Behav Ecol Sociobiol (1997) 40: 261-270 (? Springer-Verlag 1997

Linda A. Whittingham Peter 0. Dunn

Robert D. Magrath

Relatedness, polyandry and extra-group paternity

in the cooperatively-breeding white-browed scrubwren

(Sericornis frontalis)

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 coopera-

tively breeding white-browed scrubwren, Sericornis

frontalis, in Canberra, Australia. Our analyses revealed a

remarkable variety of mating tactics and social organi-

zation. Scrubwrens bred in pairs or multi-male groups

that consisted of a female and two or more males. Fe-

males 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 re-

productive benefits both directly and potentially indi-

rectly (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 mo-

nopolized 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 pre-

dicted 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 Department of 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 breeding- DNA 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 in-

directly (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 produc-

tion 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 cate-

gories are not exclusive, as helpers may gain both indi-

rect 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 dom- inates reproduction (high skew), while at the other, re-

production is shared equally (low skew). Vehrencamp

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(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 con- straints 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 terri- tories (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 repro- duction 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 related- ness. 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 coopera- tively (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 domi- nant (alpha) and subordinate males (R. Magrath un- published 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 im- portance of kin selection in maintaining philopatry by subordinate males.

Methods

Study site and species

White-browed scrubwrens are small (11-15 g), insectivorous pas- serines (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 breeding seasons we studied a pop- ulation of scrubwrens resident at the Australian National Botanic Gardens. a 40-ha reserve of native vegetation in Canberra, Aus- tralia. We caught and uniquely color-banded all adults and off- spring on about 50 territories. Territorial social groups were pairs or multi-male groups consisting of one female, a dominant male, and up to four subordinate males. We determined the dominance status of males from daily observations of male chases and dis- placements 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 breeding season following hatching, and there were no obvious differences in appearance among males of different age or status. We refer to dominant males as alpha males and the most dominant subordinate males as beta males. Females always dispersed from their natal group, and so breeding females were unrelated to the dominant males (see below).

Over the 2 years of the study, there were 108 group-years, which is the number of different seasons each social group attempted breeding, summed over groups. When one or more of the potential breeders (female, alpha or beta male) changed between breeding attempts we considered this a different social 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% were groups with two males, and 100% were groups of three or more males. On average, males made up 64% of the adult population in each year.

Scrubwrens bred in the Botanic Gardens from 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. Fe- males 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 presumed fertile 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 determined paternity for 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 contributed one brood and six pairs contributed two broods, while nine multi-male groups con- tributed one brood and nine multi-male groups contributed two 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-male groups. The paternity of 15 nestlings could not be determined because there was insufficient DNA.

Blood samples (20-70 pl) used for DNA fingerprinting were suspended in Queen's lysis buffer (Seutin et al. 1991) and stored at 4?C prior to analysis. Our DNA fingerprinting procedures followed Mulder et al. (1994). Briefly, we digested 8 ,ug of genomic DNA per individual with Hae III and added 6 ng of a molecular size- marker to each sample. Samples were subjected to electrophoresis at 2 V/cm through a 40-cm (0.80%) agarose gel for 45-50 h. Fol- lowing electrophoresis, DNA was transferred by Southern blotting onto Immobilon-N or Hybond-N+? membranes. All membranes

263

were hybridized separately with radioactively labeled per (Shin et al. 1985), 33.15 (Jeffreys et al. 1985) and the DNA molecular size- marker to produce three separate autoradiographs. The molecular size markers in each lane allowed us to correct for distortions in the migration of DNA fragments across the gel.

DNA fingerprints were scored following methods in Westneat (1990) and Lifjeld et al. (1993). The average number of scorable fingerprint bands 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 fingerprint bands that were not present in either putative parent (novel fragments, Westneat 1990). Thus, novel fragments were inherited from indi- viduals other than the putative parents or resulted from mutation. Nestlings were excluded as the progeny of a particular set of pu- tative parents if their fingerprint profile contained more novel fragments than 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 1000 meiotic events which was similar to 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 scrubwren nestling would have one or two mutant bands was 0.085 and 0.004, respectively. Therefore, nestlings with two or more novel fragments were unlikely to have acquired them 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) between each 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-sharing between 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-sharing was < 0.330 (Fig. 1). We assigned paternity to 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-sharing between adults within social groups to determine their relatedness. We considered two individuals to be "unrelated" if their band-sharing was < 0.330. Band-sharing bet- ween putatively unrelated individuals (females and their mates) averaged 0.169 ? 0.061(? SD, n = 13) for pairs and 0.174 ? 0.087 for females and alpha males in their group (n = 16 females breeding

Pairs Groups .8 I .8 I

.7-Q Female 7 00 Female

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2 4 6 8 10 12 14 16 18 0 5 10 15 20 25

V .8 , .9 C~~~~~~~~~~~~~

X .7 i Putative father .8- I Alpha male 6 ~~~~~~~~~~~~~~~~.7

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Novel fragments

Fig. 1 Band-sharing (mean from both probes) in the white-browed scrubwren between offspring and their putative parents in relation to the total number of novel fragments (both probes combined) for pairs (left) and multi-male groups (right). We considered young that had fewer than two novel fragments (vertical lines) with a set of putative parents and band-sharing > 0.330 (horizontal lines) with each parent to be the progeny of those parents (see Methods for statistics). For multi-male groups, the number of novel fragments in the upper (female) and middle (alpha male) boxes were based on a comparison of offspring with the female and the alpha male as putative parents;

whereas, in the lower box (beta male) the number of novel fragments for offspring was based on the female and the beta male as putative parents. "Novel fragments" can come from mutations, the other male in the social group or an extra-group male. Note that for beta males there was high band-sharing for some offspring even though there were at least three novel fragments, because in all of these cases the beta male was the son of the female and alpha male (i.e. a first order relative of both the parents and most offspring). See Fig. 2 for a breakdown of beta male band-sharing by type of group

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with different alpha males). The upper 99% CI (one-tailed) for band-sharing between all females and their mates was 0.346, which represents an upper limit for band-sharing between unrelated in- dividuals. Thus, we considered two individuals to be "related" if their band-sharing was > 0.346. In our sample there were no cases where band-sharing was between 0.330 and 0.346, so all individuals within a social group could be classified as "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 scrubwrens breed 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-pair paternity" to refer to paternity by the beta male, and we refer to paternity by males outside a social group of any size as "extra-group paternity".

We used the mean reproductive success of females breeding in pairs versus multi-male groups to provide an estimate of the indi- rect reproductive benefits to males of breeding on their own in a pair versus remaining in their natal territory as a non-breeding beta male (Brown 1987). We only included females in the analysis if: (1) the female bred in the same group size for all breeding attempts within a season, (2) the female was monitored closely so that all nests producing fledglings were found, (3) the number of young fledging was known for every breeding attempt, 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 first clutches). If we had data from two seasons for the same female in the same- sized group, we used the mean seasonal reproductive success.

Results

Types of multi-male groups

We classified groups according to relatedness among adults, which was determined from the mean band- sharing of both probes (see Methods, Fig. 1). In all groups, the alpha male was unrelated to the breeding female [mean (? SD) band-sharing- 0.174 ? 0.087; range = 0.036 - 0.311, n 16 groups with different fe- males and alpha males]. However, there was variability in whether or not the beta male was related to the other adults in the group, so we classified groups according to the relatedness of the beta male to the dominant pair.

We found four types of multi-male groups: (1) in seven of 18 groups, the beta male was related to the alpha male (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 related to the alpha male (0.320); (3) in five groups the beta male was related to 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-male groups there was a third male who was subordinate to the beta male; however, none of the these males gained paternity and 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 un-

known 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 evi-

dence 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 ex-

clude 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

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Novel fragments

Fig. 2 Band-sharing (mean from both probes) in the white-browed scrubwren between offspring and the beta male in relation to the total number of novel fragments (both probes combined) for each of the four types of groups (note that these were combined in Fig. 1). Novel fragments are based on the female and beta male as putative parents in all four boxes. Filled circles represent nestlings sired by the beta

Direct reproductive benefits

The reproductive benefits for males breeding in multi- male groups depended on the type of group. Alpha males fathered the most young in two types of multi- male groups: (1) the beta male was related to both the female and alpha, in which case the alpha male sired 2.8 + 0.2 [SE] nestlings per brood (n = 12 broods) and (2) the beta male was related only to the female, in which case the alpha male sired 3 nestlings (n = 1 brood). In contrast, alpha males sired the fewest young (1.3 ? 0.2 nestlings per brood, n = 9 broods) when they lived with a beta male that was unrelated both to the alpha male and female (Fig. 3). When alpha and beta males were unrelated to each other and to the female they had similar fertilization success (U 42, P = 0.89; Fig. 3). For beta males, fertilization success was greatest when they lived with an unrelated alpha male and female (1.2 ? 0.3 nestlings per brood, n - 9 broods), and fewest when they lived with a related female (no nestlings sired;

male, open circles represent nestlings sired by the alpha male and diamonds represent nestlings sired by a male from outside the group. See Fig. 1 for an explanation of the vertical and horizontal lines. The relatively high band-sharing in the upper right panel is likely due to some degree of relatedness (less than first-order) between the alpha and beta males

Fig. 3). Thus, the best situation for the alpha male in terms of fertilization success within a group was the worst situation for the beta male, and the best situation for the beta male (living with an unrelated alpha male and female) was the worst for the alpha male.

Indirect reproductive benefits

Potential indirect benefits can be estimated from the difference in reproductive success between multi-male groups and pairs (Brown 1987). These indirect benefits may be sufficient to favor beta males that remain on their natal territory rather than disperse and breed on their own in a pair. In the following analyses, we esti- mated the maximum indirect benefits to beta males of remaining in their natal group.

Females breeding in multi-male groups had a higher mean seasonal production of fledglings [3.3 ? 0.44 (SE); n = 34 female-groups] than did those in pairs

Table 1 Paternity of white-browed scrubwren broods and nestlings, 1992 and 1993. "Extra-group" refers to young sired by males outside the social group

% Broods (n) with one or more offspring sired by % Nestlings (n) sired by

Alpha male Beta male Extra-group Total Alpha male Beta male Extra-group Total male n male n

Pairs 90% (17) 42% (8) 19 76% (38) 24% (12) 50 Multi-male 97% (31) 31% (10) 13% (4) 32 76% (66) 18% (16) 6% (5) 87 groups All 94% (48) 24% (12) 51 76% (104) 12% (17) 137

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la 2- 0T

0& ....0 0.....

Pairs Alpha Beta Alpha Beta Alpha Beta Alpha Beta

(N= 19) Beta male Beta male Beta male Males

related to unrelated related to unrelated Alpha male to Alpha male, Alpha male, to each other and female related to female unrelated to and to female

(N= 1 2) (N= 1 ) female (N= 9) (N= 10o)

Fig. 3 Mean number (+ SE) of young sired per brood for male white- browed scrubwrens living in pairs and in four types of multi-male groups. Sample sizes indicate the number of broods. Although extra- group paternity occurred more 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 paternity with beta males in 31% (10/32)

(2.9 ? 0.40, n = 25 female-groups). Thus, a male that breeds in a pair produces a total of 2.9 fledglings per season, and on average 2.2 of these fledglings are related (r = 0.5) offspring and 0.7 are unrelated (r = 0.0) young resulting from extra-group fertilization (24%). The production of gene-equivalents is thus 1.1 (i.e. 2.2 x 0.5 gene-equivalents per young). If this male instead re- mained as a subordinate with both parents, the total production of fledglings over the season would be 3.3 full sibs (r = 0.5; Table 2). We assume here that the lack of observed extra-group young in groups in which the

of broods (Table 1). Overall, beta males sired fewer young (0.5 ? 0. 1, n = 32 broods) than either alpha males (U = 894, P < 0.001) or

pair males (U = 521, P < 0.001). Number of young sired per 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 (males living in a multi-male group in which the beta male was related to the female were combined into one group for this analysis)

beta male is related to both parents is due to the pres- ence of the beta male. If the son dispersed, his parents would produce, from the disperser's point 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-group fertilizations). Thus, the overall benefit of remaining with 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-equivalents per half-sib]. Overall, a male produces 0.7 more gene- equivalents (1.1 - 0.4) by breeding in a pair rather than remaining with his parents as a subordinate helper.

Table 2 Paternity of white-browed scrubwren broods and nestlings in four types of multi-male groups, 1992 and 1993

% Broods (n) with one or more young sired by % Nestlings (n) sired by

Type of Extra-group Total Extra-group Total multi-male group Alpha male Beta male male n Alpha male Beta male male n

Beta male is related 100% (12) 0% (0) 0% (0) 12 100% (34) 0% (0) 0% (0) 34 to alpha male and female

Beta male is related 100% (1) 0% (0) 0% (0) 1 100% (3) 0% (0) 0% (0) 3 to female, but not to alpha male

Beta male is related 90% (9) 33% (3) 33% (3) 10 66% (17) 19% (5) 15% (4) 26 to alpha male, but not to female

Beta male is not 100% (9) 78% (7) 11% (1) 9 50% (12) 46% (11) 4% (1) 24 related to alpha male or female

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Discussion

The white-browed scrubwren exhibits a remarkable va- riety of mating tactics. In our population, the most common breeding arrangement was 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 different mating strategies: (1) when beta males were sons of the female (either related or unrelated to the alpha male) and they remained on their natal territory as helpers, they did not gain paternity within the group; (2) when beta males were not related to the female but were sons of the alpha males, beta males gained paternity in some broods, and thus gained re- productive benefits both directly and potentially indi- rectly (through their father); and (3) when alpha and beta males were unrelated they usually shared paternity in the brood, and thus, both males gained reproductive benefits directly. Finally, scrubwrens also bred in so- cially monogamous pairs in which extra-group paternity was fairly common. Although each of the forms of mating and relatedness that we have discovered in scrubwrens has been described previously in birds, the simultaneous and common occurrence of this variation in one species is so far rare.

Reproductive skew

Models of reproductive skew assume that dominant in- dividuals control the reproduction of subordinates, and high-skew societies are called "despotic" (Vehrencamp 1983; Keller and Reeve 1994; Emlen 1995). Dominants can afford to be despots towards subordinates that are close relatives because the subordinates have limited breeding opportunities and gain some fitness by helping dominants to breed. In contrast, "egalitarian" societies are those in which reproduction is shared (low skew). A society is likely to be most egalitarian when subordinates are unrelated to dominants and have other options, such as a high chance of gaining a dominant breeding situa- tion. Most cooperative species studied to date have fallen into one or the other of these two types of breeding system (see also Hartley and Davies 1994). In contrast, white-browed scrubwrens breed in both des- potic and egalitarian groups.

Egalitarian groups with shared paternity between unrelated males seem to be quite rare in birds and have only been confirmed by genetic analyses in a few species (Emlen 1995). For example, unrelated males share pa- ternity fairly equally in polyandrous groups of pukekos (Porphyrio porphyrio, Jamieson et al. 1994), Galapagos hawks (Buteo galapagoensis, Faaborg et al. 1995), dun- nocks (Prunella modularis, Burke et al. 1989) and brown skuas (Catharacta lonnbergi, Millar et al. 1994). If death and dispersal of individuals commonly introduces un- related individuals into groups, then egalitarian groups

with shared paternity may occur more frequently than is currently realized.

Despotic groups appear to be the most common type among cooperatively-breeding birds. In most species helpers are the previous offspring of the breeding pair, and thus they can gain indirect benefits from assisting close kin (Brown 1987; Hartley and Davies 1994). To date, however, few genetic studies have been made of this "classical" type of cooperative breeding. If extra- group paternity is common, then indirect benefits may be much lower than estimated previously (e.g. Dunn et al. 1995). Nevertheless, recent studies generally sup- port the traditional view that helpers are genetically re- lated to the young they assist (e.g. Emlen and Wrege 1988; Rabenold et al. 1990; Haig et al. 1993, 1994; Gibbs et al. 1994), and thus helpers can gain indirect benefits if their assistance improves the reproductive success of the group (Grafen 1984). These studies also indicate a strong bias toward one male dominating paternity, as would be expected in despotic groups.

The pattern of paternity and relatedness in scrub- wrens is consistent with Vehrencamp's model of repro- ductive skew (Vehrencamp 1983). 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 predicted for an egalitarian system. This positive association between relatedness and reproduc- tive skew has been described in intraspecific studies of some mammals (Packer et al. 1991; Creel and Waser 1994). There is a similar pattern in the pukeko, although the comparison involves different populations; in one population multi-male groups were composed of kin, while in the other population individuals were unrelated (Jamieson et al. 1994). Other species with some simi- larity to scrubwrens include 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 subordinates in these species, in most cases the beta males are either unrelated (dunnocks; egalitarian sys- tem) or related (stripe-backed wren; despotic system) to the alpha male. Unrelated males in groups occur occa- sionally in stripe-backed wrens (Piper et al. 1995), but it is not clear how often these males share paternity. Al- though the pattern of shared paternity in scrubwren multi-male groups is consistent with previous models of reproductive skew, it is unclear if dominants can control the reproduction of subordinates, which is a critical and as yet untested assumption of these models.

In most cooperative birds with multi-male groups there appears to be a trade-off for males between pa- ternity lost to other group members, and other benefits, such as increased production of close kin (e.g. Rabenold et al. 1990; Gibbs et al. 1994; Poldmaa et al. 1995) or group defense of a breeding territory (Jamieson et al. 1994). However, the outcome of this tradeoff is not simple, because it can also be influenced by a conflict of

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interests between the female and her mates. For exam- ple, female dunnocks have higher reproductive success in cooperatively-polyandrous groups than in pairs be- cause they receive more male parental care, whereas male dunnocks have higher reproductive success when they are monogamous or polygynous, because they do not have to share paternity (Burke et al. 1989). This conflict of interest between the sexes adds another level of complexity to previous models of reproductive skew, and it likely reduces the overall level of reproductive skew by dominants (Vehrencamp 1983).

Extra-group paternity

Scrubwrens had an intermediate level of extra-group paternity (12% of young) compared with the few other cooperative breeders in which paternity has been stud- ied. The incidence of extra-group fertilization in coop- erative breeders spans the range for birds as a whole. At one extreme, very low levels of extra-group paternity (K 1 %) have been reported for stripe-backed wrens and red-cockaded woodpeckers (Rabenold et al. 1990; Haig et al. 1993, 1994). At the other extreme are the fairy- wrens (Malurus spp.), which have the highest known levels of extra-group paternity (60-76% of young; Brooker et al. 1990; Mulder et al. 1994). Overall, the incidence of extra-group paternity in scrubwrens is sim- ilar to that for non-cooperative breeders (mean= 17% extra-pair young; Dunn et al. 1994).

Extra-group paternity in scrubwrens is more frequent in pairs than in multi-male groups (Table 1). The in- terpretation of this pattern will depend on whether fe- males or males are ultimately shown to be responsible for paternity. We have not seen extra-group copulations, or as yet assigned paternity in cases of extra-group pa- ternity, so we simply suggest three possibilities. First, females may seek extra-group copulations to gain su- perior genotypes for their offspring. Females in multi- male groups may not seek extra-group copulation as often because they are able to choose among more than one potential mate 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 should expect relatively more extra- group fertilizations in this type of multi-male group. We detected no variation in the incidence of extra-group paternity across different types of multi-male groups, but our sample sizes are currently too 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 fertilization of their eggs. Consistent with this idea, we found that the frequency of clutches with multiple sires (regardless of type) was similar for females in pairs and multi-male groups. Second, if mate guarding is related to paternity, then two males in a group may be better at guarding their female than one male in a pair. Both al- pha and beta males in all types of multi-male groups

would have lower reproductive success if offspring were sired by unrelated extra-group males. Thus, there should be no differences in the incidence of extra-group fertil- ization across different types of multi-male groups. If philopatric sons reduce the incidence of extra-group paternity, then this would be a novel form of helping. Third, if extra-group males are responsible for the pat- tern of paternity, then it implies that siring extra-group young has a greater benefit to males when the young are sired in pairs than in multi-male groups. This is possible if the average time to gaining a breeding vacancy is shorter for offspring produced by pairs than by multi- male groups (e.g. the queue for a breeding vacancy may be longer in a multi-male group).

There is known to be a relationship between group size and incidence of extra-group paternity in one other cooperatively-breeding species, the superb fairy-wren (Malurus cyaneus; Mulder et al. 1994). However in that species extra-group paternity is greater in larger groups, and Mulder et al. argued that the pattern arises because females in multi-male groups can engage in extra-pair copulation without losing the parental care of helpers, because the offspring will at least be half-sibs to the helpers. Thus the presence of helpers may liberate female superb fairy-wrens from constraints on mate choice.

Reproductive success

Within-group fertilization success in white-browed scrubwrens was greatest for alpha males in multi-male groups in which the beta male was related to the female, intermediate for pair males, and lowest for alpha males in groups in which the beta male was unrelated to the female (Fig. 3). Alpha males did worst overall when they lived with an unrelated beta male, because they shared paternity equally. In contrast to alpha males, the beta male gained the most within-group paternity when he was unrelated to both the alpha male and female, and no paternity when in a group with his mother. The repro- ductive success of beta males appeared to be interme- diate in groups in which he was related to the alpha male but not to the female. A full accounting of the relative reproductive success of alpha and beta males will need to include their success siring offspring in other groups.

Our estimates suggest that males would gain greater reproductive success breeding in a pair (1.1 gene-equiv- alents) than remaining on their natal territory as a beta male with both parents (0.4 gene-equivalents). Thus, all else being equal, breeding in a pair is the best option. We suggest that either there are constraints on successful male dispersal and breeding in a pair, or there are other benefits of philopatry or helping. Constraints may in- clude the difficulties of finding a mate in a population with a male-biased sex ratio (cf. Pruett-Jones and Lewis 1990), while benefits may include increased survival. Adult male survival was high (88% annual survival for pair and alpha males, n =42), 50 queuing strategies may also be important (Wiley and Rabenold 1984). Scrub-

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wrens will provide an interesting system for future re- search because of the wide variety of mating and social tactics available to each sex.

Acknowledgements We thank Andrew Cockburn, Camille Crow- ley, Olivia Forge, David Green, Milton Lewis, Megan McKenzie, Raoul Mulder, Derrick Smith and especially Tony Giannasca for help in the field, Angela Higgins for laboratory assistance and 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 Pruett- Jones, Stephen Yezerinac and three anonymous reviewers for comments on the manuscript. This research was supported by Australian Research Council grants to R.D.M., and by a grant to A. Cockburn and R.D.M.

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Communicated by S. Pruett-Jones