Polygynandry, Extra-Group Paternity and Multiple-Paternity Litters In
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Molecular Ecology (2007) 16, 5294–5306 doi: 10.1111/j.1365-294X.2007.03571.x Polygynandry,Blackwell Publishing Ltd extra-group paternity and multiple-paternity litters in European badger (Meles meles) social groups HANNAH L. DUGDALE,*† DAVID W. MACDONALD,* LISA C. POPE† and TERRY BURKE† *Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, Tubney House, Abingdon Road, Tubney OX13 5QL, UK, †Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK Abstract The costs and benefits of natal philopatry are central to the formation and maintenance of social groups. Badger groups, thought to form passively according to the resource dispersion hypothesis (RDH), are maintained through natal philopatry and delayed dispersal; however, there is minimal evidence for the functional benefits of such grouping. We assigned parentage to 630 badger cubs from a high-density population in Wytham Woods, Oxford, born between 1988 and 2005. Our methodological approach was different to previous studies; we used 22 microsatellite loci to assign parent pairs, which in combination with sibship inference provided a high parentage assignment rate. We assigned both parents to 331 cubs at ≥ 95% confidence, revealing a polygynandrous mating system with up to five mothers and five fathers within a social group. We estimated that only 27% of adult males and 31% of adult females bred each year, suggesting a cost to group living for both sexes. Any strong motivation or selection to disperse, however, may be reduced because just under half of the paternities were gained by extra-group males, mainly from neighbouring groups, with males displaying a mixture of paternity strategies. We provide the strongest evidence to date for multiple- paternity litters, and for the first time show that within-group and extra-group males can sire cubs in the same litter. We investigate the factors that may play a role in determining the degree of delayed dispersal and conclude that the ecological constraints hypothesis, benefits of philopatry hypothesis, and life history hypothesis may all play a part, as proposed by the broad constraints hypothesis. Keywords: cervus, Extra Pair Copulation (EPC), mating system, microsatellites, Mustelidae, reproductive skew Received 4 April 2007; revision received 24 June 2007; accepted 5 September 2007 the environment, the minimum defendable territory that Introduction provides sufficient resources for a minimum social unit may Mammals exhibit a diverse array of mating systems, chara- also accommodate more individuals. Once social groups form, cterized by the ecological and behavioural opportunities the factors under which selection will favour natal philopatry for individuals to monopolize mates and the way in which (Waser & Jones 1983) are central to the maintenance of social mates are acquired (Emlen & Oring 1977). Breeding system groups (Macdonald & Carr 1989). Delayed dispersal may properties determine group composition (Ross 2001). occur due to ecological constraints on dispersing and breeding As individuals are expected to act in a way that maximizes elsewhere (Emlen 1982), benefits of philopatry (Stacey & their lifetime inclusive fitness (Hamilton 1964), understanding Ligon 1991), certain life history traits, such as a low rate of why individuals live in groups requires knowledge of the breeder mortality that increases habitat saturation (Arnold costs and benefits of group living. The resource dispersion & Owens 1998), or a combination of these factors (the broad hypothesis (RDH) (Macdonald 1983; Carr & Macdonald constraints hypothesis, Hatchwell & Komdeur 2000). 1986) proposes that when resources are spaced patchily in Social species that encounter a variety of environmental conditions may exhibit variation in their mating system Correspondence: Hannah L. Dugdale, Fax: +44 (0) 1865 393101. (Taylor et al. 2000). The European badger is a promising E-mail: [email protected] species for understanding such variation because it has a © 2007 The Authors Journal compilation © 2007 Blackwell Publishing Ltd BADGER MATING SYSTEM 5295 widespread distribution from the British Isles to Japan and Our study combines parentage assignment and sibship from the southern Mediterranean to the Russian Arctic inference, a novel approach recommended by Garant & Circle. It exhibits large variation in social organization over Kruuk (2005), to test whether (i) badger social groups exhibit this range, living singly, or in pairs and defending territories plural breeding; (ii) females breed with extra-group males; in parts of mainland Europe, whereas in lowland England (iii) males have different paternity strategies; and (iv) multiple- badgers are typically group living (Johnson et al. 2000). Despite paternity litters occur. We discuss our results in relation to their sociality, there is minimal evidence of the functional the four proposed hypotheses for the occurrence of delayed significance of grouping in badgers (Johnson et al. 2004), dispersal. In particular, we ask: Is group living costly to whereas there is evidence of an ecological basis of group liv- badgers? Does extra-group paternity reduce inbreeding? ing that does not invoke cooperation (Johnson et al. 2001a, b). Do multiple-paternity litters provide fitness benefits? Do Badger social groups have been reported to vary in size delayed implantation and the potential for superfetation from 2 to 29 individuals (da Silva et al. 1994). One proposal, (conception during pregnancy, Yamaguchi et al. 2006) facilitate first advanced for badgers by Kruuk (1978) is that groups multiple-paternity litters? form according to the RDH (Macdonald 1983) and are main- tained by natal philopatry (Cheeseman et al. 1988; da Silva Materials and methods et al. 1994). Dispersal is restricted (Pope et al. 2006), with only 20% of the badgers trapped in Wytham Woods at any given Study site and population demography time having ‘dispersed’ (i.e. resident in more than one group), with residence defined as trapped in the same group in two Our data come from Wytham Woods, Oxfordshire (51°46′N, consecutive trapping events, and at least one of two trapping 01°19′W), that cover 4 km2 and consist of deciduous events prior to that (D. W. Macdonald, C. Newman, C. D. woodland, surrounded by permanent pasture and mixed Buesching & P. J. Johnson, unpublished). Dispersal may be arable land (Kruuk 1978). Enclosing features potentially costly; females that dispersed failed to produce cubs (da limit badger movement in and out of the study area Silva et al. 1993) and reduced fecundity was associated with (Macdonald & Newman 2002). From June 1987 to November increased dispersal rates in a culled compared with a con- 2005, trapping events have usually been undertaken at trol population (Tuyttens et al. 2000). Costs of group living also least four times a year, in January, June, August and include low levels of cub productivity (Cheeseman et al. 1987; November (Macdonald & Newman 2002). The badger Cresswell et al. 1992; Woodroffe & Macdonald 1995; Rogers population ranged from 60 to 228 adults and 23–61 cubs et al. 1997; Macdonald & Newman 2002) and a decreased (1987–96) with the highest density being 44 badgers/km2 proportion of lactating females in a control vs. culled popu- (Macdonald & Newman 2002). lation (Tuyttens et al. 2000). Few benefits to badgers of group living have been identified (Johnson et al. 2004). Although Sample collection cooperative breeding has been suggested in badgers (Woodroffe 1993), this has not been confirmed. The number Badgers were sedated by an intramuscular injection of of nonbreeding females had a negative effect on mean approximately 0.2 mL/kg ketamine hydrochloride. Cubs litter size, after controlling for territory quality (Woodroffe were first trapped around 16 weeks of age; those judged & Macdonald 2000); however, longer-term benefits have to weigh ≤ 2 kg were considered too small for sedation not been investigated. and were released after a hair sample was plucked. On Badgers give birth once a year, around February, with initial capture, badgers were marked with a unique tattoo cubs remaining underground for the first 8 weeks. This, number, through which recaptures were identified. Badgers along with the presence of many potential parents, means were classified as cub or adult based on their size and that it is not possible to identify individuals that have bred tooth wear; they were then sexed. Tooth wear was graded successfully using conventional ecological methods. Our on a subjective scale of 1 (no tooth wear: white teeth, study uses microsatellite data to assign parentage in a long- pointed canines and unworn ridges on molars) to 5 term study in Wytham Woods, Oxford, UK. Microsatellites (extreme tooth wear: canines broken or missing and molars were also used to determine parentage in Woodchester Park, worn down to the dentine). Approximately 3 mL of blood Gloucestershire, UK, which is a similarly high-density was collected from the jugular vein of each badger using population (Carpenter et al. 2005). Prior to this, multiple a vacutainer containing EDTA, and mixed immediately. maternity and extra-group paternity had been shown Blood was transferred into two 1.5-mL microcentrifuge (Evans et al. 1989; da Silva et al. 1994; Domingo-Roura et al. tubes and frozen immediately at –4 °C. Additionally, 2003), but parentage could not be assigned to individuals. from June 2002 onwards, approximately 100 guard hairs Behavioural observations