing successfully to become an independent breeder. Second, two-female
associations are more successful in raising young, so subordinates can accrue
some indirect fitness benefits from remaining with the dominant. This helping
effect is the reason the dominant is willing to offer a reproductive staying
incentive to keep the subordinate in the group.
We integrate the current model with the models of Reeve and his co-workers
(Reeve, 1991;
Reeve and Keller, 1995;
Reeve and Ratnieks, 1993) by
incorporating two additional variables: d, the probability with which
a subordinate disperses successfully (0 < d < 1); and
h, the ratio of offspring fitness in a two-female association
relative to that for a single breeder (h 1). The integrated
model is then analyzed as follows:
- We determine (as above) the optimum numbers of young that Alpha should
produce herself, and that she should allow Beta to produce,
n* and f* (these are the numbers that
maximize Alpha's inclusive fitness, taking into account the increased fitness
of offspring in a two-member group).
- If this division of reproduction results in a higher inclusive fitness
payoff for Beta than she would gain by dispersing, then she will remain in the
group, and the results of the model are unaffected by incorporating the
possibility of dispersal.
- If, in contrast, Beta would do better to disperse than to accept the
f* young allowed her by Alpha, we now find an expression
for the minimum number of young Alpha must allocate to ensure that Beta would
do better to stay in the group. This is equivalent to the staying incentive of
Reeve and Ratnieks (1993),
though here it is a function of the number of young produced by Alpha.
- We find the optimum brood size for Alpha to produce,
n1*, given that if she produces n
young, she must grant at least f1* (n)
to Beta.
- Finally, we check whether it pays Alpha to grant Beta her staying incentive
[i.e., to produce n1* young herself, and allow
Beta to produce f1* (n)] or whether
she would do better to allow Beta to disperse and breed alone.
To find f1* (n), the minimum number
of young Alpha must allocate to ensure that Beta does better to stay in the
group, we proceed as follows: Let ßD equal the
inclusive fitness payoff to Beta if she disperses to breed independently, and
ßS equal her payoff if she stays to help Alpha. If we
assume that Beta enjoys the same reproductive success when breeding alone as
would Alpha, we can write:
 |
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is given by (2). Similarly, we
can write:
 |
 |
which simplifies to
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Beta's critical share of reproduction as a function of n,
f1* (n), is found by setting
ßS = ßD and solving for
f.
Having obtained an expression for f1*
(n), we can find the optimum number of young for Alpha to produce
given that if she produces n young, she must grant at least
f1* (n), to Beta. Alpha's inclusive
fitness for any n, f is given by
 | (5) |
To find Alpha's optimum number of young, we replace f in Equation
5 with the derived expression for f1*
(n), and solve for d/dn =
0.
The variables n1* and
f1* (n1*)
specify Alpha's optimum distribution of reproduction, given that she must
allow Beta enough young to keep her in the association. However, we have yet
to test whether it pays Alpha to offer a staying incentive, or whether she
would do better if Beta dispersed. Thus the solutions
n1* and f1*
(n1*) are evolutionarily stable solutions only
for * > 1, where
* is the expression obtained after
substituting n1* and
f1* (n1*) in
Equation 5, and 1 is Alpha's inclusive fitness when Beta
disperses, given by
 |
If * > 1, the
evolutionarily stable solution is for Beta to disperse and for both breeders
to produce young.
Results of the integrated model
Considering the effect of relatedness on the division of reproduction, we
find that initially, as relatedness increases, the number of young produced by
Beta declines (Figure 4). This
is essentially the effect reported by Reeve
(1991) and Reeve and Ratnieks
(1993): with increasing
relatedness, the size of the staying incentive required to keep the
subordinate as a helper declines (here we call this the "incentive
effect"). However, above a certain threshold value of relatedness
(around r = 0.2 in the example shown), this trend is reversed: Beta
starts to produce more young, while the number of young produced by Alpha
decreases. This is the pattern seen in the basic model above, which we call
the "beneficial sharing" effect. At higher values of relatedness,
it pays Alpha to grant a share of reproduction to Beta because the first few
young are cheap for Beta to produce. Again, when r = 1 there is no
conflict between the breeders, and they agree to produce a total brood size
closer to that which is most productive by sharing equally the costs of
reproduction.
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The two contrasting effects of relatedness on skew are shown clearly in Figure 5 for three levels of costliness of young. The stable level of skew (once again measured by Pamilo and Crozier's index S, defined above) initially rises with relatedness (the incentive effect), but at higher values of relatedness skew declines (the beneficial sharing effect). The point at which Alpha grants reproduction to Beta as a beneficial share rather than as a staying incentive depends on the cost of young. When young are relatively cheap, the incentive effect dominates for all but the highest values of relatedness, and the expected relationship between skew and relatedness is positive for biologically reasonable parameter values. When young are costly, in contrast, Alpha starts to offer a beneficial share at relatively low levels of relatedness, and the correlation between skew and relatedness is for the most part negative.
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Figure 6 shows the effect of the relative cost of young on the stable level of skew for three values of relatedness. When r = 0, it never pays Alpha to offer a beneficial share, so subordinate reproduction always represents an incentive offered by Alpha. At higher levels of relatedness, there is a switching point between incentives and beneficial sharing as costs increase. When costs are very low, incentives predominate. Here an increase in cost is associated with an increase in skew, because the benefit to Beta of dispersing declines relative to that of staying, so Alpha needs to offer less reproduction as an incentive for Beta to stay. As costs rise further, we reach the switching point at which Alpha starts to offer a beneficial share of reproduction to Beta. In this region, skew declines with increasing costs because Alpha benefits more and more from sharing the expense of the brood with Beta.
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The three curves in Figure 6
converge as costs become small. The point of convergence is the decision point
at which Beta does better to disperse than to stay in the association. Because
this point is the same regardless of relatedness, we agree with Reeve and
Ratnieks (1993) that
relatedness should have no effect on the probability that a subordinate will
join an association rather than disperse to breed independently. The model
also agrees with that of Reeve and Ratnieks in predicting an overall negative
relationship between skew and d, the probability of successful
dispersal, though this is not shown in the figures.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Models of reproductive skew attempt to identify the factors that determine the division of reproduction in animal societies. Here we have shown that one previously neglected factor, the cost of producing young, can exert an important influence on the stable level of skew within groups. When cost is an accelerating function of the number of young that an individual produces, it will sometimes pay a dominant animal to allow a related subordinate to contribute to the joint brood—not as a staying incentive to keep her in the group, but because additional offspring would be expensive for the dominant to produce but are cheap for the subordinate. Note that costs of rearing that are shared among group members are not relevant to the present argument. Instead, we are concerned with personal costs paid by a parent to produce young—e.g., the costs to avian parents of egg production (which have recently been shown to be comparable with the costs of incubation and provisioning of chicks in some species; Monaghan and Nager, 1997
).
Incorporating shared costs into the model does not, however, qualitatively
alter the results.
Introducing the beneficial sharing effect into existing skew models can
alter their predictions quite dramatically. In incentive-based models
(Reeve, 1991;
Reeve and Ratnieks, 1993),
which assume that the dominant has perfect control over subordinate
reproduction, related subordinates gain indirect fitness benefits from helping
their relatives to breed and so require less in the way of incentives to keep
them in the group. In an alternative incomplete control model by Cant
(1998), which assumes that
dominants cannot prevent subordinates from breeding, related subordinates are
selected to add fewer young to the dominant's brood. Both models, therefore,
predict a positive relationship between reproductive skew and relatedness. The
present analysis, however, reveals that this result depends on the assumptions
one makes about the cost of producing young. When costs are relatively low
and/or linear the model predicts a positive correlation between skew and
relatedness. When costs are high and accelerating the model predicts the
opposite relationship because dominants are more likely to offer a beneficial
share of reproduction to a related subordinate than to an unrelated one.
Because we have defined cost in terms of opportunities to invest in future
young, an accelerating cost function is equivalent to a convex-down
relationship between investment in the current brood and adult survivorship,
which is a standard assumption in optimal clutch size theory
(Charnov and Krebs, 1974;
Daan et al., 1990;
Kacelnik, 1989). Adding
successive young to a single brood is likely to result in ever greater
decrements in parental fitness because there is only a finite amount of
resources available to invest in both offspring production and survival of the
parent itself, and in mammals because increased fetal litter size may also
lead to increased energetic costs of locomotion and foraging or increased risk
of predation. In contrast, the conditions associated with accelerating costs
of young are less likely to apply to continuously breeding species, producing
eggs one at a time rather than in litters or clutches, particularly if the
mother is freed from the constraints of having to find resources for egg
production herself. Such a situation corresponds to that of many social
insects, where workers bring resources for egg production to the queen. The
current analysis therefore suggests that one should find positive associations
between skew and relatedness (as predicted by previous models) in social
insects, whereas among communally breeding birds and mammals there is more
likely to be no association or even a negative one.
Available data on skew and relatedness in ants and wasps seem to offer
preliminary support for the prediction of incentive-based models that high
skew will be associated with high relatedness
(Bourke, 1997;
Bourke and Franks, 1995;
Bourke et al., 1997; but see
Field et al., 1998). Keller
and Reeve (1994;
Reeve and Keller, 1995)
suggested that there was a similar trend among birds, and in a recent paper
they present comparative evidence to this effect
(Reeve et al., 1998). However,
if we restrict the analysis to skew among females (with which the current
model is concerned), we find that there are too few data at present to test
this prediction. Of the four species of communally breeding birds in which
relatedness and skew between females have been reliably estimated (common
moorhen Gallinula chloropus:
McRae, 1996; pukeko
Porphyrio porphyrio: Jamieson,
1997; acorn woodpecker Melanerpes formicivorus:
Koenig et al., 1995; Galapagos
mockingbird Nesomimis galapageonsis:
Curry, 1988;
Curry and Grant, 1990), only
two (moorhens and pukeko) showed a significant difference between skew in
related versus unrelated associations.
In mammals, comparative data offer a similarly inconclusive picture. In
naked mole rats (Heterocephalus glaber), high skew among females is
associated with high relatedness, as predicted by incentive-based skew models.
In damaraland mole rats (Cryptomys damarensis), however, maximum skew
among females is associated with substantially lower levels of intracolony
relatedness (Bennett, 1994;
O'Riain MJ, personal communication), suggesting that factors other than
relatedness (e.g., severe ecological constraints) are likely to have driven
the evolution of high skew in the the eusocial Bathyergidae
(Faulkes et al., 1997). In
lions, all adult females in a pride are close relatives, yet normally all
reproduce (Packer et al.,
1988, 1991). At an
intraspecific level, the strongest support for incentive-based models comes
from Creel and Waser's (1991,
1997) studies of dwarf
mongooses, among whom female subordinates less closely related to the same-sex
dominant are more likely to reproduce. As Clutton-Brock
(1998) points out, however,
these females also tend to be older and less closely related to male breeders,
and both of these factors may provide an alternative explanation for the
observed pattern of reproduction (e.g., the dominant may be less easily able
to suppress reproduction by older individuals, and subordinate females may
avoid mating with closely related males). Further genetic studies of
cooperatively breeding vertebrates are required before alternative models
based on incentives, beneficial sharing, and limited control can be properly
evaluated.
As mentioned above, the present model is relevant only to females and
suggests that there is an important distinction to be made between
reproductive skew among males and among females. Beneficial sharing is only
possible when subordinate reproduction can lead to an increase in the total
productivity of the group. Although this may be true among females, it does
not apply to males, who usually have no influence over brood size but merely
compete for a share of paternity. Consequently, the beneficial sharing
approach will be of little use in explaining variation in skew among males,
and the incentive-based models of Reeve et al. are likely to be better suited
to this task (Cant, 1998;
Clutton-Brock, 1998). Thus,
among males one would expect only positive associations between skew and
relatedness, as has been shown in lions
(Packer et al., 1991) and
white-fronted bee-eaters (Emlen and Wrege,
1992; reviewed by Reeve et
al., 1998). The best way to test this would be to compare skew
among males and females in the same society. Social vertebrates in which there
are several breeding males and females per group (e.g., banded mongooses,
lions, and acorn woodpeckers) may thus prove to be excellent species on which
to test the predictions of the current model.
One interesting possibility for future theoretical research suggested by the model is the investigation of multiple breeding events. Because the costs of offspring production are expressed in terms of a reduction in future reproductive success, a fuller analysis would need to consider an individual's opportunities for breeding over 2 or more successive years. This would make explicit the trade-off between greater productivity in one breeding season and the next. Furthermore, the fitness costs of producing a given number of young would then depend on the likely extent of breeding opportunities in the future (because if an individual has little chance to breed in future, there is little to be lost by sacrificing a degree of survival probability in order to raise more offspring during the current breeding attempt).
A further complication is that production costs suffered by dominants may
be reduced by better access to resources, morphological specialization for
reproduction (e.g., female naked mole rats;
Jarvis et al., 1991), or
escape from more costly behavioral roles (e.g., babysitting in suricates;
Clutton-Brock et al., 1998). In
such cases, the production of young may involve a greater decrement to future
fitness for subordinates than for dominants, which will restrict the
possibility for beneficial sharing. Assessing the importance of these
different factors is difficult because costs are unlikely to be fixed, but
they will be influenced by behavioral decisions on the part of group members
(e.g., concerning the division of labor involved in brood care). There is thus
considerable scope for futher models of beneficial sharing that incorporate
individual differences in cost.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank Andrew Bourke, Tim Clutton-Brock, Nick Davies, William Foster, Laurent Keller, and Kern Reeve for comments on the manuscript and Sue McRae for helpful discussions. M.A.C. was funded by a Biotechnology and Biological Sciences Research Council studentship. R.A.J. was funded by a Royal Society University Research Fellowship.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Bennett NC, 1994. Reproductive suppression in social Cryptomys damarensis colonies—a lifetime of socially induced sterility in males and females (Rodentia, Bathyergidae). J Zool 234:25-39.
Bourke AFG, 1997. Sociality and kin selection in insects. In: Behavioural ecology: an evolutionary approach, 4th ed (Krebs JR, Davies NB, eds). Oxford: Blackwell Scientific Publications;203 -227.
Bourke AFG, Franks NR, 1995. Social evolution in ants. Princeton, New Jersey: Princeton University Press.
Bourke AFG, Green HA, Bruford MW, 1997. Parentage, reproductive skew and queen turnover in a multiple-queen ant analysed with microsatellites. Proc R Soc Lond B 264:277-283.[Medline]
Bourke AFG, Heinze J, 1994. The ecology of communal breeding: a case of multiple-queen leptothoracine ants. Phil Trans Roy Soc Lond B 345:359-372.
Cant MA, 1998. A model for the evolution of reproductive skew without reproductive suppression. Anim Behav 55:163-169.[Web of Science][Medline]
Charnov EL, Krebs JR, 1974. On clutch-size and fitness. Ibis 116:217-219.[Web of Science]
Clutton-Brock TH, Gaynor D, Kansky R, MacColl ADC, McIlrath G, Chadwick P, Brotherton PNM, O'Riain MJ, Manser M, Skinner JD,1998 . Costs of cooperative behaviour in suricates (Suricata suricatta). Proc R Soc Lond B 265:185-190.[Medline]
Clutton-Brock TH, 1998. Reproductive concessions and skew in vertebrates. Trends Ecol Evol 7:288-292.
Creel SR, Waser PM, 1991. Failures of reproductive suppression in dwarf mongooses (Helogale parvula), accident or adaptation? Behav Ecol Sociobiol 2:7-15.
Creel SR, Waser PM, 1997. Variation in reproductive suppression among dwarf mongooses: interplay between mechanisms and evolution. In: Cooperative breeding in mammals (Solomon NG, French JA, eds). Cambridge: Cambridge University Press;150 -170.
Curry RL, 1988. Group structure, within-group conflict, and reproductive tactics in cooperatively breeding Galapagos mockingbirds, Nesomimus parvulus. Anim Behav 36:1708-1728.
Curry RL, Grant PR, 1990. Galapagos mockingbirds, territorial co-operative breeding in a climatically variable environment. In:Co-operative breeding in birds (Stacey PB, Koenig WD, eds). Cambridge: Cambridge University Press;289 -332.
Daan S, Dijkstra C, Tinbergen JM, 1990. Family planning in the kestrel (Falco tinnunculus): the ultimate control of covariation of laying date and clutch size. Behaviour 114:83-116.[Web of Science]
Emlen ST, 1997. Predicting family dynamics in social vertebrates. In: Behavioural ecology: an evolutionary approach, 4th ed (Krebs JR, Davies NB, eds). Oxford: Blackwell Scientific Publications;228 -253.
Emlen ST, Wrege PH, 1992. Parent-offspring conflict and the recruitment of helpers among bee-eaters. Nature 356:331-333.
Faulkes CG, Bennett NC, Bruford MW, O'Brien HP, Aguilar GH, Jarvis JUM, 1997. Ecological constraints drive social evolution in the African mole-rats. Proc R Soc Lond B 264:1619-1627.[Medline]
Field J, Solis CR, Queller DC, Strassmann JE, 1998. Social and genetic structure of paper-wasp co-foundress associations: tests of reproductive skew models. Am Nat 151:545-563.[Web of Science][Medline]
Heinze J, 1995. Reproductive skew and genetic
relatedness in Leptothorax ants. Proc R Soc Lond B
261:375-379.
Jamieson IG, 1997. Testing reproductive skew models in
a communally breeding bird, the pukeko, Porphyrio porphyrio.Proc R Soc Lond B
264:335-340.
Jarvis JUM, O'Riain MJ, McDaid E, 1991. Growth and factors affecting body size in naked mole-rats. In: The biology of the naked mole-rat (Sherman PW, Jarvis JUM, Alexander RD, eds). Princeton, New Jersey: Princeton University Press;338 -383.
Johnstone RA, Cant MA, in press. Reproductive skew and indiscriminate infanticide. Anim Behav.
Johnstone RA, Woodroffe R, Cant MA, Wright J, in press. Reproductive skew in multi-member groups. Am Nat.
Kacelnik A, 1989. Short-term adjustment of parental effort in starlings. Acta XIX Congr Int Ornith 2:1843-1856.
Keane B, Waser PM, Creel SR, Creel NM, Elliott LF, Minchella DJ,1994 . Subordinate reproduction in dwarf mongooses. Anim Behav 47:65-75.
Keller L, Reeve HK, 1994. Partitioning of reproduction in animal societies. Trends Ecol Evol 9:98-102.
Keller L, Vargo EL, 1993. Reproductive structure and reproductive roles in colonies of eusocial insects. In: Queen number and sociality in insects (Keller L, ed). Oxford: Oxford University Press; 16-44.
Koenig WD, Mumme RL, Stanback MT, Pitelka FA, 1995. Patterns and consequences of egg destruction among joint-nesting acorn woodpeckers. Anim Behav 50:607-621.[Web of Science]
McRae SB, 1996. Family values, costs and benefits of communal nesting in the moorhen. Anim Behav 52:225-245.
Monaghan P, Nager RG, 1997. Why don't birds lay more eggs? Trends Ecol Evol 17:270-274.
Packer C, Gilbert D, Pusey AE, O'Brien SJ, 1991. A molecular genetic analysis of kinship and cooperation in African lions.Nature 351:562-565.[Web of Science]
Packer C, Herbst L, Pusey AE et al., 1988. Reproductive success in lions. In: Reproductive success: studies of individual variation in contrasting breeding systems (Clutton-Brock TH, ed). Chicago: University of Chicago Press;363 -383.
Pamilo P, Crozier RH, 1996 Reproductive skew simplified. Oikos 75:533-535.[Web of Science]
Reeve HK, 1991. Polistes. In: The social biology of wasps (Ross KG, Matthews RW, eds). New York: Comstock; 99-148.
Reeve HK, 1998. Game theory, reproductive skew and nepotism. In: Game theory and animal behaviour (Dugatkin LA, Reeve HK, eds). Oxford: Oxford University Press;118 -145.
Reeve HK, Emlen ST, Keller L, 1998. Reproductive
sharing in animal societies: reproductive incentives or incomplete control by
dominant breeders? Behav Ecol
9:267-278.
Reeve HK, Keller L, 1995. Partitioning of reproduction in mother-daughter versus sibling associations, a test of optimal skew theory.Am Nat 145:119-132.[Web of Science]
Reeve HK, Ratnieks FLW, 1993. Queen-queen conflicts in polygynous societies, mutual tolerance and reproductive skew. In: Queen number and sociality in insects (Keller L, ed). Oxford: Oxford University Press; 45-85.
Rood JP, 1975. Population dynamics and food habits of the banded mongoose. E Afr Wildl J 13:89-111.
Rood JP, 1990. Group size, survival, reproduction and routes to breeding in dwarf mongooses. Anim Behav 39:566-572.
Spradberry JP, 1991. Evolution of queen number and queen control. In: The social biology of wasps (Ross KG, Matthews RW, eds). New York: Comstock;366 -388.
Trivers RL, 1972. Parental investment and sexual selection. In: Sexual selection and the descent of man 1871-1971 (Campbell B, ed). Chicago: Aldine;136 -179.
Trivers RL, 1974. Parent-offspring conflict. Am Zool 14:249-264.
Vehrencamp SL, 1979. The roles of individuals, kin and group selection in the evolution of sociality. In: Handbook of behavioural neurobiology, vol. 3. Social behaviour and communication (Marler P, Vandenbergh JG, eds). New York: Plenum Press; 351-394
Vehrencamp SL, 1983a. A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667-682.[Web of Science]
Vehrencamp SL, 1983b. Optimal degree of skew in cooperative societies. Am Zool 23:327-335.
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