(? Springer-Verlag1997
Behav Ecol Sociobiol (1997) 40: 261-270
Linda A. Whittingham Peter 0. Dunn
Robert D. Magrath
Relatedness,polyandryand extra-grouppaternity
scrubwren
white-browed
in the cooperatively-breeding
(Sericornisfrontalis)
Received:21 May 1996 / Accepted after revision: 14 December 1996
Abstract We used DNA fingerprinting to examine the
genetic parentage and mating system of the cooperatively breeding white-browed scrubwren, Sericornis
frontalis, in Canberra, Australia. Our analyses revealed a
remarkable variety of mating tactics and social organization. Scrubwrens bred in pairs or multi-male groups
that consisted of a female and two or more males. Females were always unrelated to the pair male or alpha
(dominant) male. Among multi-male groups we found
three different mating tactics. Firstly, when alpha and
beta (subordinate) males were unrelated, they usually
shared paternity in the brood. This resulted in both
males gaining reproductive benefits directly. Secondly,
when beta males were not related to the female but were
related to the alpha males, beta males sired offspring in
some broods. In this situation, beta males gained reproductive benefits both directly and potentially indirectly (through the related alpha male). Thirdly, when
beta males were related to the female or both the female
and alpha male, they remained on their natal territory
and did not sire any offspring. Thus beta males gained
only indirect reproductive benefits. Overall, when group
members were related closely, the dominant male monopolized reproductive success, whereas when the
members were not related closely the two males shared
paternity equally. This positive association between
monopolization of reproduction and relatedness is predicted by models of reproductive skew, but has not been
reported previously within a single population of birds.
Other cooperatively breeding birds with both closely
L.A. Whittingham P.O. Dunn R.D. Magrath
Division of Botany and Zoology,
Australian National University, Canberra,ACT 0200, Australia
L.A. Whittingham(M) P.O. Dunn
Departmentof Biological Sciences, Lapham Hall,
P.O. Box 413, University of Wisconsin-Milwaukee,
Milwaukee, WI 53201, USA
Tel.: 414-229-2252;Fax: 414-229-3926:
e-mail: whitting(a_
csd.uwm.edu
related and unrelated helpers may show a similar variety
of mating tactics. Finally, we found that extra-group
paternity was more common in pairs (24% of young)
than in multi-male groups (6%), and we discuss three
possible reasons for this difference.
Key words Cooperative breedingDNA fingerprinting*Reproductive skew
Mating systems* Kin selection
Introduction
Genetic studies of cooperatively-breeding species of
birds have shown that individuals can gain reproductive
success both directly (through descendent kin) and indirectly (through non-descendent kin). Subordinate
males in cooperative groups can gain direct success
through shared paternity within groups, extra-group
fertilizations, or both (Rabenold et al. 1990; Davies
1992; Jamieson et al. 1994; Millar et al. 1994; Mulder
et al. 1994; Dunn et al. 1995; Faaborg et al. 1995).
Subordinates of either sex can gain indirect success
through helping related breeders increase their production of young or by increasing the survival of related
breeders (e.g. Joste et al. 1985; Wrege and Emlen 1987;
reviews in Brown 1987; Emlen 1991). These two categories are not exclusive, as helpers may gain both indirect and direct reproductive success. To date, however,
few studies have reported situations where helpers
commonly gain both direct and indirect reproductive
benefits (e.g. Piper and Slater 1993; Haydock et al.
1996).
Systems in which there is variation in relatedness
among adults allow tests of predictions of models of
reproductive skew, which is the "distribution of direct
reproduction among individuals" (reviewed in Keller
and Reeve 1994). At one extreme, one individual dominates reproduction (high skew), while at the other, reproduction is shared equally (low skew). Vehrencamp
262
(1983) suggested that both relatedness and ecological
constraints will affect the degree of reproductive skew
within societies. When subordinates are closely related
to the dominant breeding adults and there are constraints on successful dispersal, the dominant group
member(s) may be able to monopolize most of the
breeding (a despotic society). A high reproductive skew
results because subordinates achieve indirect benefits
from assisting kin (relatedness) and subordinates may
have little alternative because of limited breeding territories (ecological constraints). At the other extreme,
when subordinates are unrelated to the dominant
breeding adults and have a high probability of successful
dispersal to high-quality breeding sites, Vehrencamp's
model predicts a more equitable distribution of reproduction within the group (e.g. egalitarian groups with
unrelated helpers). Dominants should share breeding
opportunities with helpers because they may disperse if
not given the opportunity to breed (Vehrencamp 1983).
Most cooperative species of birds studied to date have
generally shown one or the other of these two types of
breeding systems.
Intraspecific variation in relatedness in multi-male
groups should also affect reproductive skew, assuming
that dispersal options are not associated with relatedness. In fact, some studies have found that subordinate
males in bird and mammal societies are more likely to
gain paternity if they are less closely related to the
breeders (Packer et al. 1991; Piper and Slater 1993;
Keane et al. 1994).
We studied white-browed scrubwrens (Sericornis
frontalis), which have been reported to breed cooperatively (Bell 1983; Ambrose and Davies 1989). In our
study population, social groups consist of a breeding
female and one or more males, and most subordinates in
multi-male groups are philopatric sons who remain on
their natal territory (R. Magrath, unpublished work
1992-1996). Nevertheless, some subordinate males are
immigrants unrelated to the original residents, and the
death and replacement of the original female can mean
that the breeding female is unrelated to both the dominant (alpha) and subordinate males (R. Magrath unpublished work). Thus family groups in this species
contain both males and females that may be either
closely related or unrelated. We used multilocus DNA
fingerprinting to examine the genetic mating system and
the relatedness of adults within multi-male groups. We
also determined the frequency of extra-group paternity
in pairs and groups. Extra-group paternity is potentially
important, as it could affect reproductive success of
males within groups, the payoff to subordinate males of
remaining in a group, and the relatedness of members
within groups. We use these results to examine the importance of kin selection in maintaining philopatry by
subordinate males.
Methods
Study site and species
White-browedscrubwrensare small (11-15 g), insectivorous passerines(Family Pardalotidae;Sibley and Ahlquist 1990) that occur
commonly in habitats with dense undergrowth in southeastern
Australia (Christidis and Schodde 1991). The species apparently
breeds cooperatively on permanent all-purpose territories (Bell
1983; Ambrose and Davies 1989), but little is known about the
details of the social system.
During the 1992 and 1993 breedingseasons we studied a population of scrubwrensresident at the AustralianNational Botanic
Gardens. a 40-ha reserve of native vegetation in Canberra, Australia. We caught and uniquely color-banded all adults and offspring on about 50 territories.Territorialsocial groups were pairs
or multi-male groups consisting of one female, a dominant male,
and up to four subordinatemales. We determinedthe dominance
status of males from daily observations of male chases and displacements during the breeding season. Dominance was stable
among breeding attempts within a season and from year to year,
and older males were more dominant. All individuals acquired
adult plumage before the breedingseason following hatching, and
there were no obvious differencesin appearanceamong males of
differentage or status. We refer to dominant males as alpha males
and the most dominant subordinatemales as beta males. Females
always dispersed from their natal group, and so breeding females
were unrelatedto the dominant males (see below).
Over the 2 years of the study, therewere 108group-years,which
is the number of different seasons each social group attempted
breeding,summedover groups. When one or more of the potential
breeders (female, alpha or beta male) changed between breeding
attempts we consideredthis a differentsocial group. In our sample,
alpha or beta males changed between breeding attempts in three
groups, and in two other cases females bred in a pair and then in a
multi-male group. Of the 108 group-years,44% were pairs, 46%
weregroups with two males, and 100%weregroups of threeor more
males. On average,males made up 64% of the adult population in
each year.
Scrubwrensbred in the Botanic Gardensfrom July (mid winter)
to January(mid summer).Females laid up to six clutches (93% of
clutches contained three eggs) and fledged up to three broods
during a season, although many nests were lost to predators. Females built the nest and incubated alone. The mean incubation
period was 18.5 days, and nestling period 15 days. Males fed the
female during the presumedfertile period and through incubation.
Young were fed by males and females in the nest and for up to 8
weeks after fledging.
DNA fingerprinting
We determinedpaternityfor 137 nestlings, of which 50 were from
19 broods of 13 pairs and 87 were from 32 broods of 18 multi-male
groups. In our analyses, seven pairs contributedone brood and six
pairs contributed two broods, while nine multi-male groups contributedone brood and nine multi-malegroups contributedtwo or
more broods (Z2 = 0.05, 1 df, P = 0.83). The mean size of broods
for which we had paternity data was 3.0 ? 0.05 (SE) young for
pairs and 3.0 ? 0.06 young for multi-malegroups. The paternityof
15 nestlingscould not be determinedbecause there was insufficient
DNA.
Blood samples (20-70 pl) used for DNA fingerprintingwere
suspendedin Queen's lysis buffer(Seutin et al. 1991) and stored at
4?C prior to analysis. Our DNA fingerprintingproceduresfollowed
Mulder et al. (1994). Briefly, we digested 8 ,ug of genomic DNA
per individual with Hae III and added 6 ng of a molecular sizemarkerto each sample. Samples were subjectedto electrophoresis
at 2 V/cm through a 40-cm (0.80%) agarose gel for 45-50 h. Following electrophoresis,DNA was transferredby Southernblotting
onto Immobilon-N or Hybond-N+? membranes. All membranes
263
were hybridizedseparatelywith radioactivelylabeled per (Shin et
al. 1985), 33.15 (Jeffreyset al. 1985) and the DNA molecular sizemarkerto produce three separate autoradiographs.The molecular
size markersin each lane allowed us to correctfor distortionsin the
migration of DNA fragmentsacross the gel.
DNA fingerprintswere scored following methods in Westneat
(1990) and Lifjeld et al. (1993). The average number of scorable
fingerprintbands in the 2.5-30 kb range was 17.3 i 6.4 for per and
12.7 i 5.5 for 33.15. Parentage was determined using a two-step
procedure.First, we examined each nestling for fingerprintbands
that were not present in either putative parent (novel fragments,
Westneat 1990). Thus, novel fragments were inherited from individuals other than the putative parents or resultedfrom mutation.
Nestlings were excluded as the progeny of a particularset of putative parents if their fingerprint profile contained more novel
fragmentsthan expected from mutation (in our case two or more
for both probes combined;Fig. 1). In this study the mutation rate
was 5.6 per 1000meiotic events which was similarto the rate found
in other species of birds (Burke and Bruford 1987;Westneat et al.
1990). The probability that a scrubwren nestling would have a
particular number of mutant bands can be estimated from the
number of mutant bands per individual and the Poisson distribu-
tion (Burke and Bruford 1987). In our case the probability that a
scrubwrennestling would have one or two mutant bands was 0.085
and 0.004, respectively.Therefore,nestlingswith two or more novel
fragmentswere unlikely to have acquiredthem from mutation, and
we considered these nestlings unrelated to one or both of their
putative parents. Second, we used the proportion of bands shared
(Wetton et al. 1987)betweeneach nestling and each of the adults in
its group to determine if the nestling was related to the putative
mother or either of the males in the group. Based on the lower 99%
CI (one-tailed) for band-sharingbetween mothers and unexcluded
nestlings (mean of both probes ? SD = 0.509 ? 0.074, n = 103),
we excluded nestlings from putative parents when they had two or
more novel fragments and their mean band-sharingwas < 0.330
(Fig. 1). We assigned paternityto males when they shared > 0.330
of their bands with a nestling and there was one or no novel
fragments(Fig. 1).
We used band-sharingbetween adults within social groups to
determine their relatedness. We considered two individuals to be
"unrelated"if their band-sharingwas < 0.330. Band-sharingbetween putatively unrelated individuals (females and their mates)
averaged0.169 ? 0.061(? SD, n = 13) for pairs and 0.174 ? 0.087
for femalesand alpha males in their group (n = 16 femalesbreeding
Pairs
Groups
I
.8
Female
.7-Q
.6-
0
75
00
'U0
^"
7
0
0
.61
00
0
04,
65
0
~0
.
00
000
? 00
X
0
0
~~~~~~~~~~~~~~~.3
~~~~~~~~~~~~~~~.2-
.3.2-
.1
.10
2
O
V .8
X
Female
00
0
6
00
.4-
_
I
.8
4
6
8
10
12
14
18
16
C~~~~~~~~~~~~~
.7
Putative father
i
.8-
8 I
0
0
I
I
.1
0
0
.3
.6
.5
1
.33
.2 .6
24
0
000o
5
15
10
25
20
0
1
1
0 41
o0
0
0
0
68101o2114
Alpha male
I
~~~~~~~~~~~~~~~~.7
6
.4
.4-
0
.9
,
L
0
S
.3
.2m0
.1-
14
IO 0
00
0
1618
o
0
5
0
.8-..7
.5.4.
0O
~o'g8o
5183o
F8
8
-
08
20
15
10o
0
I -o - 0
-
-
-
25
-
-
Beta male
0
0
0
0
0
-
.2
8
.1
I
00
1000
0
2
0
0000
00
0.
Novel fragments
.0 o
1
00 00
0
00
0
0
0 0
5
10
0
15
20
25
Novel fragments
Fig. 1 Band-sharing(mean from both probes) in the white-browed
scrubwrenbetweenoffspringand theirputativeparentsin relationto
the total numberof novel fragments(both probescombined)for pairs
(left) and multi-malegroups (right).We consideredyoung that had
fewer than two novel fragments(verticallines)with a set of putative
parentsand band-sharing> 0.330 (horizontallines)with each parent
to be the progenyof those parents(see Methods for statistics).For
multi-male groups, the number of novel fragments in the upper
(female)and middle(alphamale) boxes were based on a comparison
of offspringwith the female and the alpha male as putativeparents;
whereas,in the lowerbox (beta male) the numberof novel fragments
for offspringwas based on the female and the beta male as putative
parents."Novel fragments"can come from mutations,the othermale
in the social group or an extra-groupmale. Note that for beta males
there was high band-sharingfor some offspringeven though there
were at least three novel fragments,becausein all of these cases the
beta male was the son of the femaleand alpha male (i.e. a firstorder
relative of both the parents and most offspring).See Fig. 2 for a
breakdownof beta male band-sharingby type of group
264
with different alpha males). The upper 99% CI (one-tailed) for
band-sharingbetweenall females and their mates was 0.346, which
representsan upper limit for band-sharingbetween unrelated individuals. Thus, we considered two individuals to be "related" if
their band-sharingwas > 0.346. In our sample there were no cases
where band-sharingwas between0.330 and 0.346, so all individuals
within a social group could be classifiedas "related"or "unrelated"
to each other. Birds with intermediate levels of relatedness (e.g.
second or third order) probably occur among adults within social
groups, but we could not discern these finer levels of relatedness
with our data (see Piper and Rabenold 1992).
In scrubwrens the use of the term "extra-pair paternity" is
problematical,because scrubwrensbreed in multi-male groups in
which the female has social bonds with dominant and subordinate
males. Thus young sired by a beta male are not "extra-pair"from
the female's perspective, only from the alpha male's perspective.
For clarity, we do not use the term "extra-pairpaternity"to refer
to paternity by the beta male, and we refer to paternity by males
outside a social group of any size as "extra-grouppaternity".
We used the mean reproductivesuccess of females breedingin
pairs versus multi-male groups to provide an estimate of the indirect reproductivebenefits to males of breeding on their own in a
pair versus remainingin their natal territoryas a non-breedingbeta
male (Brown 1987). We only included females in the analysis if:
(1) the female bred in the same group size for all breedingattempts
within a season, (2) the female was monitored closely so that all
nests producing fledglings were found, (3) the number of young
fledgingwas known for every breedingattempt, and (4) the female
was in a breeding group from early in the breeding season (by
August at the latest;the modal month of initiation of firstclutches).
If we had data from two seasons for the same female in the samesized group, we used the mean seasonal reproductivesuccess.
Results
Types of multi-malegroups
We classified groups according to relatednessamong
adults, which was determined from the mean bandsharing of both probes (see Methods, Fig. 1). In all
groups, the alpha male was unrelatedto the breeding
female [mean (? SD) band-sharing- 0.174 ? 0.087;
range= 0.036 - 0.311, n 16 groups with differentfemales and alpha males].However, there was variability
in whetheror not the beta male was relatedto the other
adults in the group, so we classifiedgroupsaccordingto
the relatednessof the beta male to the dominantpair.
We foundfourtypesof multi-malegroups:(1) in seven
of 18 groups,the beta male was relatedto the alphamale
(band-sharing 0.511 ? 0.064;range - 0.444 -0.582)and
female (0.511 ? 0.053, range = 0.452-0.610); (2) in one
group, the beta male was the son of the female (0.616),
but he was not relatedto the alpha male (0.320);(3) in
five groups the beta male was relatedto the alpha male
(0.520 ? 0.104, range- 0.397-0.610), but not to the
female (0.157 ? 0.131; range 0.048-0.304), and (4) in
five groups the beta male was not related to either the
alpha male (0.164 ? 0.093, range= 0.066-0.285) or to
the female (0.183 ? 0.092, range = 0.043-0.296).In 3 of
18 multi-malegroups there was a third male who was
subordinateto the beta male;however,none of the these
males gained paternityand they shall not be considered
further.
Paternity within multi-male groups
In groups, the alpha male sired 76% (66/87) of the
nestlings, siring at least one young in 97% (31/32) of
broods and all of the young in 5900 (19/32) of broods.
Of the 21 nestlings not sired by the alpha male, 16 were
sired by the beta male (Fig. 2) and 5 were sired by unknown extra-group males (Table 1). The beta male
gained paternity in 31% (10/32) of broods.
Beta males gained a greater share of paternity in
groups in which they had a lower potential indirect
benefit from helping breeders to reproduce (Fig. 3). The
beta male gained paternity in seven of nine broods in
which he was unrelated to both the alpha male and the
female (Table 2). Beta males that were related to the
alpha male but not the female shared paternity with
their father in three of ten broods. There was no evidence of beta male paternity (i.e. inbreeding) when the
beta male was the son of the female (Table 2). In cases
where alpha and beta males were related we could exclude one or the other male as a potential sire because
one of them always had at least two novel fragments and
band-sharing less than 0.330 with the young.
Extra-group parentage and the number of mates
Overall, 12% (17/137) of nestlings in 24% (12/51) of
broods were sired by extra-group males (Table 1). The
percentage of extra-group young was significantly higher
in pairs (24%; 12/50 nestlings) than in multi-male
groups (6%; 5/87 nestlings; x
9.7, ldf, P = 0.002).
Similarly, the percentage of broods with extra-group
young was greater for pairs (42%; 8/19) than multi-male
groups (130%; 4/32; x2- 5.8, l df, P -0.02; Table 1).
Using individual social groups as the unit of analysis
produced similar results: extra-group paternity was
more likely among offspring of pairs (62%, 8/13 pairs)
than multimale groups (22%, 4/18 multi-male groups;
z2= 4.9, Idf, P = 0.03). Among pairs, the male sired
at least one nestling in 9000 (17/19) of broods, and
among multi-male groups alpha males sired at least one
nestling in 970o (31/32) of broods. Extra-group paternity
was less frequent than shared paternity in multi-male
groups and so sample sizes were too small to reveal
whether the frequency of extra-group paternity differed
among multi-male group types (Table 2).
Considering all sources of paternity, both within and
outside the social group, the percentage of broods with
multiple sires was similar for pairs (32%; 6/19) and
multi-male groups (410%; 13/32; C' 0.42, ldf, P 0.52). Both alpha and beta males sired young in 9 of the
13 multiply sired broods of multi-male groups; we found
no broods in which alpha, beta and extra-group males
all sired young. We found no evidence of intraspecific
brood parasitism (i.e. nestlings unrelated to the resident
female; Fig. 1).
265
.1.
.12
0
.7
.6
0
15080
-I
.32 3
c
o
.5
0
0
-
-
-
-
-
-
I
I
.4-
0
l
Beta male related
to female, unrelated
to Alpha
.7
.6?
???0
I000
.4-
Beta related to Alpha
and female
0
I
-
-
.3
-
-
0
-
-
-
-
-
-?
.3
.2
.2
M
0.
5
?
U
X
;
I
al
.
.7-
Ito
.6
.5
10
15
Beta male related
Alpha, unrelated
to female
.6
~~~.400~~~~~~~~~~~~~
.4
1
.3
18
0
5
25
i
?
?
l
-I
.
0
0
i
.5
0
20
Beta unrelated to
both Alpha and female
.7
0
15
10
I
.8
*i
5
0
25
20
- - - - - -
.2-
.1
0
10
*
15
0
~~
~~~~0
0 0
0
25
20
5
0 0
10
15
20
25
Novel fragments
Fig. 2 Band-sharing(mean from both probes) in the white-browed
scrubwrenbetweenoffspringand the beta male in relationto the total
numberof novel fragments(both probes combined)for each of the
four types of groups(note that thesewerecombinedin Fig. 1). Novel
fragmentsare based on the femaleand beta male as putativeparents
in all four boxes. Filled circlesrepresentnestlingssired by the beta
male, open circles representnestlings sired by the alpha male and
diamondsrepresentnestlingssiredby a male from outsidethe group.
See Fig. 1 for an explanationof the verticaland horizontallines.The
relativelyhigh band-sharingin the upperrightpanel is likely due to
some degree of relatedness(less than first-order)betweenthe alpha
and beta males
Direct reproductivebenefits
Fig. 3). Thus, the best situation for the alpha male in
terms of fertilization success within a group was the
The reproductivebenefits for males breedingin multi- worst situationfor the beta male, and the best situation
male groups depended on the type of group. Alpha for the beta male (living with an unrelatedalpha male
males fathered the most young in two types of multi- and female)was the worst for the alpha male.
male groups:(1) the beta male was relatedto both the
female and alpha, in which case the alpha male sired
2.8 + 0.2 [SE] nestlings per brood (n = 12 broods) and Indirectreproductivebenefits
(2) the beta male was relatedonly to the female,in which
case the alpha male sired 3 nestlings (n = 1 brood). In Potential indirect benefits can be estimated from the
contrast, alpha males sired the fewest young (1.3 ? 0.2 differencein reproductivesuccess between multi-male
nestlingsper brood, n = 9 broods) when they lived with groups and pairs (Brown 1987). These indirectbenefits
a beta male that was unrelatedboth to the alpha male may be sufficientto favor beta males that remain on
and female (Fig. 3). When alpha and beta males were their natal territoryratherthan disperseand breed on
unrelated to each other and to the female they had their own in a pair. In the following analyses,we estisimilar fertilizationsuccess (U 42, P = 0.89; Fig. 3). mated the maximum indirect benefits to beta males of
For beta males, fertilizationsuccess was greatestwhen remainingin their natal group.
they lived with an unrelated alpha male and female
Females breedingin multi-malegroups had a higher
(1.2 ? 0.3 nestlingsper brood, n - 9 broods),and fewest mean seasonalproductionof fledglings[3.3 ? 0.44 (SE);
when they lived with a relatedfemale(no nestlingssired; n = 34 female-groups] than did those in pairs
Table 1 Paternityof white-browedscrubwrenbroods and nestlings, 1992 and 1993. "Extra-group"refersto young sired by males outside
the social group
Pairs
Multi-male
groups
All
% Broods (n) with one or more offspring sired by
% Nestlings (n) sired by
Alpha male
Beta male
90% (17)
97% (31)
31% (10)
94% (48)
Extra-group
male
Total
n
Alpha male
Beta male
42% (8)
13% (4)
19
32
76% (38)
76% (66)
18% (16)
24% (12)
51
76% (104)
Extra-group
male
Total
n
24% (12)
6% (5)
50
87
12% (17)
137
266
la 20T
0.....
....0
0&
Pairs
(N= 19)
Alpha Beta
Betamale
relatedto
Alphamale
andfemale
Alpha Beta
Betamale
unrelated
to Alphamale,
relatedto female
(N= 1)
(N= 12)
Alpha Beta
Betamale
relatedto
Alphamale,
to
unrelated
Alpha Beta
Males
unrelated
to each other
andto female
female
(N= 9)
(N= 10o)
Fig. 3 Mean number(+ SE) of young siredper brood for malewhitebrowed scrubwrensliving in pairs and in four types of multi-male
groups. Samplesizes indicatethe numberof broods. Althoughextragroup paternityoccurredmore often in pairs than groups (Table 1),
males in pairs sired as many young per brood (2.0 ? 0.2, n = 19
broods) as alpha males in all types of groups (2.1 ?
0.2, n = 32 broods; U = 308, P = 0.95). This occurred because
alpha males also shared paternitywith beta males in 31% (10/32)
of broods(Table 1). Overall,beta malessiredfeweryoung (0.5 ? 0. 1,
n = 32 broods) than either alpha males (U = 894, P < 0.001) or
pair males (U = 521, P < 0.001). Numberof young siredper brood
varied with group type for both alpha (Kruskal Wallis
H = 13.2, 2 df, P= 0.001) and beta (H = 13.8, 2 df, P = 0.001)
males (maleslivingin a multi-malegroup in whichthe beta male was
relatedto the femalewerecombinedinto one group for this analysis)
(2.9 ? 0.40, n = 25 female-groups).Thus, a male that
breeds in a pair produces a total of 2.9 fledglingsper
season, and on average2.2 of these fledglingsare related
(r = 0.5) offspringand 0.7 are unrelated(r = 0.0) young
resulting from extra-group fertilization (24%). The
productionof gene-equivalentsis thus 1.1 (i.e. 2.2 x 0.5
gene-equivalentsper young). If this male instead remained as a subordinatewith both parents, the total
production of fledglingsover the season would be 3.3
full sibs (r = 0.5; Table 2). We assumehere that the lack
of observedextra-groupyoung in groups in which the
beta male is relatedto both parentsis due to the presence of the beta male. If the son dispersed,his parents
would produce, from the disperser'spoint of view, 2.2
full sibs (r = 0.5) and 0.7 half-sibs (r = 0.25; half-sibs
are the result of 24% extra-groupfertilizations).Thus,
the overall benefit of remainingwith his parents is 0.4
gene-equivalents[i.e. (3.3 - 2.2) x 0.5 gene-equivalents
per full sib +(0.0 - 0.7) x 0.25 gene-equivalentsper
half-sib]. Overall, a male produces 0.7 more geneequivalents(1.1 - 0.4) by breedingin a pair ratherthan
remainingwith his parentsas a subordinatehelper.
Table 2 Paternityof white-browedscrubwrenbroods and nestlings in four types of multi-malegroups, 1992 and 1993
% Broods (n) with one or more young sired by
Type of
multi-malegroup
Extra-group Total
male
n
Alpha male
Beta male
Beta male is related
to alpha male and
female
100% (12)
0% (0)
0% (0)
Beta male is related
to female, but not
to alpha male
100% (1)
0% (0)
Beta male is related
to alpha male, but
not to female
90% (9)
100% (9)
Beta male is not
related to alpha
male or female
% Nestlings (n) sired by
Extra-group
male
Total
n
Alpha male
Beta male
12
100% (34)
0% (0)
0% (0)
34
0% (0)
1
100% (3)
0% (0)
0% (0)
3
33% (3)
33% (3)
10
66% (17)
19% (5)
15% (4)
26
78% (7)
11% (1)
9
50% (12)
46% (11)
4% (1)
24
267
Discussion
The white-browedscrubwrenexhibits a remarkablevariety of mating tactics. In our population, the most
common breeding arrangementwas a pair or group
consisting of a female and two males. Among the four
different types of multi-male groups (see above) we
found three differentmating strategies:(1) when beta
malesweresons of the female(eitherrelatedor unrelated
to the alpha male) and they remained on their natal
territoryas helpers, they did not gain paternitywithin
the group; (2) when beta males were not relatedto the
female but were sons of the alpha males, beta males
gained paternity in some broods, and thus gained reproductive benefits both directly and potentially indirectly (through their father); and (3) when alpha and
beta males were unrelatedthey usually sharedpaternity
in the brood, and thus, both males gained reproductive
benefits directly. Finally, scrubwrensalso bred in socially monogamouspairsin which extra-grouppaternity
was fairly common. Although each of the forms of
mating and relatedness that we have discovered in
scrubwrenshas been describedpreviouslyin birds, the
simultaneousand common occurrenceof this variation
in one species is so far rare.
Reproductiveskew
Models of reproductiveskew assume that dominantindividualscontrol the reproductionof subordinates,and
high-skewsocieties are called "despotic"(Vehrencamp
1983;Keller and Reeve 1994;Emlen 1995). Dominants
can afford to be despots towards subordinatesthat are
close relatives because the subordinateshave limited
breedingopportunitiesand gain some fitnessby helping
dominantsto breed. In contrast, "egalitarian"societies
are those in which reproductionis shared(low skew). A
societyis likelyto be most egalitarianwhen subordinates
are unrelatedto dominantsand have other options, such
as a high chance of gaining a dominant breedingsituation. Most cooperative species studied to date have
fallen into one or the other of these two types of
breedingsystem (see also Hartley and Davies 1994). In
contrast, white-browedscrubwrensbreed in both despotic and egalitariangroups.
Egalitarian groups with shared paternity between
unrelatedmales seem to be quite rarein birds and have
only been confirmedby geneticanalysesin a few species
(Emlen 1995). For example, unrelatedmales share paternityfairly equallyin polyandrousgroups of pukekos
(Porphyrioporphyrio,Jamiesonet al. 1994), Galapagos
hawks (Buteogalapagoensis,Faaborg et al. 1995), dunnocks (Prunellamodularis,Burkeet al. 1989)and brown
skuas (Catharactalonnbergi,Millaret al. 1994).If death
and dispersal of individualscommonly introducesunrelated individualsinto groups, then egalitariangroups
with sharedpaternitymay occurmore frequentlythan is
currentlyrealized.
Despotic groupsappearto be the most common type
among cooperatively-breedingbirds. In most species
helpers are the previous offspringof the breedingpair,
and thus they can gain indirectbenefits from assisting
close kin (Brown 1987; Hartley and Davies 1994). To
date, however, few genetic studies have been made of
this "classical"type of cooperativebreeding.If extragroup paternityis common, then indirectbenefitsmay
be much lower than estimated previously (e.g. Dunn
et al. 1995). Nevertheless,recent studies generallysupport the traditionalview that helpersare geneticallyrelated to the young they assist (e.g. Emlen and Wrege
1988;Rabenoldet al. 1990;Haig et al. 1993, 1994;Gibbs
et al. 1994),and thus helperscan gain indirectbenefitsif
theirassistanceimprovesthe reproductivesuccessof the
group (Grafen 1984). These studies also indicate a
strong bias toward one male dominatingpaternity,as
would be expectedin despotic groups.
The pattern of paternity and relatednessin scrubwrens is consistentwith Vehrencamp'smodel of reproductive skew (Vehrencamp1983). As predicted for a
despotic system, alpha males sired all or most of the
young when their son lived in their group, but males in
multi-male groups shared paternity when they were
unrelated,as predictedfor an egalitariansystem. This
positive association between relatednessand reproductive skew has been describedin intraspecificstudies of
some mammals (Packer et al. 1991; Creel and Waser
1994).Thereis a similarpatternin the pukeko,although
the comparison involves differentpopulations;in one
population multi-male groups were composed of kin,
while in the otherpopulationindividualswere unrelated
(Jamiesonet al. 1994). Other species with some similarity to scrubwrensinclude dunnocks (Burke et al.
1989) and stripe-backed wrens (Campylorhynchus nu-
chalis, Rabenold et al. 1990; Piper and Slater 1993).
Although dominant males sometimes share paternity
with subordinatesin these species,in most cases the beta
males are either unrelated (dunnocks;egalitariansystem) or related(stripe-backedwren;despotic system)to
the alpha male. Unrelatedmales in groups occur occasionallyin stripe-backedwrens(Piperet al. 1995),but it
is not clear how often these males share paternity.Although the pattern of shared paternity in scrubwren
multi-malegroupsis consistentwith previousmodels of
reproductiveskew, it is unclearif dominantscan control
the reproductionof subordinates,which is a criticaland
as yet untestedassumptionof these models.
In most cooperative birds with multi-male groups
there appears to be a trade-offfor males between paternitylost to other group members,and other benefits,
such as increasedproductionof close kin (e.g. Rabenold
et al. 1990; Gibbs et al. 1994;Poldmaa et al. 1995) or
group defense of a breedingterritory(Jamiesonet al.
1994). However, the outcome of this tradeoff is not
simple,becauseit can also be influencedby a conflictof
268
interestsbetween the female and her mates. For example, female dunnocks have higher reproductivesuccess
in cooperatively-polyandrousgroups than in pairs because they receive more male parental care, whereas
male dunnocks have higher reproductivesuccess when
they are monogamous or polygynous, because they do
not have to share paternity (Burke et al. 1989). This
conflict of interestbetweenthe sexes adds another level
of complexityto previousmodels of reproductiveskew,
and it likely reduces the overall level of reproductive
skew by dominants(Vehrencamp1983).
Extra-grouppaternity
Scrubwrenshad an intermediatelevel of extra-group
paternity(12% of young) comparedwith the few other
cooperativebreedersin which paternityhas been studied. The incidenceof extra-groupfertilizationin cooperativebreedersspans the rangefor birdsas a whole. At
one extreme, very low levels of extra-grouppaternity
(K 1%) have been reportedfor stripe-backedwrensand
red-cockadedwoodpeckers(Rabenoldet al. 1990;Haig
et al. 1993, 1994). At the other extreme are the fairywrens (Malurusspp.), which have the highest known
levels of extra-group paternity (60-76% of young;
Brooker et al. 1990; Mulder et al. 1994). Overall, the
incidenceof extra-grouppaternityin scrubwrensis similar to that for non-cooperativebreeders(mean= 17%
extra-pairyoung; Dunn et al. 1994).
Extra-grouppaternityin scrubwrensis more frequent
in pairs than in multi-malegroups (Table 1). The interpretationof this pattern will depend on whether females or males are ultimatelyshown to be responsible
for paternity.We have not seen extra-groupcopulations,
or as yet assignedpaternityin cases of extra-grouppaternity, so we simply suggest three possibilities. First,
females may seek extra-groupcopulations to gain superior genotypes for their offspring.Females in multimale groups may not seek extra-groupcopulation as
often becausethey are able to choose among more than
one potentialmate on their own territory(i.e. the alpha
and beta males). Of course, beta males that are sons
would not offer females greater genetic diversity of
mates,and, thus, we shouldexpectrelativelymore extragroup fertilizationsin this type of multi-malegroup. We
detected no variation in the incidence of extra-group
paternity across different types of multi-male groups,
but our sample sizes are currentlytoo small to exclude
such variation;if anything, the trend went against this
hypothesis (Table 2). Alternatively, females may be
mating with several males for each clutch to ensure
fertilizationof their eggs. Consistentwith this idea, we
found that the frequencyof clutcheswith multiplesires
(regardlessof type) was similarfor femalesin pairs and
multi-malegroups.Second,if mate guardingis relatedto
paternity,then two males in a group may be better at
guardingtheir female than one male in a pair. Both alpha and beta males in all types of multi-malegroups
would have lower reproductivesuccessif offspringwere
siredby unrelatedextra-groupmales.Thus, thereshould
be no differencesin the incidenceof extra-groupfertilization across differenttypes of multi-malegroups. If
philopatric sons reduce the incidence of extra-group
paternity,then this would be a novel form of helping.
Third, if extra-groupmales are responsiblefor the pattern of paternity,then it implies that siringextra-group
young has a greaterbenefitto maleswhen the young are
siredin pairsthan in multi-malegroups.This is possible
if the average time to gaining a breeding vacancy is
shorter for offspringproducedby pairs than by multimale groups (e.g. the queue for a breedingvacancymay
be longer in a multi-malegroup).
There is known to be a relationshipbetween group
size and incidenceof extra-grouppaternityin one other
cooperatively-breedingspecies, the superb fairy-wren
(Maluruscyaneus;Mulderet al. 1994). Howeverin that
speciesextra-grouppaternityis greaterin largergroups,
and Mulderet al. arguedthat the patternarisesbecause
females in multi-malegroups can engage in extra-pair
copulation without losing the parentalcare of helpers,
because the offspring will at least be half-sibs to the
helpers.Thus the presenceof helpersmay liberatefemale
superbfairy-wrensfrom constraintson mate choice.
Reproductivesuccess
Within-group fertilization success in white-browed
scrubwrenswas greatest for alpha males in multi-male
groupsin which the beta male was relatedto the female,
intermediatefor pair males, and lowest for alpha males
in groups in which the beta male was unrelatedto the
female(Fig. 3). Alpha malesdid worst overallwhen they
lived with an unrelatedbeta male, because they shared
paternityequally. In contrast to alpha males, the beta
male gained the most within-grouppaternitywhen he
was unrelatedto both the alphamale and female,and no
paternitywhen in a group with his mother. The reproductive success of beta males appearedto be intermediate in groupsin whichhe was relatedto the alphamale
but not to the female. A full accountingof the relative
reproductivesuccessof alphaand beta maleswill need to
includetheir success siringoffspringin other groups.
Our estimatessuggest that males would gain greater
reproductivesuccessbreedingin a pair (1.1 gene-equivalents) than remainingon their natal territoryas a beta
male with both parents(0.4 gene-equivalents).Thus, all
else beingequal,breedingin a pairis the best option. We
suggest that either there are constraints on successful
male dispersaland breedingin a pair, or thereare other
benefits of philopatry or helping. Constraintsmay include the difficultiesof finding a mate in a population
with a male-biasedsex ratio (cf. Pruett-Jonesand Lewis
1990), while benefits may include increased survival.
Adult male survivalwas high (88% annual survivalfor
pair and alphamales,n =42), 50 queuingstrategiesmay
also be important (Wiley and Rabenold 1984). Scrub-
269
wrens will provide an interestingsystem for future re- Grafen A (1984) Natural selection, kin selection and group selection. In: Krebs JR, Davies NB (eds) Behavioural ecology.
searchbecauseof the wide varietyof mating and social
Blackwell, Oxford, pp 62-86
tactics availableto each sex.
Haig SM, Belthoff JR, Allen DH (1993) Examination of populaAcknowledgementsWe thank Andrew Cockburn, Camille Crowley, Olivia Forge, David Green, Milton Lewis, Megan McKenzie,
Raoul Mulder, Derrick Smith and especially Tony Giannasca for
help in the field, Angela Higgins for laboratoryassistanceand Alec
Jeffreys and Ted Bargiello for use of the 33.15 and per probes,
respectively. In addition, we thank Andrew Cockburn, Mike
Double, David Green, Elsie Krebs, Rob Heinsohn, Steve PruettJones, Stephen Yezerinac and three anonymous reviewers for
comments on the manuscript. This research was supported by
Australian ResearchCouncil grants to R.D.M., and by a grant to
A. Cockburn and R.D.M.
References
Ambrose SJ, Davies SJJF (1989) The social organization of the
white-browed scrubwren (Sericornis frontalis) Gould
(Acanthizidae) in arid, semi-arid and mesic environments of
Western Australia. Emu 89:40-46
Bell HL (1983) Cooperative breeding by the white-browedscrubwren, Sericornisfrontalis. Emu 82:315-316
Brooker MG, Rowley I, Adams M, Baverstock PR (1990) Promiscuity: an inbreeding avoidance mechanism in a socially
monogamous species?Behav Ecol Sociobiol 26:191-199
Brown JL (1987) Helping and communal breeding in birds.
Princeton University Press, Princeton
BurkeT, BrufordMW (1987) DNA fingerprintingin birds. Nature
327:149-152
Burke T, Davies NB, Bruford MW, Hatchwell BJ (1989) Parental
care and mating behaviour of polyandrous dunnocks Prunella
modularisrelated to paternity by DNA fingerprinting.Nature
338:249-251
ChristidisL, Schodde R (1991) Genetic differentiationin the whitebrowed scrubwren (Sericornis frontalis) complex (Aves:
Acanthizidae).Aust J Zool 39:709-718
Creel SR, Waser PM (1994) Inclusive fitness and reproductive
strategiesin dwarf mongooses. Behav Ecol 5:339-348
Davies NB (1992) Dunnock behaviour and social evolution. Oxford University Press, Oxford
Dunn PO, Cockburn A, Mulder RA (1995) Fairy-wren helpers
often care for young to which they are unrelated. Proc R Soc
Lond 259:339-343
Dunn PO, Robertson RJ, Michaud-FreemanD, Boag PT (1994)
Extra-pairpaternityin tree swallows:why do femalesmate with
more than one male? Behav Ecol Sociobiol 35:273-281
Emlen ST (1991) The evolution of cooperative breeding in birds
and mammals. In: Krebs JR, Davies NB (eds) Behavioural
ecology: An evolutionary approach, 3rd edn, Blackwell Scientific Publications, Oxford, pp 301-357
Emlen ST (1995) An evolutionary theory of the family. Proc Natl
Acad Sci 92:8092-8099
Emlen ST, Wrege PH (1988) The role of kinship in helping decisions among white-fronted bee-eaters. Behav Ecol Sociobiol
23:305-315
FaaborgJ, ParkerPG, DeLay L, VriesTJ de, BednarzJC, Paz MS,
Naranjo J, Waite TA (1995) Confirmation of cooperative
polyandryin the Galapagos hawk (Buteogalapagoensis).Behav
Ecol Sociobiol 36:83-90
Gibbs HL, Goldizen AW, Bullough C, Goldizen AR (1994) Parentage analysisof multi-malesocial groups of Tasmaniannative
hens (Tribonvyx
niortierii):genetic evidence for monogamy and
polyandry. Behav Ecol Sociobiol 35:363-371
tion structure in red-cockadedwoodpeckers using DNA profiles. Evolution 47:185-194
Haig SM, Walters JR, Plissner JH (1994) Genetic evidence for
monogamy in the cooperatively breeding red-cockadedwoodpecker. Behav Ecol Sociobiol 34:295-303
Hartley IR, Davies NB (1994) Limits to cooperative polyandry in
birds. Proc R Soc Lond 257:67-73
Haydock J, ParkerPG, Rabenold KN (1996) Extra-pairpaternity
uncommonin the cooperativelybreedingbicoloredwren. Behav
Ecol Sociobiol 38:1-16
Jamieson IG, Quinn JS, Rose PA, White BN (1994) Shared paternity is a result of an egalitarian mating system in a communally breedingbird, the pukeko. Proc R Soc Lond 257:271277
Jeffreys AJ, Wilson V, Thein SL (1985) Individual-specific"fingerprints"of human DNA. Nature 316:76-79
Joste N, Ligon JD, Stacey PB (1985) Sharedpaternityin the acorn
woodpecker (Melanerpesformicivorus).Behav Ecol Sociobiol
17:39-41
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) Partitioningof reproductionin animal
societies. Trends Ecol Evol 9:98-102
Lifjeld JT, Dunn PO, Robertson RJ, Boag PT (1993) Extra-pair
paternity in monogamous tree swallows. Anim Behav 45:213229
Millar CD, Anthony I, Lambert DM, Stapleton PM, Bergmann
CG, Bellamy AR, Young EC (1994) Patterns of reproductive
success determined by DNA fingerprintingin a communally
breedingoceanic bird. Biol J Linn Soc 52:31-48
Mulder RA, Dunn PO, CockburnA, Lazenby-CohenKA, Howell
MJ (1994) Helpers liberatefemale fairy-wrensfrom constraints
on extra-pairmate choice. Proc R Soc Lond 255:223-229
Packer C, Gilbert DA, Pusey AE, O'Brien SJ (1991) A molecular
analysis of kinship and cooperation in African lions. Nature
351:562-565
Piper WH, Rabenold PP (1992) Use of fragment-sharingestimates
from DNA fingerprintingto determinerelatednessin a tropical
wren. Mol Ecol 1:69-78
Piper WH, Slater G (1993) Polyandry and incest avoidance in the
cooperative stripe-backed wren of Venezuela. Behaviour
124:227-247
Piper WH, ParkerPG, Rabenold KN (1995) Facultativedispersal
by juvenile males in the cooperative stripe-backedwren. Behav
Ecol 6:337-342
Poldmaa T, MontgomerieR, Boag PT (1995) Mating system of the
cooperativelybreedingnoisy miner Manorinamelanocephala,as
revealed by DNA profiling. Behav Ecol Sociobiol 37:137-143
Pruett-JonesSJ, Lewis MJ (1990) Sex ratio and habitat limitation
promote delayed dispersal in superb fairy-wrens. Nature
348:541-542
Rabenold PP, Rabenold KN, Piper WH, Haydock J, Zack SW
(1990) Shared paternity revealed by genetic analysis in cooperatively breedingtropical wrens. Nature 348:538-540
Seutin G, White BN, Boag PT (1991) Preservationof avian blood
and tissue samples for DNA analysis. Can J Zool 69:82-90
Shin H-S, BargielloTA, Clark BT, Jackson FR, Young MW (1985)
An unusual coding sequence from a Drosophilaclock gene is
conservedin vertebrates.Nature 317:445-448
Sibley C, Ahlquist J (1990) Phylogeny and classificationof birds.
Yale University Press, New Haven
Vehrencamp SL (1983) A model for the evolution of despotic
versus egalitariansocieties. Anim Behav 31:667-682
270
Westneat DF (1990) Genetic parentage in the indigo bunting: a WregePH, Emlen ST (1987) Biochemicaldeterminationof parental
uncertainty in white-fronted bee-eaters. Behav Ecol Sociobiol
study using DNA fingerprinting.Behav Ecol Sociobiol 27:6776
20:153-160
Wetton JH, CarterRE, ParkinDT, WaltersD (1987) Demographic
study of a wild house sparrow population by DNA fingerprinting. Nature 327:147-149
Communicated by S. Pruett-Jones
Wiley RH, Rabenold KN (1984) The evolution of cooperative
breeding by delayed reciprocityand queuing for favorable social positions. Evolution 38:609-621