Behavioral Ecology
doi:10.1093/beheco/arr018
Advance Access publication 17 March 2011
Original Article
Monogamous dominant pairs monopolize
reproduction in the cooperatively breeding pied
babbler
Martha J. Nelson-Flower,a Phil A.R. Hockey,a Colleen O’Ryan,b Nichola J. Raihani,c Morné A. du Plessis,a,d
and Amanda R. Ridleya,e
a
Percy FitzPatrick Institute of African Ornithology, Department of Science and Technology and National
Research Foundation Centre of Excellence, Department of Zoology, University of Cape Town,
Rondebosch 7701, South Africa, bDepartment of Molecular and Cell Biology, University of Cape Town,
Rondebosch 7701, South Africa, cInstitute of Zoology, Zoological Society of London, Regent’s Park,
London NW1 4RY, UK, dWorldwide Fund for Nature South Africa, Private Bag X2, Die Boord,
Stellenbosch 7613, South Africa, and eCentre for the Integrative Study of Animal Behaviour, Department
of Biological Sciences, Macquarie University, Marsfield, NSW 2122, Australia
Understanding how reproduction is partitioned between group members is essential in explaining the apparent reproductive
altruism of cooperatively breeding systems. Here, we use genetic data from a population of cooperatively breeding pied babblers
(Turdoides bicolor) to show that reproduction is highly skewed toward behaviorally dominant birds. Dominant birds monopolized
reproduction, accounting for 95.2% of all chicks. Inbreeding avoidance appears to constrain subordinate reproduction because
the rare incidences of subordinate reproduction occurred only with unrelated members of their groups. However, even when
unrelated potential breeding partners were present in the group, subordinates rarely bred. Although half of chicks hatched into
groups where subordinates could potentially breed, only 9.6% of these chicks had a subordinate parent, indicating that additional factors limit subordinate reproduction, such as reproductive conflict with dominants. Groups were highly kin structured
and most subordinates were closely related to one another such that help was almost invariably directed toward close relatives.
Consequently, helping in this species confers indirect fitness benefits on subordinates, which are likely to play an important role
in the evolution and maintenance of cooperative helping behavior. Key words: cooperative breeding, inbreeding, monogamy,
pied babbler, reproductive skew, Turdoides bicolor. [Behav Ecol 22:559–565 (2011)]
INTRODUCTION
ooperative breeding occurs when more than 2 individuals
help to raise young in a single brood, and some of the
helping (often subordinate) individuals do not breed
(Cockburn 2004). Many cooperatively breeding systems are
characterized by high reproductive skew in one or both sexes,
such that a small proportion of individuals monopolize reproduction (Keller and Reeve 1994; Cockburn 2004; Raihani and
Clutton-Brock 2010). A first question to investigate is why
subordinates refrain from breeding. Although subordinates
may be sexually mature, they may not be in sufficiently good
physical condition to breed (Clutton-Brock et al. 2001) or may
be tolerated in the group only as helpers (Kokko et al. 2002).
Alternatively, they may be constrained from breeding in the
natal group by the absence of unrelated breeding partners
(Koenig and Pitelka 1979) and the attendant risk of inbreeding depression should they breed with relatives (Pusey 1987;
Pusey and Wolf 1996). Parentage must therefore be verified to
be sure that subordinates are not in fact breeding and that
they do not do so with kin. A second question to investigate is
why subordinates help. Subordinates may help nondescend-
C
Address correspondence to M.J. Nelson-Flower. E-mail: marthajn
@hotmail.com.
Received 27 September 2010; revised 1 January 2011; accepted 10
January 2011.
The Author 2011. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
ant kin to facilitate the success of shared genes and gain indirect fitness benefits, the primary tenet of kin selection
theory (Hamilton 1964; Maynard-Smith 1964, reviewed by
Griffin and West 2003). Alternatively, helpers may acquire direct fitness benefits, either in addition to or in the absence of
kin-selected indirect benefits. Direct benefits may be gained
when help increases group size (‘‘group augmentation’’—Brown 1987; Kokko et al. 2001), leading to increased chances
of survival due to better vigilance (Pulliam 1973; Ridley et al.
2008) and larger coalition sizes at dispersal (reviewed by
Heinsohn and Legge 1999; Russell 2004). In interpreting
the inclusive fitness consequences of helping, it is again important to verify parentage since subordinates may help because they are the parents of some of the offspring
(Richardson et al. 2001, 2002).
To answer these questions and better understand cooperatively breeding systems, molecular techniques must be used
to provide reliable information about parentage within the
group. Such techniques have revealed that extrapair reproduction in cooperative breeders is common (Mulder et al.
1994; Li and Brown 2000; Richardson et al. 2001). Mating
systems among avian cooperative breeders include polygyny
(where several group females breed in a single nest), polygynandry (where several group members, both male and female,
breed in a single nest), hidden leks (where a very high rate of
extra-group paternity is the norm), and finally, true monogamy, which has been estimated to occur in only a few cooperatively breeding birds (reviewed by Cockburn 2004).
Behavioral Ecology
560
Molecular techniques have also been used to investigate the
extent of inbreeding in cooperatively breeding species
(reviewed by Cockburn 1998; Griffith et al. 2002). Thus, genetic information is now essential to understand 1) the direct
fitness benefits of obtaining dominance, 2) the direct fitness
benefits obtained through reproduction as a subordinate, 3)
the potential indirect fitness benefits of helping as a subordinate group member, 4) the extent of inbreeding and whether
inbreeding avoidance restricts subordinate reproduction, and
5) the extent and outcome of reproductive conflict within
groups where subordinates have the opportunity to breed.
The pied babbler (Turdoides bicolor) is a cooperatively
breeding passerine (70–95 g) that lives in family groups comprising a dominant pair and a variable number of adult helpers of both sexes. Based on behavioral observations, it has
been speculated, but not empirically demonstrated, that
dominant individuals monopolize breeding opportunities
and that inbreeding is rare (Raihani 2008). We used microsatellite DNA genotyping and field observations of courtship,
copulation, and group composition to answer 4 questions: 1)
which group members are breeding, 2) how related are
group members to one another, 3) does inbreeding occur,
and 4) what reproductive opportunities are available to subordinates?
MATERIALS AND METHODS
Study site and population
Comprehensive observations of pied babbler group life histories and breeding attempts were collected from July 2003 to
May 2008 at the Kuruman River Reserve, South Africa (lat
2658#S, long 2149#E) (for information on climate and vegetation, see Raihani and Ridley 2007). Twenty-three wild pied
babbler groups were habituated to the close presence of a human observer at a distance of 2–3 m, allowing observational
data to be collected without disturbing natural behavior (for
habituation techniques, see Ridley and Raihani 2007a). Each
individual in the population was ringed with a unique combination of colored leg rings.
Pied babbler groups ranged in size from 2 to 11 adults
(individuals more than 12 months old—Ridley and Raihani
2008) with a mean group size of 4.3 6 0.2 adults. Habituated
groups were adjacent to one another and defended yearround territories of 1–3 km2. Groups typically comprised
a dominant pair with subordinate helpers, the status of
which could be determined based on the observation of
dominance assertions (pecks and other attacks), to which
subordinates responded with submissive behavior (Raihani
2008). Peaceful interactions between babbler groups were
very rare (Ridley AR, unpublished data), making it difficult
for adult subordinates to associate with nongroup members
while simultaneously remaining members of their own
groups. Individuals that attempted to immigrate into nonnatal groups were often chased and attacked by members
of the receiving group (Raihani et al. 2010). An individual
could immigrate either as a dominant or subordinate and
immigration was not sex biased (Nelson-Flower 2010;
Raihani et al. 2010). Average age at dispersal was 1.5 years;
older birds were more likely to immigrate into groups as
dominants, whereas younger birds were more likely to immigrate into subordinate positions (Raihani et al. 2010). Immigrant subordinates never inherited dominance in these
(non-natal) groups. Copulation was witnessed between members of the same group (N ¼ 53 copulations in 16 groups
over 5 years, usually between dominants, but sometimes between dominants and subordinates) but was never observed
between members of different groups.
Which group members are breeding?
Parentage analysis allows assessment of both the level of reproductive skew and whether subordinates are breeding with relatives within the group. Samples were collected from 319
individuals in 23 groups over 5 years and were genotyped at
9 polymorphic loci (see Supplementary Material). Parentage
was calculated using CERVUS v. 3.0.3 (Kalinowski et al. 2007).
Allele frequencies used in parentage analysis were based on
the entire population rather than a subset (N ¼ 42) of unrelated individuals (for rationale, see Kalinowski et al. 2007)
because the parentage predictions resulting from the allele
frequencies estimated by the 2 data sets were similar, and
the data set of unrelated individuals was missing some rare
alleles. For the parentage analysis, only those nestlings that
were observed to have hatched into a fully sampled group with
known dominance structure (based on behavioral observations of ringed birds) were included. This reduced the sample
size to 159 nestlings from 67 broods produced by 12 groups.
For these 159 offspring, only adults were included as potential parents, but the CERVUS program was given no prior information about the social pairings of these potential parents.
Pied babblers are highly territorial (Ridley and Raihani 2007b)
and it was assumed that extra-group females would not have
opportunities to lay eggs in the group nest: Breeding was
asynchronous between groups and extra-group individuals
were attacked and chased off whenever they approached a babbler group (Raihani 2008). Only heavy females (mean body
mass of 88.4 6 1.0 g, range 83.1–95.1 g) lay eggs (Raihani
2008); those adult females with a preforage (dawn) body mass
of greater than 80 g during the period the eggs were laid (2–3
days prior to the onset of incubation) were included as candidate mothers (for weighing protocols, see Ridley and
Raihani 2007b). Because group females could potentially copulate with extra-group males (although this has never been
observed), all known adult males in the population at the time
of an offspring’s hatching were included as candidate fathers.
Those adult males that immigrated into the population after
the offspring hatched were also listed as potential fathers. All
males that had dispersed or disappeared from the study population were also included, unless there was proof of their
death.
CERVUS v. 3.0.3 simulation inputs were 100 000 offspring
using the analysis option ‘‘parent pair (sexes known)’’; 2
(range 1–3) candidate mothers per offspring with an estimated 99% of candidate mothers sampled; 70 (range 29–
76) candidate fathers per offspring, with an estimated 80%
of candidate fathers sampled (most chicks in this analysis were
born into groups which were surrounded by other groups with
fully sampled adults); 89% of candidate mothers related to
the offspring in question (almost all group subordinates were
related to at least 1 of the breeders) with a mean estimated
relatedness of 0.38 (based on relatedness calculations—Konovalov and Heg 2008; see below); and an estimate of
10% of candidate fathers related to the offspring in question
(based on behavioral observations) with a mean estimated
relatedness of 0.125. The proportion of loci typed was set at
0.982 (generated by the program), and the genotyping error
rate was set at 0.01.
How related are group members to one another?
Relatedness was calculated based on the microsatellite loci using an algorithm that is relatively insensitive to allele frequency
bias (Konovalov and Heg 2008) within the program KINGROUP v2_090218 (Konovalov et al. 2004). Relatedness was
also calculated using the KINSHIP estimator (Goodnight
and Queller 1999). However, the relatedness estimator of
Nelson-Flower et al.
Monogamous dominant pairs in pied babblers
561
Konovalov and Heg (2008) recaptured known relationships
more accurately (i.e., mothers and offspring in groups without helpers), and only these results are presented. Ninety-five
percent confidence intervals (CIs) around the population
mean were calculated using bootstrapping (10 000 replicates)
in R version 2.12.1 (www.r-project.org). High levels of relatedness among group subordinates can indicate that a single
dominant pair is monopolizing reproduction and that indirect fitness benefits are available to helpful subordinates. Relatedness was calculated for each group-year: In order to avoid
pseudoreplication, mean relatedness was found for each
group as a whole. Relatedness was also calculated between
subordinates and the chicks they helped to raise and between
dominants and subordinates. Gene flow was quantified between groups using the F-statistic FST (Wright 1951). FST is
the proportion of the total genetic diversity that separates
groups and ranges from 0 to 1: If there is no population substructure (i.e., no stable groups), FST will approach 0. FST was
calculated using analysis of molecular variation in the program GenAlEx 6.2 (Peakall and Smouse 2006). The program
tests each F-statistic for each year for significance by comparing the calculated value against a null distribution of 1000
random permutations of the data set. A significant FST value
indicates that there is group-based substructure in the population. Only fully blood-sampled groups were included in this
analysis (N ¼ 56 group-years, from 18 groups over 5 years).
at the time, with 100 000 permutations (sensu Stiver et al.
2008).
We also investigated courtship behavior, which occurs primarily as a prelude to copulation and involves either males aerially chasing females or mutual presentation of nesting
material (Raihani 2008). Courtship behavior between relatives
could indicate the occurrence of inbreeding. We compared
levels of relatedness between individuals observed in courtship behavior and between those sexually mature birds within
the group which undertook no courtship. We used a 2-sample
randomization/permutation test in RUNDOM PRO 3.14
(Jadwiszczak 2009) with 100 000 permutations to compare
relatedness between pairs of courting birds within groups with
relatedness between pairs of noncourting, adult opposite-sex
birds in groups.
•
Does inbreeding occur?
The extent of inbreeding can be determined from genetic patterns within the population using the F-statistics FIS and FIT
(Wright 1951), which were calculated as described above for
FST. Potential inbreeding within social pairs (the dominant
pair in each group) was investigated by measuring their relatedness, calculated as described above (the pedigree is not
yet deep enough to use pedigree-calculated values). Although
dispersal constraints imposed by social status and age are
likely to have considerable importance in structuring dispersal
in the population (Raihani et al. 2010), relatedness between
potential mates may also play a role. To investigate relatedness
and mate choice, the relatedness of social pairs was compared
with the relatedness between each mated-pair member and all
other opposite-sex adults in the population at the time. If the
relatedness of social pairs was significantly less than that of all
other possible pairings for these individuals, it indicates avoidance of related individuals as mates. If the relatedness of social pairs was significantly higher than that of all other
possible pairings for these individuals, then inbreeding may
be occurring regularly. If the mean relatedness between mates
did not differ from that of all other possible pairings for these
individuals, they are choosing mates that are neither more
nor less related to them than is average within the population.
Because relatedness estimates are by their nature based on
pairs of individuals, analyses ‘‘sample’’ each individual more
than once and data are thus nonindependent. This nonindependence can be controlled for by using a randomization/
permutation test, which generates a distribution of mean differences between 2 groups of values. This distribution is created by randomly assigning the data values into the groups
being compared and calculating the mean difference between
them. The permutation is repeated N times (recommended
1000 or more—Jadwiszczak 2009) to create a distribution of
simulated mean differences, against which the observed values can be compared and tested statistically. A 2-sample randomization/permutation test within the program RUNDOM
PRO 3.14 (Jadwiszczak 2009) was used to compare relatedness
of social pairs with the relatedness between each member of
each pair and all other opposite-sex adults in the population
What reproductive opportunities are available to
subordinates?
Because inbreeding and extra-group copulations appear to be
avoided (see below), the main route to reproduction for subordinate adults lies in immigration of unrelated potential
breeding partners to their groups. Individuals that joined
one of the fully sampled study groups during the breeding
season and stayed for 2 weeks or longer were considered to be
immigrants (Ridley et al. 2008). All individuals that were returning former group members, that were offspring of either
of the current dominant pair, or that were never bloodsampled were excluded from the analysis. Data from breeding
seasons only (September 1 to May 31) are presented. We measured the proportion of dominants and subordinates each
season that were new immigrants in groups, the proportion
of subordinates that could potentially breed each year, and
the proportion of these potentially breeding subordinates
that did successfully reproduce.
RESULTS
Which group members are breeding?
Parentage was determined for 145 offspring from groups with
sampled adults (91.2% of 159). Of these, parentage of 106
chicks (66.7% of 159) was determined with 95% confidence
and a further 39 chicks (24.5% of 159) with 85% confidence.
Of these 145 young, 95.2% were the progeny of the dominant
pair. Three subordinate individuals were assigned parentage
of a total of only 7 offspring (4.8%); in every case, subordinates reproduced with unrelated dominants. Of the 145 offspring, 72 (49.7%) were hatched into groups where the
dominant pair were the only unrelated opposite-sex pair in
the group and 73 (50.3%) into groups where there were alternate unrelated breeding partners for one or both dominants. Therefore, in groups where dominants could find
alternate partners, 9.6% of chicks (7 of 73) were extrapair.
Two subordinate females produced a total of 5 chicks. In
the first case, a subordinate female shared reproduction for
1 brood with her mother (the dominant female) and produced 1 chick. In the second case, a subordinate femaleshared reproduction with the unrelated dominant female
for 2 broods in 2 years with 2 different dominant males and
produced 2 chicks each year. Finally, 1 subordinate male cuckolded his father by fathering 1 brood of 2 chicks with a newly
immigrated dominant female. In no case did subordinates
breed together.
Fourteen chicks (8.8% of 159) could not be assigned
parents. An acknowledged difficulty in investigating cooperatively breeding systems is that other close relatives (siblings
etc.) are present in the pool of potential parents, thus
Behavioral Ecology
562
Table 1
F-statistics (FST, FIS, and FIT) calculated for the pied babbler
population over 5 years of study
Year
N
Groups FST
2003–2004 55 8
2004–2005 78 10
2005–2006 131 14
2006–2007 121 15
2007–2008 103 9
0.159
0.134
0.145
0.152
0.142
P
FIS
P
FIT
P
0.001
0.001
0.001
0.001
0.001
20.251
20.225
20.185
20.189
20.191
1.000
1.000
1.000
1.000
1.000
20.053
20.061
20.013
20.008
20.022
0.957
0.995
0.779
0.655
0.857
Values were calculated using analysis of molecular variation with
significance tested with 1000 permutations of the data set in
GENALEX 6.2 (Peakall and Smouse 2006).
confounding parentage prediction programs (Cockburn 1998;
McRae and Amos 1999). Thirteen of the unassigned chicks
had high match scores, but these matches were not significantly better than those of the second-best matches. In each
case, the dominant pair was one of the predicted sets of parents. Finally, parentage of 1 chick was assigned to a dominant
female with a neighboring dominant male (85% confidence).
The neighboring male and the group dominant male were
related to one another with R ¼ 0.57 and both matched to
the offspring. It is likely that the group dominant male was the
genetic father and the program chose the neighboring male
because of the high relatedness between the 2 candidates. In
support of this, the neighboring male was never observed in
a nonconfrontational association with the predicted mother.
How related are group members to one another?
Mean intragroup relatedness was 0.250 6 0.042 (N ¼ 19
groups). This ranged from –0.231 to 0.419 but was significantly greater than the population mean relatedness of
0.051 (95% CI ¼ 0.048–0.053), indicating that most groups
were highly kin structured. FST values were positive and highly
significant in each year (Table 1), indicating that groups consisted of kin. Mean relatedness between helping subordinates
and the chicks they provisioned was 0.38 6 0.01 (N ¼ 723
pairs from 15 groups). Mean relatedness between dominants
and subordinates was also 0.38 6 0.01 (N ¼ 596 pairs from 21
groups).
Does inbreeding occur?
In each year, both inbreeding coefficients (FIS and FIT) were
negative but nonsignificant (Table 1), indicating that there is
no systematic inbreeding within the population. The mean
relatedness of social (dominant) pairs (20.009 6 0.037;
N ¼ 37 pairs) was no different from the mean relatedness of
pairs that produced offspring together: this was usually the
dominant pair but in 4 cases was a dominant with a subordinate (0.018 6 0.038; N ¼ 31 pairs; 2 sample randomization/
permutation test, P ¼ 0.622). The mean relatedness of social
pairs was low and was not significantly different from the
mean relatedness of the member of each pair with all other
opposite-sex adults in the population in any year (2-sample
randomization/ permutation test, Figure 1). Dispersing pied
babblers chose mates that were neither more nor less related
to them than the population average. Nevertheless, the average relatedness between pairs (0.018) was an order of magnitude lower than the average relatedness within groups
(0.250).
Courtship between related adults was very rare. Courtship
was most commonly observed between the dominant pair
(85.1% of 242 observed courting interactions, N ¼ 19 groups).
Figure 1
Relatedness of mated and unmated pairs of opposite-sex adult pied
babblers per year over 5 years of study. Means 6 standard error of the
mean were generated from relatedness values calculated using the
Konovalov and Heg (2008) algorithm within the program
KINGROUP v2_090218 (Konovalov et al. 2004); sample sizes are
shown. A 2-sample randomization/permutation test with 100 000
permutations within the program RUNDOM PRO 3.14 (Jadwiszczak
2009) was used to calculate significance
In addition, however, courtship occasionally occurred between dominants and subordinates (12.8%) and, very rarely,
between subordinates (2.1%). Levels of relatedness strongly
predicted courtship behavior independently of social status;
adult courtship occurred most commonly between unrelated
group members (2-sample randomization/permutation test,
P , 0.001); mean relatedness was significantly lower between
courting (N ¼ 46) than between noncourting (N ¼ 480) adult
opposite-sex pairs.
What reproductive opportunities are available to
subordinates?
Overall, 40 individuals immigrated into non-natal groups
(Table 2). Twenty-seven adults immigrated into non-natal
groups and immediately became dominant with the result
that 24.2 6 5.5% of dominants (range 11.9–37.5%, N ¼ 4
years) were new immigrants in their groups each year. Over
the same period, 13 individuals (3 subadults and 10 adults)
immigrated into non-natal groups and became subordinate:
only 4.1 6 0.7% of subordinates lived in non-natal groups
each year (range ¼ 3.0–5.6%, N ¼ 4 years). Overall, adult
subordinates made up 41.6 6 9.5% (range 22.5–67.0%, N ¼
4 years) of group members. Immigration (usually of new, unrelated dominants) created opportunities for 34.1 6 1.7% of
these adult subordinates to breed with an unrelated adult
group member (range 30.3–37.5%, N ¼ 4 years). However,
while opportunities for adult subordinates to breed were relatively common, only a small fraction (12.5 6 7.4%) of these
potentially breeding subordinates actually successfully reproduced (range 0–33.3%, N ¼ 4 years).
DISCUSSION
Although many cooperatively breeding species have high
levels of extrapair paternity and subordinates commonly
breed within the group (Cockburn 2004), here we provide
evidence that in pied babblers monogamous dominant pairs
monopolize reproduction. Dominant pairs within groups
Nelson-Flower et al.
•
Monogamous dominant pairs in pied babblers
563
Table 2
Summary of immigration into non-natal groups and subordinate breeding opportunities created by immigration for 4 breeding seasons in the
pied babbler population
Year
2004–2005
2005–2006
2006–2007
2007–2008
Mean
Immigrant
dominants
7
28.0%
6
19.4%
5
11.9%
9
37.5%
24.2 6 5.5%
Immigrant
subordinates
Subordinates that
could breed
3
3
5
2
4.1 6 0.7%
8
10
23
6
34.1 6 1.7%
5.3%
3.0%
5.3%
2.8%
were socially monogamous (Raihani 2008) and almost completely sexually monogamous, with only rare instances of
successful reproduction by subordinates. Where extrapair
reproduction did occur, dominants bred with unrelated
group subordinates. However, subordinates generally gained
little or no direct reproductive success. This level of monogamy for both males and females is comparable to some other
cooperatively breeding birds, including laughing kookaburras (Dacelo novaeguineae—Legge and Cockburn 2000), Florida scrub-jays (Aphelocoma coerulescens—Quinn et al. 1999),
red-cockaded woodpeckers (Picoides borealis—Haig et al.
1994), and Arabian babblers (Turdoides squamiceps—Lundy
et al. 1998). In these species, as in pied babblers, groups
contain subordinate helpers which are not related to the
opposite-sex breeder but which very rarely reproduce, either
within the group or outside of it (reviewed by Cockburn
2004). Outside the group, breeding is likely limited by intense territoriality that severely restricts opportunities for
extra-group copulations (Quinn et al. 1999). Within pied
babbler groups, high reproductive skew is likely to be maintained by a combination of the inability of subordinates to
breed because of inadequate physical condition, inbreeding
avoidance, reproductive suppression of subordinates by
dominants, or mate choice by dominant females.
Inbreeding avoidance by subordinate pied babblers plays an
important role in sustaining the species’ high reproductive
skew. However, in many groups, subordinates did have access
to unrelated breeding partners but still did not breed, although they did engage in courtship behavior with these potential breeding partners. Reproductive skew in pied babblers
can therefore only partly be explained by inbreeding avoidance: other factors such as physiological or hormonal state
must also be involved in restricting subordinate reproduction.
Inadequate physical condition is one factor that can limit subordinate reproduction in cooperatively breeding groups
(Creel et al. 1992; Clutton-Brock et al. 2001). In pied babblers,
females with low body mass do not breed (Raihani 2008),
although there is no evidence that heavier subordinates more
often engage in courtship and other prebreeding behaviors
(Nelson-Flower 2010). Mate choice by dominant females is
likely to reinforce monogamy among pied babblers because
females appear to prefer the largest (thus almost invariably
dominant) males (Ridley AR, unpublished data). In general,
high skew among females is more common in avian than in
mammalian cooperative breeders, perhaps because of the relative ease with which a dominant female bird can prevent
a subordinate female from laying in a shared nest site
(Raihani and Clutton-Brock 2010). In pied babblers, interactions between competitive females at the nest during the dominant female’s fertile period are an important influence on
the division of reproduction (Nelson-Flower 2010). Aggressive
suppression of subordinate reproduction also works to maintain high skew; aggression regularly occurs between dominants and subordinates in cooperatively breeding species
(Taborsky 1985; Curry 1988; Emlen and Wrege 1992; Piper
32.0%
30.3%
36.5%
37.5%
Potential subordinate breeders
that did breed
1
0
1
2
12.5 6 7.4%
12.5%
0%
4.3%
33.3%
and Slater 1993; Cooney and Bennett 2000; Williams 2004;
Ratnieks et al. 2006; Young et al. 2006), including between
dominant and subordinate pied babblers of both sexes during
the fertile periods of dominant females (Nelson-Flower 2010).
Taken together, this evidence indicates that the primary
route to reproduction in pied babblers is through acquisition
of dominance. In terms of relative and absolute fitness, such
positions are therefore extremely valuable and strong selective
pressures are likely to be at work on traits that assist individuals
in gaining dominance. For example, phenotypic traits such as
plumage coloration can influence which individual becomes
dominant (Cockburn et al. 2008), as can physical size (Ciszek
2000; Clutton-Brock et al. 2006; Hodge et al. 2008, but see
Bolton et al. 2006; Spong et al. 2008). For pied babblers, large
body mass (Ridley et al. 2008) and age (Raihani et al. 2010)
have also been suggested to be important in acquiring a breeding position. For female pied babblers, aggression is likely to
be an important trait influencing the likelihood of gaining
dominance; some females gain dominance through aggressive
overthrow of dominant females in non-natal groups (Raihani
et al. 2010), and aggressive juvenile females are more likely to
attempt dispersal early in life (Raihani et al. 2008) increasing
their exposure to unrelated potential mates. Aggression may
be less important for males because they gain dominance
through founding a new group or filling a reproductive vacancy rather than supplanting an existing dominant (Raihani
et al. 2010).
The role of kin selection in the evolution of cooperative
breeding remains unresolved (Clutton-Brock 2002), but it
has recently been suggested that the rate of female promiscuity (and thus intragroup relatedness levels) has driven the
transition between cooperative societies and independent
breeding (‘‘the monogamy hypothesis,’’ Boomsma 2007,
2009). Lifetime genetic monogamy has been suggested to
be central to the evolution of helping behavior in eusocial
insects (Hughes et al. 2008) and shrimps (Duffy and
Macdonald 2010). Hatchwell (2009) and Cornwallis et al.
(2010) recently suggested that, in birds, close relatedness
and thus kin selection were important in the evolution of cooperative breeding. In pied babblers, mean relatedness values
and FST values indicate that groups were highly kin structured.
This high relatedness among subordinates reflects both the
strongly monogamous breeding system and the low immigration rate by unrelated subordinates. Most subordinates were
genetically linked to the current brood through at least one of
the dominant pair, with a mean relatedness to the chicks of
0.38. It is therefore likely that kin selection has played a role
in the evolution of cooperative breeding in this species, and
future work will address the question of the indirect benefits
gained by subordinate helpers. Whether such selection plays
an important role in the maintenance of cooperative behavior
in pied babblers is more difficult to discern, owing to the
confounding effects of the direct fitness benefits of helping
(e.g., cooperative sentinel calling—Hollén et al. 2008; Bell
et al. 2009). The direct fitness benefits of group living (Ridley
564
et al. 2008) could additionally or independently serve to maintain cooperative behavior in pied babblers. In general, it is
likely that ecological constraints and genetic relatedness
operated together during the development of sociality
(Cornwallis et al. 2010; West and Gardner 2010), and the same
is likely to be true for the evolution of cooperative breeding in
the pied babbler.
SUPPLEMENTARY MATERIAL
Supplementary material can be found at http://www.beheco
.oxfordjournals.org/.
FUNDING
Department of Science and Technology and National Research Foundation Centre of Excellence at the Percy FitzPatrick Institute for African Ornithology, University of Cape
Town (426078PFP1074).
We are grateful to Prof. T. Clutton-Brock for assistance in the initiation
and continuation of the Pied Babbler Research Project. The Northern
Cape Conservation Authority permitted research on pied babblers and
the Kotzes and the de Bruins kindly allowed us access to babbler groups
on their land. M. Bell, K. Bradley, K. Golabek, J. Oates, A. Radford, R.
Rose, and H. Wade helped with maintaining habituation of babbler
groups. Dr D. Dawson at the Sheffield Molecular Genetics Facility
(University of Sheffield) very kindly provided test primers. J. Bishop,
N. Coutts, and N. Muna helped with technical advice in the laboratory. Useful comments and discussion were provided by T. Flower, M.
Bell, N. Jordan, D. Lukas, A. Radford, and S. Sharp. The comments of
2 anonymous reviewers greatly improved the manuscript. Prof. N.
Davies at the University of Cambridge hosted M.J.N.-F. as an academic
visitor while writing this paper. Fieldwork received ethical clearance
from the University of Cape Town’s Animal Ethics Committee.
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