JOURNAL TRANSCRIPT

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Molecular Ecology (2012) 21, 472–492

doi: 10.1111/j.1365-294X.2011.05232.x

INVITED REVIEW

The evolution of social philopatry and dispersal in female mammals T . H . C L U T T O N - B R O C K and D . L U K A S Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK

Abstract In most social mammals, some females disperse from their natal group while others remain and breed there throughout their lives but, in a few, females typically disperse after adolescence and few individuals remain and breed in their natal group. These contrasts in philopatry and dispersal have an important consequence on the kinship structure of groups which, in turn, affects forms of social relationships between females. As yet, there is still widespread disagreement over the reasons for the evolution of habitual female dispersal, partly as a result of contrasting definitions of dispersal. This paper reviews variation in the frequency with which females leave their natal group or range (social dispersal) and argues that both the avoidance of local competition for resources and breeding opportunities and the need to find unrelated partners play an important role in contrasts between and within species. Keywords: dispersal, mammals, philopatry, sociality Received 17 March 2011; revision received 17 May 2011; accepted 19 May 2011

Introduction Among social mammals, there are marked differences in the kinship structure of female groups: in most species, female group members are philopatric, matrilineal relatives, but in a few species they are typically unrelated immigrants from other groups (Wrangham 1980; Pusey & Packer 1987; Clutton-Brock 2009). These contrasts in kin structure have important consequences for the evolution of social behaviour: where most female group members are close relatives, groups are usually stable and cooperation between females is relatively common while, where females are unrelated, females often move between social groups and cooperative behaviour is seldom highly developed (Sterck 1997; Clutton-Brock 2009). Interspecific differences in the kinship structure of social groups are a consequence of contrasting patterns of female philopatry and dispersal: in some species, most females remain and breed in their natal group throughout their lives and female group members are mostly close relatives while, in others, females usually leave their natal group as adolescents or young adults and either die, join established breedCorrespondence: Tim H. Clutton-Brock, Fax: +44 1223 336 676; E-mail: [email protected]

ing groups or found new breeding units and female group members are typically unrelated to each other (Lukas et al. 2005). The causes of differences in female philopatry and dispersal have attracted interest for more than 30 years but there is still little agreement as to the importance of different evolutionary mechanisms (Greenwood 1980; Moore & Ali 1984; Pusey 1987; Clutton-Brock 1989; Perrin & Mazalov 1999; Ronce 2007; Clobert et al. 2008). One contributory factor is that the evolution of philopatry and dispersal is relevant to many distinct areas of population biology and has been considered by scientists from different disciplines with contrasting agendas, including population demographers, population geneticists interested in the movement of individuals between local populations or demes (Johnson & Gaines 1990; Clobert et al. 2008) and behavioural ecologists, interested principally in the social mechanisms affecting the tendency of individuals to remain in their natal group or to leave it to search for breeding opportunities elsewhere (Brown 1987; Ekman & Rosander 1992; Kokko & Ekman 2002). As a result, the definitions of philopatry and dispersal used in different studies have varied widely (Reed 1993; Bowler & Benton 2005) confusing comparisons and complicating conclusions. On one hand, population geneticists and demographers  2011 Blackwell Publishing Ltd

P H I L O P A T R Y A N D D I S P E R S A L I N F E M A L E M A M M A L S 473 commonly use philopatry to refer to the continued presence of individuals within their natal population or deme and dispersal to occur when individuals leave their natal population (see Mayr 1963; Shields 1982; Reed 1993; Laporte & Charlesworth 2002): for example, Shields (1987) defines philopatry as ‘limited dispersal such that the average propagule moves no more than ten home ranges away from its site of origin’ and regards both sexes as philopatric if neither exceeds this limit. In contrast, behavioural biologists interested in the kinship structure of female groups and the causes of immigration and emigration have commonly defined dispersal as movements out of the natal group or range (Greenwood 1980; Waser & Jones 1983; Clutton-Brock 1989; Waser 1996). Since many individuals that leave their natal group settle within less than ten home range diameters (e.g. Cockburn et al. 1985; Pope 2000; Sutherland et al. 2000; Radespiel et al. 2003) these two approaches commonly produce different results. A second problem is that some studies of dispersal have classified females as philopatric or dispersive on the basis of whether they leave their natal territory or group (Clutton-Brock 1989) while others define sex differences in dispersal as the ratio of mean male dispersal distance to mean female dispersal distance and have classified females on the basis of whether they move further from their natal territory than males (Clarke et al. 1997; Miller et al. 2011). Where classifications are based on sex differences in dispersal distance (Greenwood 1980), species whose females are classified as philopatric commonly include species in which most or all females leave their natal territory to breed but do not move as far as males (as, for example, in many passerine birds) as well as species where females typically breed in their natal group or range. The factors affecting whether individuals leave or remain in their natal range or group are often likely to differ from those affecting the distance they move if they do leave. In many social species, social factors operating within their natal group (including the intensity of aggression directed at them by resident breeding females, their need for alliances with relatives and the availability of unrelated breeding partners) play an important role in determining whether or not females leave their natal group and, if so, which individuals remain and which stay (see below). In contrast, the distances moved by individuals once they have left their natal group are likely to be strongly affected by immediate ecological parameters, including the quality and availability of vacant habitat and breeding partners and there is limited evidence that individuals that have left their natal group continue to discriminate against breeding with relatives (see below). A third problem contributing to ongoing discussions of the evolution of philopatry and dispersal is that  2011 Blackwell Publishing Ltd

empirical data providing reliable and accurate estimates of the frequency of dispersal and the distances moved are scarce. Unless large numbers of individuals are marked it is seldom possible to distinguish between mortality and dispersal while even in studies where all individuals are marked or recognisable, it is frequently difficult to determine whether individuals that disappear have died or dispersed (Waser et al. 1994; Creel & Creel 2002). If the practical difficulties of estimating dispersal frequency are substantial, those of measuring and comparing dispersal distances are far greater. In most vertebrates, individuals are usually difficult to follow once they have left their natal group or range and those that settle close to their group of origin are more likely to be detected than those that move further, so that dispersal distances are often likely to be systematically biased towards shorter distances (van Noordwijk 1995; Koenig et al. 1996; Sharp et al. 2008). Where records of dispersal distance are based on a small proportion of the initial sample (as, for example, in most studies of ringing in birds) biases may be very strong, their magnitude is seldom possible to assess (Koenig et al. 1996) and it may often be unsafe to assume that biases affect both sexes equally and comparisons of mean dispersal distance may conceal important differences in variance (Sharp et al. 2008). For example, in species where one sex commonly remains and breeds in their natal group (and is consequently classified as philopatric), individuals that do disperse are often unable to join established breeding groups and move further than individuals of the sex that disperses more frequently (Pope 2000; Ji et al. 2001; Blundell et al. 2002), so that comparisons of mean dispersal distance mask important differences in distribution. The recent development of extensive genetic sampling to assign parentage represents an important development which has provided new insights into dispersal in a number of rodents (Telfer et al. 2003; Aars et al. 2006; Waser et al. 2006; Waser & Hadfield 2011) as well as in other animals (Christie et al. 2011; Planes & Lemer 2011) but its application to larger, more mobile mammals where it is difficult to catch or sample large numbers of individuals is likely to be limited by logistic problems. Moreover, the application of paternity or other genetic (Prugnolle & de Meeuˆs 2002; Lawson-Handley & Perrin 2007) or demographic (Abadi et al. 2010) techniques does not solve the problem that, unless the behaviour of recognisable individuals can be monitored, it is usually difficult to gain a reliable understanding of the reasons why they leave their natal groups or of the factors affecting how far they move. Without studies at this level, it is seldom possible to test the assumptions of theoretical models of dispersal and there is a danger that models will be developed that do not reflect the

474 T . H . C L U T T O N - B R O C K and D . L U K A S biological processes important in natural populations. For example, some recent models of dispersal have been based on the assumption that local resource competition (Clark 1978) favours the evolution of dispersal from groups that include a high proportion of close kin (Hamilton & May 1977; Perrin & Mazalov 2000) whereas the available evidence suggests that the presence of relatives increases the probability that individuals will remain in their natal group (see below). In this situation, we believe that it is useful to distinguish between questions concerning the reasons why social animals leave their natal group or territory and questions concerning the distances they move after leaving their natal group. This paper reviews our understanding of the evolution of social philopatry and dispersal from the natal group or territory in social mammals. We treat females as philopatric if they remain and breed in their natal range or group and we use natal dispersal to refer to permanent movement out of this area and secondary dispersal to refer to permanent or semi-permanent movements of breeding adults that have previously left their natal group or range. Inevitably, attempts to apply a single definition of dispersal distance face a number of ambiguities (Creel & Creel 2002): for example, in some ungulates, both sexes occupy distinct breeding ranges that are separate from those they use throughout the rest of the year (e.g. Clutton-Brock et al. 1982b; Nelson & Mech 1987). In other cases, individuals of one sex leave their natal group but often settle in part of their natal territory with immigrants of the opposite sex (Creel & Creel 2002). And in some cases, groups sub-divide and occupy part of their original range or parents abandon part of their range to their offspring (Berteaux & Boutin 2000). There is no single definition that is entirely satisfactory in all circumstances and, in such cases, we treat individuals that have left their natal group and associate with unrelated animals of the opposite sex as having dispersed. We initially describe contrasts in female philopatry between and within species (section ‘Variation in female philopatry and dispersal’) before reviewing the benefits of philopatry (section ‘The benefits of philopatry’) and dispersal (section ‘The benefits of dispersal’) and the evolution of species differences in female philopatry (section ‘Species differences in female philopatry’), and of sex differences in dispersal (section ‘The evolution of sex differences in philopatry’).

Variation in female philopatry and dispersal Different species of mammals show marked contrasts in the frequency of reproductive philopatry and natal dispersal in females as well as in the incidence of secondary dispersal (Pusey 1987; Nunes 2007). At one

extreme, are species, like many cercopithecine primates, where most females have spent their entire lives in their natal group, female immigration into other groups is rare or nonexistent and the formation of new groups is uncommon. In these species, most female group members are matrilineal relatives though, where group size is large and female lifespans are long, groups can include several matrilineal sub-groups whose members often compete with each other (Silk 2007). Since females that leave their natal group are seldom able to join other established breeding groups and the formation of new breeding groups is uncommon, most successful cases of female dispersal involve groups fissioning and occupying a part of their previous range, as in some social rodents, several bats and many baboons and macaques (Altmann et al. 1985; Armitage 1991; Alberts & Altmann 1995; Hoogland 1995; Thierry 2007; Kerth 2008; Armitage et al. 2011). In most of these species, males habitually disperse to join other groups at or soon after adolescence so that male and female group members are seldom close relatives (Pusey & Packer 1987) but, in a few species, including killer whales and pilot whales, both females and males commonly remain in their natal group but females typically mate with members of other social groups (Amos et al. 1993; Baird 2000). In addition, in naked mole-rats, both sexes usually remain in their natal group though some males disperse and breeding between close relatives may be common (Honeycutt et al. 1991a,b; ORiain & Jarvis 1997) though females still show a preference for unrelated males (Clarke & Faulkes 1999). At the other extreme, there are a number of social mammals where most females leave their natal group or territory as adolescents or young adults and, if they survive, breed in other territories or groups so that resident breeding females are almost always immigrants born in different groups or ranges from the one they breed in, and are seldom closely related to each other. They include two distinct groups of species. First, there are species where breeding females occupy individual ranges or territories (like many of the insectivores and smaller carnivores as well as many rodents) or live in mixed-sex pairs or in groups that include a single breeding female (like many nocturnal carnivores and primates) (Gaines & Mcclenaghan 1980; Sandell 1989; van Schaik & Kappeler 2003; Nunes 2007). In these ‘singular’ breeders, adolescent females may either be evicted from their natal territory by the dominant female or may leave voluntarily. Though females do not move as far as males in some species, they rarely breed in their natal territory, so it is appropriate to regard them as having dispersed. Second, there are a small number of ‘plural’ breeders where several breeding females live in groups defended by one or  2011 Blackwell Publishing Ltd

P H I L O P A T R Y A N D D I S P E R S A L I N F E M A L E M A M M A L S 475 more males and almost all females leave their natal breeding group as adolescents or young adults and join other breeding units, so that female group members are typically unrelated. Examples include most social equids, several tropical bats, spider monkeys and woolly spider monkeys, red colobus monkeys, hamadryas baboons and all three of the African great apes (Wrangham 1980; Berger 1987; Pusey 1987; Strier & Ziegler 2000; Korstjens & Schippers 2003; Hammond et al. 2006; di Fiore & Campbell 2007; Stumpf 2007). In many of these species, social bonds between breeding females are weak, groups often disband if the resident male dies or is displaced and secondary dispersal of females is common. Between these extremes lie a wide variety of species where some females breed in their natal groups and others disperse to breed. In some species, many females leave as adolescents or young adults but a proportion remain and breed in their natal group: for example, in meerkats dominant females evict all subordinates above a threshold age, so that groups include one mature breeding female and several younger subordinates (Clutton-Brock et al. 2006). In many of these species, dispersing females are usually prevented from joining established breeding groups by residents so that, unless they displace resident females, dispersers either establish new breeding groups or die: examples include African lions, meerkats, golden lion tamarins, red howler monkeys and black-tailed prairie dogs (Pusey & Packer 1987; Crockett & Pope 1993; Hoogland 1995; SilleroZubiri et al. 1996; Creel & Creel 2002; Clutton-Brock et al. 2006; Vander Waal et al. 2009). In other cases, dispersing females are sometimes able to join established groups so that breeding groups may include a mixture of related and unrelated females, as in some Asian colobine monkeys (Kirkpatrick 2007) and some ungulates where related females forage independently but share overlapping home ranges (Clutton-Brock et al. 1982a). Finally, in many of the more wide ranging semi-migratory or migratory species, including some bats and several of the larger herbivores, bonds between mature females are often weak or absent and adolescent females disperse into local populations after separating from their mothers (Estes 1974; Clutton-Brock et al. 2002; Kerth 2008b). However, if populations are geographically divided or opportunities for dispersal are constrained, related females may still encounter each other more frequently than unrelated females (Pratt & Anderson 1985; Bashaw et al. 2007; Bradley et al. 2007; Kerth 2008a, b). The proximate causes of female dispersal also vary. In some species, adolescent females or young adults are evicted from their natal group by adult females who are frequently close relatives: for example, in meerkats,  2011 Blackwell Publishing Ltd

females only disperse after the dominant female in their group drives them out by force (Clutton-Brock et al. 1998). In others, including many rodents and some primates, dispersing females appear to leave their group voluntarily (Bekoff 1977; Moore & Ali 1984; Wolff 1993; Nunes 2007). Within species, the relative frequency of dispersal commonly increases with group size (Pope 2000; Clutton-Brock et al. 2008; Vander Waal et al. 2009) or with local population density (Matthysen 2005) and is reduced by experimental reductions in population density (Brody & Armitage 1985; Aars & Ims 2000). In many mammals, social dispersal represents a conditional strategy and the probability that individuals will leave their natal group and the timing of leaving are affected by their relative size, condition and development of individuals and, in some cases, by their genotype, too (Bowler & Benton 2005; Nunes 2007; Ronce 2007; Clobert et al. 2009): for example, female meadow voles that are malnourished during early development but are well nourished as adults show a stronger tendency to disperse (Bondrup-Nielsen 1993). In some cases, smaller and more subordinate individuals are more likely to disperse (Hanski et al. 1991; Bowler & Benton 2005) while, in others, larger or heavier individuals are more likely to disperse (Nunes et al. 1998; Clutton-Brock et al. 2002). Rates of female dispersal and, in some cases, dispersal distance, are also commonly associated with variation in hormone levels: for example, experimental increases in androgen levels at the time of birth raise the tendency for female ground squirrels to disperse as adolescents or young adults (Holekamp 1984; Nunes et al. 1999). In addition, the availability of vacant territories may be important. For example, studies of several group-living birds and mammals show that the frequency of dispersal increases with the availability of vacant territories or breeding opportunities outside the group (Dobson 1981; Brody & Armitage 1985; Komdeur et al. 1995; Ekman et al. 2004). Conversely, the probability that individuals will remain in their natal group may be affected by chance of breeding there. For example, as mothers age and their probability of survival falls, the relative benefits of philopatry to their daughters are likely to increase and studies of common lizards show that the offspring of older mothers are less likely to disperse (Ronce et al. 1998). In a number of species where females live in relatively large groups, cohesion declines as group size increases and large groups may fission into two or more new groups (Henzi et al. 1997; Waterman 2002; Lefebvre et al. 2003; Archie et al. 2006). When groups split, maternal kinship commonly affects which group individuals eventually belong to and fissioning often raises coefficients of relatedness between group members (Chepko-Sade et al. 1979a, b; Van Horn

476 T . H . C L U T T O N - B R O C K and D . L U K A S et al. 2007). In species where paternal kin tend to associate, paternal kinship, too, may influence the membership of sub-groups. For example, studies of baboons, macaques and gorillas show that when troops fission paternal relatives also tend to join the same sub-group (Smith 2000; Widdig et al. 2006; Nsubuga et al. 2008). Variation in kinship between neighbouring groups may also affect the distance moved. For example, in high density populations of African lions, females are less likely to disperse from prides surrounded by large numbers of unrelated females and, when prides fission, daughters settle relatively close to their mother’s pride (Vander Waal et al. 2009). The size of dispersing splinter groups also differs between species. Where females occupy separate ranges or territories, individuals usually disperse alone and independent dispersal is also common in species where females are readily accepted into established breeding groups. In contrast, where dispersing females cannot join established breeding groups, several females often disperse together: for example, in meerkats, several females are commonly evicted at the same time and often disperse together (Clutton-Brock et al. 1998). Similarly, in banded mongooses, established breeding females evict multiple younger females in sporadic eviction events and younger females disperse together and either die, join established breeding groups or found new breeding units (Gilchrist 2008; Cant et al. 2010). Where females disperse together, new breeding units often consist of a mixture of descendant and nondescendant relatives, though dominant females may subsequently evict non-descendant relatives so that established groups eventually consist of a dominant female and her descendant kin (Young et al. 2006; Clutton-Brock et al. 2008). In cases where dispersal occurs primarily through group fission, as in many of the baboons and macaques (Okamoto 2004), members of the same matrilineal group join the same sub-group and are seldom evicted, so that many breeding units include a mixture of descendant and non-descendant relatives. The age at which females disperse differs widely between species. In plural breeders where female dispersal usually involves groups fissioning, splinter groups commonly involve old as well as young females and dispersal may occur in females of any age (Okamoto 2004). Where breeding females occupy separate ranges or territories, subordinates usually leave (or are evicted) soon after reaching sexual maturity (Nunes et al. 1997). In contrast, in singular cooperative breeders, females may remain in their natal group as nonbreeders for several years before they leave or are evicted: for example, in meerkats, females reach sexual maturity at a year but are seldom evicted from their

natal group until they are at least 2-years old, though few are tolerated after they are 4 years (Clutton-Brock et al. 2008). Different species of cooperative breeders differ in the age at which natal females are evicted and these differences have an important influence on the size of social groups. Finally, the distances moved by dispersing females range from less than a hundred metres in some rodents (Gaines & Mcclenaghan 1980; Jones 1987; Stenseth & Lidicker 1992), through distances of a few hundred metres in the case of the more sedentary primates (Pope 2000) to 20 km or more in some carnivores (Creel & Creel 2002) and much larger distances in some cetaceans (Whitehead & Weilgart 2000). Intraspecific variation in the distance moved can be affected by the kinship structure of local groups. For example, in high density populations of African lions, females are less likely to disperse from prides surrounded by large numbers of unrelated females and, if prides fission, daughters settle relatively close to their mothers (Vander Waal et al. 2009). Interspecific differences in the distances moved reflect variation in relative mobility (Sutherland et al. 2000) as well as differences in the availability of vacant habitat, which is likely to be inversely related to variation in survival. In addition, a substantial number of studies have shown that there are often marked differences in the average distance moved between the sexes and the origin of these differences is still debated (see below).

The benefits of philopatry Dispersal from the natal group often has high costs unless dispersing females can join other breeding groups (Berger 1987; Van Vuren & Armitage 1994; Nunes 2007; Ronce 2007; Doligez & Part 2008; Strier 2008). In many species, dispersing individuals are likely to lack detailed knowledge of the distribution of resources accrued by older residents, their feeding efficiency may be impaired and cortisol levels may be increased to a level where immune responses are affected: for example, studies of African elephants feeding in a novel environment show that foraging efficiency increases and foraging time declines as they get to know the area (Pinter-Wollman et al. 2009). Similarly, dispersing meerkats have lower rates of weight gain while foraging than residents, levels of glucocorticoids rise and they suffer higher parasite load (Young & Monfort 2009). As well as affecting survival, the energetic costs of dispersal may delay breeding and reduce reproductive potential (Ronce 2007; Fisher et al. 2009). Individuals that disperse to unfamiliar areas may also be more vulnerable to predators: for example, experimental studies show that dispersing white-footed  2011 Blackwell Publishing Ltd

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sisting largely or exclusively of unrelated females (Crockett & Pope 1993); and, in white-faced capuchins, the length of inter-birth intervals are negatively related to the number of matrilineal kin in their group (Fedigan et al. 2008). Where comparisons of breeding success or survival between philopatric individuals and dispersers are based solely on observational data, there is a danger that local variation in habitat quality generates consistent differences in survival rates in successive generations, leading to correlations between breeding success and association with kin that have no causal basis. However, several rodent studies that have either manipulated the proportion of relatives in local populations or housed animals with kin versus non-kin have shown that the presence of kin exert distinct effects on breeding success or survival: for example, experiments with several voles show that associating with kin increases fecundity and, in some cases, survival, too (Kawata 1990; Sera & Gaines 1994) though it does not always do so (Boonstra & Hogg 1988; Sera & Gaines 1994; Dalton 2000). Similar effects of the presence of kin have also been demonstrated in house mice (Dobson et al. 2000; Rusu & Krackow 2004), where association with kin increases the lifetime breeding success of females (Fig. 1, Ko¨nig 1994). There are probably several different reasons why associating with kin leads to improved fecundity or breeding success. In many rodents, relatives are more tolerant of each other’s presence than unrelated females, rates of aggression between relatives are lower than between unrelated females and home range overlap

Number of offspring weaned

mice are more susceptible than residents to predation by owls (Metzgar 1967). In addition, they are often likely to be attacked by members of resident groups, sometimes with fatal consequences (Fritts & Mech 1981; Packer & Pusey 1982; Boydston et al. 2001; Creel & Creel 2002). High rates of mortality in dispersers may be particularly common in carnivores, where attacks by residents are likely to be dangerous (Waser 1996): for example, grey wolves making extra-territorial forays die at five times the rate of residents (Messier 1985) while mortality rates in dispersing African wild dogs are 2.7 times higher than those of residents in females and 6.8 times higher in males (Creel & Creel 2002). Several studies have also shown that dispersal is associated with substantial increases in mortality in many other species (Errington 1963; Van Vuren & Armitage 1994): for example, in red howler monkeys, 43–52% of dispersing females are suspected or known to die (Crockett & Pope 1993). As well as suffering the direct costs of moving between groups, dispersing females lose the potential benefits of associating with kin and both empirical results and theoretical models suggest that this may have an important influence on the probability that they will disperse (Lambin et al. 2001; Perrin & Goudet 2001; Silk 2007). Females are often more tolerant of kin than non-kin and associating with kin can have important benefits to breeding success or survival (Silk 2007; Krebs et al. 2007). Some of the clearest evidence comes from studies of rodents where females occupy individual home ranges that overlap those of neighbouring females. For example, in voles, females show a preference for settling close to relatives and individuals with ranges close to kin breed earlier (Pusenius et al. 1998), rear more offspring (Lambin & Yoccoz 1998) and show higher rates of survival in the next breeding season (Lambin & Krebs 1993) than individuals with ranges close to non-kin. In Alpine marmots, infants are more likely to survive their first winter in hibernation groups consisting largely of close relatives than in groups where most individuals are not closely related (Arnold 1990a,b) while the breeding success of dominant females is depressed by the number of unrelated subordinate females in the group but not by the number of daughters present (Hacklander et al. 2003). Similar effects of associating with kin occur in other social mammals: for example, in grey seals, females that breed in areas where individuals are closely related produced larger and faster growing pups than females in areas where relatedness was relatively low (Pomeroy et al. 2000, 2001); in red howler monkeys, females that recruit into their natal group and associate with relatives give birth at earlier ages and have higher breeding success than individuals that disperse and breed in groups con-

First female

15

Second female

10

5

0 Familiar related

Unfamiliar unrelated

Familiar unrelated

Unamiliar/ related

Fig. 1 Effects of the presence of kin on the lifetime breeding success of female house mice in artificial groups (data from Ko¨nig 1994). The median number of offspring weaned within a standardized lifespan in four types artificially created social groups of house mice is the highest if individuals are paired with another female which is both familiar and related. While the first female to start breeding (grey columns) only has a lowered reproductive success when paired with an unfamiliar, unrelated female, the second female (black columns) always produces fewer offspring if not paired with a familiar, related female.

478 T . H . C L U T T O N - B R O C K and D . L U K A S between relatives is often greater (Sera & Gaines 1994; Mappes et al. 1995): for example, the reproductive success of female voles in enclosures seeded with unrelated females is negatively correlated with their proximity to neighbours but this disappears when kin are involved (Mappes et al. 1995; Pusenius et al. 1998). Relatives may also be more tolerant of each other’s offspring and the risk of female infanticide may decline where neighbours are close relatives (Lambin & Yoccoz 1998; Dalton 2000). In addition, related females may assist each other in defending resources or repelling intruders and younger individuals often benefit from the presence of older relatives (Silk 2007): for example, in wood rats, females whose mothers are present in their group produce more offspring than those whose mothers are absent (Moses & Millar 1994) and similar effects occur in some primates (Fairbanks & Mcguire 1987; Pavelka et al. 2002; Cheney et al. 2004). In some voles and mice, several breeding females often nest together, pool their young and nurse them communally and this practice can improve breeding success and reduce rearing costs to females (Koenig 1994; Hayes 2000): for example, in prairie voles (where communal breeding is common) the presence of additional breeding sisters is associated with reduced weight loss in mothers if food is scarce as well as with improved growth in their pups (Hayes 2000). However, communal breeding is not always associated with improved breeding success: for example, in populations of whitefooted mice, some females form communal breeding groups with relatives where population density is relatively high while others breed alone (Wolff 1994) but, in contrast to prairie voles and house mice, there is no obvious effect of communal breeding on reproductive success (Wolff 1994).

The benefits of dispersal The substantial benefits of philopatry suggest that, where females disperse to breed, they must gain large benefits by leaving their natal range or group. Four main categories of benefits have been suggested. First, dispersal may allow subordinate females to escape from groups or ranges where there is intense competition for resources or breeding opportunities with other individuals (Clark 1978; Ekman & Rosander 1992; Perrin & Mazalov 2000; Matthysen 2005; Clobert et al. 2008). In many social species, subordinate females suffer from competition for resources or breeding opportunities with more dominant group members, leading to a reduction in both their fecundity and the survival of their offspring (Clutton-Brock et al. 1982b, 2006; Hoogland 1995): for example, in yellow-bellied marmots, competition between mothers and daughters

often delays the age of first reproduction in daughters with costs to the daughter’s lifetime fitness (Van Vuren & Armitage 1994). In some populations, the proportion of females that disperse increases with population density, supporting the suggestion that females commonly disperse to avoid competition for limited resources. For example, in several social rodents, the probability that females disperse increases with population density (Lidicker & Patton 1987; Nunes 2007). Increased rates of dispersal are often stimulated by short-term changes in resource abundance (Nunes 2007) and dispersing females frequently move to areas of higher food abundance. For example, in Eurasian red squirrels, dispersing females move to areas where food is relatively abundant (Lurz et al. 1997). In other cases, dispersal rates increase if groups exceed the optimal size for their members. For example, in African lions, female dispersal increases in groups that exceed the habitat-specified optimum (Vander Waal et al. 2009). A number of studies have manipulated the local distribution of resources or competitors and shown that this affects patterns of dispersal: for example in California ground squirrels, supplementation of local food resources increases rates of emigration from un-supplemented to supplemented areas (Dobson 1979) while in pocket gophers (Sullivan et al. 2001), yellow-bellied marmots (Brody & Armitage 1985) and California ground squirrels (Dobson 1981) the experimental removal of individuals or groups has been shown to increase immigration from neighbouring areas. However, dispersal is not associated with competition for resources in all cases: for example, in savannah baboons, females normally remain in their natal group or range, even if there is strong competition for resources (Alberts & Altmann 1995) while, in horses, almost all females emigrate from their natal group, even if population density is relatively low and resources are abundant (Berger 1986). Moreover, in some cases, high population density is associated with reductions in dispersal rather than increases: for example, in some rodents the saturation of local environments is associated with reductions in dispersal and increased retention of daughters (and, in some cases, sons) in the natal range (Gundersen & Andreassen 1998; Lambin et al. 2001) while in brown bears, high population density is associated with reduction of the dispersal distance of females (Støen et al. 2006). In addition, social dispersal may allow females to escape from attempts by dominant females to restrict their ability to conceive, breed and raise young. In some species where females defend individual territories as well as in some socially monogamous species, young adult females become the target of aggression from the resident breeding female (who is often their mother) and are eventually forced to leave (Tilson 1981; Komers  2011 Blackwell Publishing Ltd

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(a)

Keep territory

0.6 n = 124

0.4

0.2

0

0

40

(b)

80 120

160

200

240

280

240

280

Share territory

0.6 n = 134

0.4

Percentage of individuals

& Brotherton 1997; Nunes 2007). Similarly, in some singular cooperative breeders (including meerkats, African wild dogs and tamarins) older subordinate females become the target of aggression from dominant females and eventually leave the group or are evicted (Dietz & Baker 1993; Clutton-Brock et al. 1998; Creel & Creel 2002; Goldizen 2003). In several of these species, the probability that subordinates will be evicted rises with group size (Clutton-Brock et al. 2008; Cant et al. 2010) and increase at times when dominants or subordinates are attempting to breed (Clutton-Brock et al. 1998b; Ebensperger 1998a,b; Creel & Creel 2002). In other species, younger females appear to leave voluntarily to seek breeding opportunities in other groups (Komers & Brotherton 1997; Brockelman et al. 1998; Goldizen 2003; McGuire et al. 2007). Second, theoretical analyses of dispersal have suggested females may disperse to avoid the indirect costs of competing with kin (Hamilton & May 1977; Gandon 1999; Perrin & Mazalov 2000). However, there is little or no evidence that the presence of maternal kin commonly stimulates voluntary dispersal, after the effects of local density or group size on dispersal frequency have been allowed for (Wolff 1992; Lambin et al. 2001). For example, in root voles, adolescent females exposed either to their mother or to an unrelated breeding female were no more likely to show reproductive suppression or to attempt to disperse in the presence of their mother than in the presence of an unrelated female (Le Galliard et al. 2007). Conversely, in several species, there is evidence that breeding females are more tolerant of closer relatives than of more distant relatives of unrelated individuals and that this is associated with reduced rates of dispersal in close kin. For example, subordinate female meerkats are less likely to be evicted from their natal group by the dominant female if they are close relatives (Clutton-Brock et al. 2010). While in yellow-bellied marmots, the presence of a female’s mother reduces the probability that she will disperse (Armitage et al. 2011), probably because mothers provide support that enhances the ability of younger females to compete with other colony members (Bekoff 1977). In addition, in a number of species that rely on predictable, localised resources, including red squirrels (Price & Boutin 1993; Berteaux & Boutin 2000) and Columbian ground squirrels (Harris & Murie 1984), breeding females that have reared offspring alter their ranging behaviour (Fig. 2), leaving their offspring to use part of their previous range (Nunes 2007). Strategies of this kind are probably best interpreted as examples of extended parental care and, as yet, there is no evidence that females treat non-descendant kin in the same way.

0.2

0

0

40

(c)

80 120

160

200

Bequeath territory

0.6 n = 29

0.4

0.2

0

0

40

(d)

80 120

160

200

240

280

80 120 160 200 240 Distance moved (m)

280

Juveniles

0.6 n = 189

0.4

0.2

0

0

40

Fig. 2 Bequeathal in red squirrels (data from Berteaux & Boutin 2000). The distances individual red squirrel females move between breeding seasons. While most adult female red squirrels remain in their territory after a breeding attempt, and either keep it (a) or share it with their daughter (b), some adult females disperse before the next breeding attempt (c). This allows some daughters to stay and inherit the territory (d) even though their mother is still alive. The average diameter of the territory is 42 m for an adult female red squirrel.

Third, females may leave their natal area to reduce the chance that their dependent young will be killed by predators or immigrant males. Where males that have recently immigrated into breeding groups are likely to kill dependent offspring, females with infants often leave groups following recent male take-overs (Hrdy 1977; Sterck & Korstjens 2000; Teichroeb et al. 2009; Zhao et al. 2011) and may even anticipate the risk of take-over and male infanticide by leaving groups which are not defended effectively by the resident male (Steenbeck 2000, Stokes et al. 2003). Finally, females may benefit from dispersal from their natal group because it allows them to gain access to unrelated males and to avoid inbreeding with close relatives (Bengtsson 1978; Greenwood 1980; Pusey 1987; Koenig & Haydock 2004). In most social mammals that live in stable groups, offspring of one sex (usually males) typically disperse to breed in other groups and the incidence of close inbreeding within the group is consequently low (Greenwood 1983; Pusey 1987) but in some species where males have relatively long breeding tenure, female dispersal plays an important role in minimising the chance of breeding with close relatives (Berger 1986; Clutton-Brock 1989; Nunes 2007). Several different kinds of evidence support the suggestion that inbreeding avoidance has played a role in the evolution of female dispersal. There is substantial evidence that, in animals that usually outbreed, mating with close relatives lowers average levels of heterozygosity among offspring and increases the chance that they will be homozygous for deleterious recessive alleles likely to reduce fitness (Morton et al. 1956; Charlesworth & Charlesworth 1987; Keller & Waller 2002). As a result, female fecundity is often reduced when partners are close relatives and so, too, is the viability and breeding success of their offspring (ungulates: Ralls et al. 1979; Slate et al. 2000; Marshall et al. 2002; rodents: Hill 1974; Haigh 1983; Pugh & Tamarin 1988; Keane 1990; Reeve et al. 1990; Krackow & Matuschak 1991; Hoogland 1992; insectivores: Stockley et al. 1993; carnivores: Packer & Pusey 1983; primates: Bulger & Hamilton 1988; Dietz & Baker 1993; Alberts & Altmann 1995; other mammals: Pusey & Wolf 1996; Frankham et al. 2002). The immediate causes of reductions in offspring fitness vary but can include reduced growth and survival (Fig. 3, Jimenez et al. 1994), later age at first breeding, lower fecundity, reduced survival of offspring, shorter lifespans, increased susceptibility to disease or parasites and reduced lifetime breeding success (Fig. 4, Slate et al. 2000) (AcevedoWhitehouse et al. 2003; Wilson et al. 2004). There is also extensive evidence that females avoid breeding with close relatives. Females whose fathers or brothers are reproductively active in their group when they reach sexual maturity commonly either avoid

Cumulative survival probability

480 T . H . C L U T T O N - B R O C K and D . L U K A S

0.5

Non-inbred Inbred

0.4 0.3 0.2 0.1 0 0

2

4

6

8

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Weeks after release

Fig. 3 Effects of inbreeding on survival in free-ranging whitefooted mice (data from Jimenez et al. 1994). Survivorship of inbred (open circles and dashed line) and non-inbred (solid diamonds and solid line) mice over 10 weeks after first capture. Non-inbred animals had higher survivorship than inbred animals during all six times, and the combined cumulative effect as shown above is statistically significant.

Fig. 4 Effects of standardised heterozygosity on lifetime breeding success in male and female red deer (from Slate et al. 2000). Female Lifetime Breeding Success (LBS) was adjusted for the effects of density and weather in the year of birth. Relationships are significant in both sexes.

mating with them, delay breeding or leave the group (Packer 1979; Hoogland 1982, 1995; Armitage 1984; Smale et al. 1997; Nunes 2007): for example, in dwarf mongooses and African wild dogs, adolescent females are more likely to disperse from their natal group if their father is still monopolising access to the group than if he has emigrated or is dead (Rood 1987; McNutt 1996) and, in voles, the presence of unfamiliar males in neighbouring territories stimulates dispersal in females (Mcguire & Getz 1991). In mountain gorillas, females that mature in groups where the only breeding male is their father usually disperse before breeding while those maturing in groups where there is a second breeding male commonly breed at least once in their natal group (Harcourt & Stewart 2007). Experimental studies of rodents confirm that the presence of  2011 Blackwell Publishing Ltd

P H I L O P A T R Y A N D D I S P E R S A L I N F E M A L E M A M M A L S 481

Percentage becoming sexually mature

closely related males can stimulate female dispersal: for example, meadow voles released in groups into experimental grassland plots are more likely to disperse from their release site if other members of the group are kin than if they are unrelated (Bollinger et al. 1993). Similarly, female white-footed mice whose fathers are still resident in their territory are less likely to become sexually mature before dispersing than those whose mothers are present while those whose mothers are present are no less likely to mature than those lacking both parents (Fig. 5, Wolff 1992) and experimental removal of fathers causes daughters to remain longer in their natal territory while the presence of mothers in the natal territory has similar effects on sons. Finally, habitual female dispersal occurs in species where the reproductive tenure of males exceeds the age of females at first breeding and the rise of close inbreeding is consequently high (see section ‘Species differences in female philopatry’). The relative importance of the different benefits of dispersal are still widely debated (Waser & Jones 1983; Bowler & Benton 2005; Ronce 2007; Clobert et al. 2008). While there is general agreement that females commonly disperse to avoid competition or persecution, there is still disagreement about the importance of inbreeding avoidance as an ultimate cause of female dispersal. Although some scientists argue that it plays an important role (Pusey 1987; Clutton-Brock 1989; Roze & Rousset 2005; Nunes 2007; Szulkin & Sheldon 2008), others are more sceptical (Moore & Ali 1984; Guillaume & Perrin 2006; Clobert et al. 2008), and some theoretical models suggest that inbreeding avoidance is unlikely on its own to account for the evolution of dispersal, though it may modify other mechanisms favouring dispersal (Perrin & Mazalov 1999; Perrin & Goudet 2001). 100

Sons

Daughters

Opposite-sex parent present

Both parents present

80 60 40 20 0 Same-sex parent present

Neither parent present

Fig. 5 Effects of the presence of like and unlike-sexed parents on the development of sexual maturity in white-footed mice (data from Wolff 1992). While in the absence of the opposite sex parent juvenile white-footed mice rapidly become sexually mature, they are inhibited in their presence. No son (grey columns) became mature if the mother or both parents were still present in the homerange, and only few females (black columns) became sexually mature in the presence of their father in the homerange.  2011 Blackwell Publishing Ltd

In part, disagreements over the relative importance of inbreeding avoidance in stimulating dispersal reflect variation in definitions of dispersal and philopatry. Many reviews of variation in female philopatry in species that live in stable social groups have concluded that the risk of close inbreeding is a common cause of female dispersal (Pusey 1987; Clutton-Brock 1989) whereas analyses of dispersal distance are often sceptical of the role of inbreeding avoidance and emphasise the importance of ecological parameters (Clobert et al. 2008). Both may well be correct. Evidence that inbreeding avoidance can play an important role in stimulating dispersal from the natal group is strong (Wolff 1992; Szulkin & Sheldon 2008) and the diversity of factors affecting dispersal by females does not (as is sometimes argued) weaken the case that females avoid inbreeding with close relatives and that this can be an important factor constraining female philopatry and promoting dispersal from the natal group (Dobson & Jones 1985; Lambin et al. 2001). However, this need not necessarily suggest that individuals continue to avoid mating with kin after they have left and several studies have found little evidence that dispersers avoid joining close relatives or mating with kin (Keller & Arcese 1998; Daniels & Walters 2000; Szulkin & Sheldon 2008). For example, studies of reindeer found no evidence that females avoided joining the mating groups of related males (Holand et al. 2007) and research on black bears has found no evidence that females avoided mating with any of the males present in the neighborhood (Costello et al. 2008), though studies of some small mammals have found that dispersing females that have left their homerange or group do avoid mating familiar kin (Dewsbury 1988; Ferkin 1990; Pusey & Wolf 1996; Le Galliard et al. 2007). A possible explanation is that these differences are a consequence of interspecific contrasts in mobility: in relatively sedentary species, where individuals live in small, discontinuous populations, the chance that dispersing females will encounter close relatives may be high, generating selection for discrimination against related partners while, in relatively mobile species, individuals that leave their natal group may be unlikely to encounter close relatives after leaving their group so that selection to discriminate against them is weak and the distance moved by dispersing females may depend primarily on the availability of resources, vacant habitat and breeding opportunities (Koenig & Haydock 2004; Clobert et al. 2008).

Species differences in female philopatry Arguments concerning the role of inbreeding in stimulating female dispersal have focussed attention on

482 T . H . C L U T T O N - B R O C K and D . L U K A S the evolution of species differences in philopatry and dispersal (see section ‘Introduction’). Evidence that female philopatry is common and dispersal often has substantial costs suggests that remaining on the natal range or territory is usually the optimal strategy for females. Explaining the evolution of habitual female dispersal in singular breeders presents little difficulty since subordinate females either leave voluntarily to find opportunities to breed or are evicted by the dominant female. In contrast, the evolution of female dispersal in the relatively small number of plural breeders where females habitually disperse at adolescence is less easy to explain. In these species, female dispersal typically occurs in low as well as high density populations (Berger 1986; Harcourt & Stewart 2007) so that it is unlikely to represent a facultative response to local food shortage. Though it is sometimes suggested that phylogenetic history may explain much of this variation (Perrin & Mazalov 1999), the presence of marked contrasts in dispersal between closely related species, the flexibility of mammalian dispersal and evidence of recent evolutionary changes in dispersal in other species argue against this conclusion. Two main explanations for the evolution of habitual female dispersal have been suggested. One, originally suggested by Wrangham (1980) for primates, and later developed by other primatologists (van Schaik 1989; Sterck et al. 1997; Koenig 2002; Isbell 2004), argues that habitual female dispersal occurs in species where the value of individual food items is low and contest competition within groups is either rare or has little effect on fitness. Under these conditions (it is suggested), linear hierarchies and supportive coalitions may be unlikely to develop, the benefits of associating with kin may be low and females may commonly disperse to avoid competing for resources. Although this explanation of contrasts in dispersal was initially widely accepted, recent reviews have stressed its shortcomings (Janson & van Schaik 2000; Koenig & Borries 2006; Thierry 2008). Attempts to estimate and compare the relative intensity of resource competition in different species are fraught with difficulties and it is not clear that competition for resources is less frequent or less intense among primates where females habitually disperse than among species where females are philopatric (Snaith & Chapman 2007; Thierry 2008). There does not appear to be any close association between female philopatry and diet quality or food distribution, either across primate species or across other mammals. And, although linear female dominance hierarchies and supportive coalitions may be more frequent in species where females are philopatric, this may reflect the fact that females typically remain in the same group for most or all of their lives.

The second suggestion is that habitual female dispersal occurs in species where the breeding tenure of individual males or of all male kin groups commonly exceeds the age at which most females are ready to breed, causing females to leave their natal groups to avoid the risk of inbreeding with their fathers and to locate unrelated partners (Berger 1986; Clutton-Brock 1989; Harcourt & Stewart 2007). Many of the species where females habitually disperse to breed, including some groups of tropical bats, the social equids and the great apes, are relatively long-lived and the average tenure of breeding males or male kin groups commonly exceeds the average age of females at first breeding whereas, in most social mammals where females are philopatric, the average tenure of males is shorter than the age at which females start to breed (Clutton-Brock 1989; Lukas & Clutton-Brock in press). Similarly, in most group-living birds (where female-biased dispersal is common), both sexes are relatively long-lived (Arnold & Owens 1998) and females are often mature by their second year of life, when their father is often likely to still be active in their group so that the risk of inbreeding would be high if females remained in their natal group (Clutton-Brock 2009; Clutton-Brock & McAuliffe 2009). However, the sample of plural breeding mammals where females normally disperse to breed is still small and there are several species (including capuchin monkeys, killer whales and banded mongooses) where females commonly remain in their natal group despite the presence of their father or brothers and either breed with more distantly resident males or with males from other groups (Baird 2000; Perry et al. 2008; Nichols et al. 2010). It is not yet clear why this strategy is not more widely adopted but a possible explanation is that females habitually disperse in species where resident males are able to control their access to extra-group partners. This explanation of habitual female dispersal emphasises the need to understand the causes of variation in male breeding tenure. Unfortunately, estimates of male tenure are available for too few mammals for quantitative comparisons to be reliable and the available evidence suggests that a substantial number of ecological and social factors may affect male tenure. Comparative evidence suggests that male tenure is typically longer in socially monogamous vertebrates than in polygynous ones, probably because increased breeding competition between males increases rates of turnover in breeding males in polygynous species (Clutton-Brock & Isvaran 2007). Extrinsic rates of male mortality may also be important: for example, mortality rates are relatively low in male hamadryas baboons and gorillas as well as in the social equids (Sigg et al. 1982; Berger 1987; Harcourt & Stewart 2007). Life-history adaptations, too, may be involved. For example, in African  2011 Blackwell Publishing Ltd

P H I L O P A T R Y A N D D I S P E R S A L I N F E M A L E M A M M A L S 483 lions, the synchronous production of relatively large numbers of cubs generates dispersing male sub-groups capable of displacing resident groups of males, leading to relatively high rates of turnover of resident male groups (Packer et al. 1988) with the result that the risk of father ⁄ daughter mating is reduced and females can remain and breed in their natal group (Clutton-Brock 1989), whereas in chimpanzees, rates of reproduction are low, males rarely leave their natal community and male kin groups appear to have indeterminate tenure in their community (Goodall 1986; Wrangham 1986). Finally, social adaptations may play a part: for example, the formation of bachelor groups of males that regularly invade breeding groups and displace resident males (Sugiyama 1965a,b; Hrdy 1977; Borries & Koenig 2000) may help to account for the relative short tenure of Hanuman langurs.

The evolution of sex differences in philopatry The functional significance of sex differences in dispersal and philopatry are also controversial (see Greenwood 1980; Dobson 1982; Moore & Ali 1984; Johnson 1986; Packer 1986; Wolff 1993; Perrin & Mazalov 2000; Perrin & Goudet 2001). A number of different reasons why males are more likely than females to leave their natal group have been suggested. First, because of their higher reproductive rate and the resulting increase in reproductive competition, resident, dominant males may be less likely to tolerate adolescent males than females are to tolerate adolescent females, raising dispersal rates in males (Greenwood 1980; Shields 1982; Smale et al. 1997). Alternatively, males may be able to gain greater benefits than females by dispersing to groups with low male:female ratios and local mate competition may exert a stronger influence on fitness in males than in females (Greenwood 1980; Shields 1987; Perrin & Mazalov 2000; Gros et al. 2009). The energetic costs of dispersal may also be higher in females than in males because of their heavier energetic investment in reproduction and females may also gain greater direct benefits than males from remaining in their natal group and associating with close relatives (Sherman 1977; Wrangham 1980; Johnson 1986; Gandon 1999): experimental studies involving manipulations of food availability or local density confirm that they often have stronger effects in females (Dobson 1979; Dobson & Kjelgaard 1985; Nunes & Holekamp 1996; Smale et al. 1997). While several different factors may contribute to the evolution of sex differences in dispersal and philopatry among mammals, the simplest explanation of the prevalence of female philopatry is that, where male tenure is shorter than the age at which females disperse so that female seldom mate in a group where their father is the  2011 Blackwell Publishing Ltd

resident breeding male, the high costs of dispersal favour female philopatry (see section ‘The benefits of philopatry’), while female avoidance of mating with philopatric males (on account of the costs of inbreeding) generates selection on younger males to disperse to find willing mates (see section ‘The benefits of dispersal’): for example, in spotted hyenas, adolescent males that immigrate into the clan with the highest number of young females have the highest long-term reproductive success (Ho¨ner et al. 2007). Where dominant males can often maintain their position for periods longer than the age of females at first breeding, they may be unlikely to abandon their position despite any costs to females because the loss of direct fitness associated with leaving a group where they are an established dominant exceeds any indirect fitness costs associated with breeding with related females. Under these circumstances, maturing females that do not have access to other unrelated males may be forced to leave to find unrelated partners and, once female dispersal has evolved and female immigration is common, philopatry may represent the optimal strategy for natal males if they are tolerated by dominants. The formation of kin groups of philopatric males is not common in mammals, but occurs in several species where females habitually disperse as adolescents, including feral horses, Ethiopian wolves, hamadryas baboons and gorillas (see Harcourt & Stewart 1981; Clutton-Brock 1989; Robbins 1995, 1996, 1999; SilleroZubiri et al. 1996). In an even smaller number of mammals, both sexes may remain and breed in their natal group throughout their lives. These appear to fall into two categories. First, there are species where males as well as females typically outbreed with members of other groups when they meet. Breeding systems of this kind include resident groups of killer whales (Heimlich-Boran 1986; Hoelzel et al. 1991; Baird 2000) and, possibly, pilot whales (Amos et al. 1993; Heimlich-Boran 1993). Second, in naked mole-rats, both males and females may remain in their natal group throughout their lives and often breed with close relatives (Alexander et al. 1991; Bennett & Faulkes 2000). However, recent studies suggest that male dispersal in naked mole-rats is more common than was previously supposed to be the case and that females prefer to mate with unrelated males (Braude 2000). Why bisexual philopatry has evolved in killer whales is still unknown and it would be useful to investigate the costs of dispersal to individuals that leave their natal groups. One of the most widely cited contrasts in dispersal is the tendency for dispersal to be female-biased in social birds and male-biased in social mammals (see Greenwood 1980, 1983; Greenwood & Harvey 1982; Pusey & Wolf 1996; Clarke et al. 1997). Several reviews

484 T . H . C L U T T O N - B R O C K and D . L U K A S and theoretical papers have sought to explain this difference (see Greenwood 1980; Dobson 1982; Pusey & Wolf 1996; Perrin & Mazalov 2000). For example, Greenwood (1980) argued male birds benefit more than females from remaining close to their original territory because effective territorial defence is facilitated by knowledge of the area whereas male mammals typically breed polygynously and defend groups of females (see also Shields 1987). Other suggestions are that female birds may be less tolerant of their daughters because they are capable of adding eggs to clutches while female mammals cannot pursue a strategy of this kind (Liberg & Vonschantz 1985); that the costs of dispersing to females may be higher in mammals than birds as a consequence of their large energetic investment in lactation (Johnson 1986); that the relative intensity of Local Mate Competition and Local Resource Competition may favour male dispersal in mammals and female dispersal in birds (Dobson 1982; Perrin & Mazalov 2000); and that, as a result of their ability to identify eggs laid by others, female birds can monopolise breeding success more effectively in birds than female mammals, so that the relative breeding success of subordinates is reduced (Raihani & Clutton-Brock 2010). A final possibility is that, as in some mammals, the breeding tenure of males in many breeding groups of birds exceeds the age at which females start to breed, generating selection on females to disperse to locate unrelated partners (see above). The available data on male tenure in group-living birds suggests that this may well be the case: life expectancy is typically high in both sexes (Arnold & Owens 1998) while females generally enter breeding condition in their second year of life (Bennett & Owens 2002) and so are likely to mature in groups where the established breeding male is a close relative (CluttonBrock 2009). Like previous explanations, this hypothesis links the contrast between birds and mammals to the incidence of polygyny in mammals – but instead of suggesting that polygyny affects the probability that males will be evicted or the benefits they can derive from moving to new groups, it argues that polygyny reduces the average tenure of males in breeding groups so that females rarely need to disperse from their natal group to obtain access to unrelated males (Clutton-Brock 2009).

Discussion This review of dispersal and philopatry in female mammals suggests four main conclusions. First, that philopatry commonly has substantial benefits to females, including the maintenance of a detailed knowledge of food distribution and escape routes and toleration or support from matrilineal kin while, unless females can move rapidly between groups, dispersal often has sub-

stantial costs in terms of survival and breeding success. Second, that in species where breeding females are usually recruited from animals born in the group, the frequency of female dispersal is affected by a range of ecological and behavioural factors, including the frequency and intensity of local competition for resources and mates, reproductive interference or suppression by dominant females, the risk of male infanticide, the presence of female relatives and the individuals’ own size and status. Third, that, evolution of habitual female dispersal is associated with the relative duration of male tenure and occurs in species where females that breed in their natal group would lack access to unrelated partners (Clutton-Brock 2009). Finally, the relative importance of different ecological and evolutionary mechanisms in affecting dispersal and philopatry depend on scale. For example, while the avoidance of close inbreeding may play an important role in promoting dispersal from the natal group, there is little evidence that it has important effects on dispersal distance or on the frequency of dispersal between sub-populations or demes which is more commonly affected by ecological parameters. In addition, this review emphasises important limitations in our understanding of the evolution of philopatry and dispersal. We need to know considerably more about the distribution of philopatry and the factors that affect it. A widespread problem here is that field studies typically describe the frequency of dispersal and relatively few provide estimates of the proportion of philopatric breeding (i.e. the percentage of breeding females that were born in the group where they breed). Since female dispersal is common in many species where most breeding females are natals, the scarcity of studies that document the origin of breeders impedes investigations of the interspecific distribution of philopatry. We also need to know considerably more about the effects of philopatry and dispersal on the relative breeding success of females that remain in their natal group versus those that disperse and to understand the causes of these differences (Doligez & Part 2008). In contrast to studies of birds (Szulkin & Sheldon 2008), no studies of mammals have yet explored the effects of variation in dispersal distance on the probability of mating with unrelated partners or on breeding success. Where males disperse from groups that include related females, it is still unclear whether they leave groups to increase access to related partners or to avoid the risk of inbreeding with close relatives and experiments that distinguish between these possibilities would be useful. Finally, we need to know more about the probability that relatives will encounter each other as prospective partners after leaving their natal group and about whether or not they continue to avoid breeding with  2011 Blackwell Publishing Ltd

P H I L O P A T R Y A N D D I S P E R S A L I N F E M A L E M A M M A L S 485 relatives once they have dispersed. In particular, it would be useful to test the suggestion that continued discrimination against breeding with relatives is confined to relatively sedentary species where the chance that dispersing relatives will encounter each other is high. Where there is evidence that dispersers do continue to avoid breeding with relatives, we need to determine whether discrimination is based on avoidance of breeding with familiar individuals or whether other forms of kin discrimination are involved. Understanding the consequences of contrasts in the kinship structure of groups generated by differences in female philopatry and dispersal is also important. Where females disperse and female group members are often unrelated, it is suggested that dominance hierarchies are poorly developed and cooperation is rare (Sterck et al. 1997) but no systematic comparisons have yet compared the social behaviour of females in species that show habitual female dispersal with those in species where females are usually philopatric. A possible consequence of female philopatry and male defence of female kin groups is that selection on female mating preferences may be weaker than in species where females disperse and have an opportunity to select between multiple mating partners and this could account for contrasts in the relative development of male ornamentation in mammals and birds (CluttonBrock & McAuliffe 2009) but no studies have yet compared the strength of female mating preferences or their effects on male fitness between species where females are philopatric and species where females disperse. Finally, it is likely that contrasts in female dispersal have important consequences for the dynamics of groups and the regulation of population density, the demographic consequences of variation in female dispersal remain almost totally unexplored (Clutton-Brock 2009). There is still much to be done.

Acknowledgements We are grateful for comments on this manuscript or discussion by Stuart Sharp, Xavier Lambin, Rafael Mares, Sinead English and Matthew Bell. During the preparation of the review, Dieter Lukas was supported by grants from the Leverhulme Trust and the Newton Trust while Tim Clutton-Brock’s empirical research was supported by the Natural Environment Research Council and Earthwatch Institute.

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