While sex-biased dispersal is an almost ubiquitous feature of mammalian life history, there is enormous diversity in terms of the mode of dispersal and in the proximate causes that have been invoked to explain it (Tables 1 and 2). Even in species that are traditionally labelled philopatric (e.g. the banner-tailed kangaroo rat, Winters & Waser 2003), or those in which both sexes disperse (e.g. guanacos, Sarno et al. 2003), there appear to be differences between the sexes in terms of dispersal distance and rate. Dispersal rate is male-biased in the great majority of mammal species (Greenwood 1980; see Table 1 for examples) and males also appear to disperse greater distances than females (Waser 1985). It is important to note that a complete bias, where one sex remains completely philopatric while all individuals of the other sex disperse, is quite rare (e.g. white sifaka, Richard et al. 1993; Bechstein's bat, Kerth et al. 2002; ring-tailed lemur, Sussman 1992; Barbary macaque, Pusey & Packer 1987). In most species, some dispersal also occurs in the typically philopatric sex, even though the magnitude of the bias may be strong. This distinction is important for understanding the evolutionary and proximate causes of sex-biased dispersal, since as mentioned above, theory predicts that if inbreeding avoidance is the only evolutionary cause of SBD, one sex should remain completely philopatric.
Although a few empirical studies have demonstrated a difference in dispersal distance between the sexes (e.g. opposums, Ji et al. 2001; otters, Blundell et al. 2002; shrews, Fontanillas et al. 2004), information is currently quite limited. The distribution of dispersal distances should be very informative for understanding evolutionary causes of dispersal (Murrell et al. 2002; Rousset & Gandon 2002) because the reasons for long-distance and short-distance dispersal are likely to be very different (Ronce et al. 2001). Short distance dispersal is probably sufficient for avoiding inbreeding or kin competition, whereas long distance dispersal might function to colonize a new territory or escape crowding (Perrin & Goudet 2001). Dispersal distance is therefore an important avenue for future research.
The timing of dispersal might also provide interesting clues to ultimate causes. Although it is often assumed that individuals undergo natal dispersal as juveniles (Dobson 1982), the timing of dispersal can be quite variable, which highlights the importance of understanding the species’ life history for genetic analyses (see ‘Measuring sex-biased dispersal’). Belding's ground squirrel males, for example, disperse up to 2 years before reaching sexual maturity (Smale et al. 1997), whereas male forked-marked lemurs wait 3 years after puberty before dispersing (Schülke 2003). Many species undergo secondary dispersal later in life, which is important to distinguish from natal dispersal, since it is likely to be motivated by very different reasons. For example, there is good evidence that close inbreeding avoidance is an important driving force behind natal male dispersal in olive baboons, but secondary dispersal (by about a quarter of all males) is more likely to result from aggressive eviction, which seems to be a more important determinant of secondary transfer than natal dispersal (Packer 1979).
Proximate causes of sex-biased dispersal
Eviction, attraction to members of other groups, and benefits of group dispersal are among the most important proximate explanations for sex-biased dispersal (Tables 1 and 2). Whereas emigration seems voluntary in most species, forceful eviction has been documented in some cases, and as mentioned above, is a potentially important reason for secondary transfer. Eviction is often the result of aggression from adult males in response to increasing maturity of male adolescents (e.g. howler monkey, grey langur, gibbon, Table 1) but is also a consequence of group takeover (e.g. white-faced capuchin, Jack & Fedigan 2004; Table 1). While aggressiveness leading to eviction is more common among males, it has also been documented among females, particularly if low-ranking (e.g. chimpanzees, Pusey & Packer 1987; Table 2, spotted hyenas, Holekamp & Smale 1995; Smale et al. 1997; Table 1). While intrasex eviction points to competition for mates (in males) or resources (in females), intersex eviction (e.g. in white-footed mice, Wolff 1992; several macaque species, Packer & Pusey 1987) invokes inbreeding avoidance as the most likely ultimate cause.
Attraction to sexual partners outside the natal group is a potentially important trigger of dispersal, which is independent of social structure. Extra-group attraction has been shown to drive emigration in several group-living primate species such as chimpanzees, macaques, mangabeys, vervets and guenons (Pusey & Packer 1987; Olupot & Waser 2001; Jack & Fedigan 2004a; Tables 1 and 2). In this case, the timing of dispersal generally coincides with the mating season. Emigration occurs at sexual maturity and clusters around the peak breeding season, suggesting male sexual attraction to extra-group females (Jack & Fedigan 2004a). Olive baboon males, for example, are attracted to oestrus females in neighbouring groups and females may solicit the attention of potential dispersers (Packer 1979). In grey-cheeked mangabeys, spatio-temporal availability of oestrus females is a major proximate factor influencing transfer, and males show a greater tendency to move into new groups that contain higher numbers of oestrus females than their previous group (Olupot & Waser 2001). Generally though, males are not necessarily attracted to groups with many females but rather to groups containing unfamiliar females (Pusey & Packer 1987).
If there is cooperation between relatives (for example in acquisition of resources or in raising young), there are clear benefits to individuals by remaining philopatric. Under these circumstances, cooperation is likely to oppose dispersal. However, this cost can be circumvented if individuals disperse as a group. Parallel dispersal maintains coalitions and familiar relationships for dispersing individuals. Although most mammals tend to disperse individually, parallel dispersal is known in some species (Tables 1 and 2). Dispersing in a coalition may be of particular benefit to immature males in aiding initial entry into a foreign group. In lions for example, coalitions of related males from the same cohort leave the natal group together (Pusey & Packer 1987). Coalitions are more successful at taking over new prides and there are clearly inclusive fitness benefits to subordinate males by dispersing with dominant kin (Pusey & Packer 1987). In white-faced capuchins, 82% of male transfers take place in the company of older maternal siblings or members of the same age cohort, which are likely to be close relatives (Jack & Fedigan 2004a). However, group dispersal might sometimes occur simply because the limited duration of female oestrus influences the period when transfer occurs (e.g. macaques, Melnick & Pearl 1987).
Is sex-biased dispersal linked to social complexity?
An increase in the magnitude of sex-biased dispersal with increased social complexity (i.e. the degree of sociality and communicative complexity) is expected on theoretical grounds, from the interaction between the benefits of kin cooperation and the costs of inbreeding (Perrin & Goudet 2001). Greenwood (1980) noticed that the degree of sociality influences the magnitude of the sex bias in dispersal, and sex differences are indeed particularly striking among long-lived, highly social, polygynous mammals (Pusey 1987; Smale et al. 1997). Moreover, there is also a close link between sex-biased dispersal and social organization in birds (especially communal breeders, e.g. Florida scrub jay, Greenwood & Harvey 1982). In line with prediction, Devillard et al. (2004) found an increase in the magnitude of male-biased dispersal with increasing social complexity in polygynous ground dwelling sciurids (ground squirrels, marmots and prairie dogs). The increased bias, however, was determined solely by an increased male dispersal, and not, as also expected, by a concomitant decreased female dispersal (Perrin & Goudet 2001). Unfortunately, levels of polygyny and sociality are linked, so the correlation between male dispersal rate and social complexity is probably confounded by a mating system effect (Devillard et al. 2004). This important question therefore warrants investigation in other species groups to address the effect of mating system and to establish whether this is a phylogenetically independent pattern.
Exceptions to the rule: female-biased dispersal in mammals
Although female-biased dispersal is rare in mammals (Greenwood 1980), it is found in phylogenetically diverse taxonomic groups, with varying social structures and mating systems, suggesting a wide range of evolutionary and proximate explanations. As is often the case in evolutionary biology, studying the exceptions to a rule can provide unique insights into more general explanations, and we therefore address the patterns and causes of female-biased dispersal in some detail. In Table 2 we provide a summary of all mammal species with FBD for which there is good data available. Inspection of Tables 1 and 2 together reveals four general points.
First, in some cases, several closely related species all exhibit FBD (e.g. Atelidae, Hominidae, Table 2). More often though, both FBD and MBD can be found in groups of closely related species with apparently similar life histories, and in some cases there is phylogenetic evidence that FBD has evolved independently from the ancestral state of MBD (e.g. hamadryas baboons, Hammond et al. 2006). Second, although mating system is often considered to be a good predictor of direction of SBD, dispersal is male-biased in several monogamous species (Table 1), and several polygynous species have predominantly female dispersal (Table 2), suggesting that the hypothesis of Greenwood (1980) is too simplistic. Third, several species that live in one male units (OMUs), which are known to have high local mate competition, exhibit FBD (e.g. hamadryas baboons, gorillas, horses). These first three points illustrate the enormous diversity in terms of taxonomy, mating system, social unit and the direction of sex-biased dispersal. Finally, there appears to be an overrepresentation of primates with FBD compared to other mammal groups, but it is unclear whether this reflects the disproportionate investment in field studies of these species (highlighted by the high representation of primate species in both Tables 1 and 2), and good quality data is needed from other taxonomic groups to investigate this.
In terms of evolutionary explanations for female-biased dispersal, FBD makes intuitive sense in species with resource defence systems, where males take the leading role in acquisition and defence of resources and there are considerable benefits to males by remaining philopatric. This strategy is quite common in pair-breeding birds (Greenwood 1980), and the same logic could account for FBD in pair-breeding mammals, such as the greater white-toothed shrew, in which males take a major role in territory acquisition and defence (Favre et al. 1997; Bouteiller-Reuter & Perrin 2005). However, resource defence may also account for FBD in some polygynous mammals (in which case the mating system is termed ‘resource defence polygyny’), such as the white-lined bat, Alaotran gentle lemur and North American porcupine (Table 2). In FBD species with high local mate competition, both inbreeding avoidance and cooperation certainly play a role. First, when dominant males have long tenure in their social groups (be they OMUs or multimale units, MMUs, Tables 1 and 2), their daughters disperse on approaching sexual maturity to avoid mating with their potential father (e.g. gorillas, hamadryas baboons, chimpanzees, howler monkeys, African wild dogs, Clutton-Brock 1989). Second (and not exclusively), males may benefit from kin cooperation and form coalitions to prevent extra-group males gaining access to females. In both OMU and MMU species, the advantages to an individual male from kin-cooperation may sometimes outweigh those of dispersal and promote male philopatry. Cooperation among male kin for territory acquisition and mate attraction might be important in mammal species that form ‘dispersed male networks’ to defend females (e.g. western gorillas, Bradley et al. 2004; possibly hamadryas baboons, Hammond et al. 2006). Finally, local resource competition has been invoked to explain several cases of FBD, even in polygynous species where LMC is expected to be greater than LRC (Table 2). This is highlighted by spider monkeys, in which female dispersal is driven by a combination of sex-ratio bias in favour of females and LRC between females, which are directly related to habitat pressures (McFarland Symington 1987).
Several proximate causes are also important to consider when attempting to explain female-biased dispersal. Extra-group attraction, aggression avoidance, eviction and benefits of parallel dispersal are important determinants of FBD as well as MBD (Tables 1 and 2). Another important consideration is that the cost of immigration might be less for females than for males, since they are more readily accepted into a new group (e.g. spider monkeys, muriquis, hamadryas baboons, Table 2), particularly if they copulate early on arrival into their new group (e.g. woolly monkey, Table 2). An extra explanation that is probably specific to females is that of abduction by males from outside the group during aggressive encounters (e.g. hamadryas baboons, Table 2). Post-weaning territory bequeathal to offspring has been invoked to explain female dispersal in species where juveniles need to acquire a key resource such as a burrow to survive. Bequeathal involves active, strategic dispersal by breeding females and appears to be condition-dependent (Price & Boutin 1993). Since adult females may be able to obtain this resource more easily than juveniles, territory bequeathal may increase the female's fitness. However, most of the species in which bequeathal has been observed have male-biased dispersal (e.g. red squirrels, Price & Boutin 1993; Berteaux & Boutin 2000, hairy-nosed wombat, Johnson & Crossman 1991; Columbian ground squirrels, Harris & Murie 1984, except common wombat, Banks et al. 2002; which has FBD, Table 2), so this cannot be taken as a general explanation for FBD. Finally, it has also been argued that females transfer to avoid infanticidal males (Marsh 1979; Stokes et al. 2003), but there appears to be very little direct evidence supporting prevalence of infanticide in FBD species (except for red colobus monkeys, mountain gorillas, and Thomas's langurs, Table 2). We would argue that it seems even more risky a strategy to attempt to immigrate into a new group with an infant who has not been sired by a resident male, or to emigrate following the death of an infant as a direct result of a male takeover (e.g. Stokes et al. 2003), and therefore this explanation seems an unlikely general explanation for FBD.
What about humans?
Far too often, there is a gap between studies of dispersal patterns in humans and those of other mammals, while in fact humans provide an important example for the occurrence of intraspecific variation in sex-biased dispersal (e.g. Hamilton et al. 2005a), and highlight the importance of geographical scale on dispersal patterns. We therefore believe a discussion of human patterns of sex-biased dispersal is justified here.
The conflicting results from the many papers describing sex-biased dispersal patterns in humans can be rather bewildering. The first global comparison of mitochondrial DNA (mtDNA) and Y chromosome patterns indicated a much higher migration rate for females than for males (Seielstad et al. 1998). By contrast, a more recent study, also on a global scale, found no evidence for sex-biased dispersal (Wilder et al. 2004), although reasons for this discrepancy could be methodological differences such as sampling strategy (the samples used in the Wilder study came from sparsely distributed populations). At a regional level, patterns can usually be explained by cultural differences or known historical events. Consistent with Seilestad et al. (1998), the majority of regional-scale studies have reported female-biased dispersal, which is typically associated with patrilocality (Perez-Lazaun et al. 1999; Oota et al. 2001; Bolnick et al. 2006). Patrilocality and female-biased dispersal is much more common in pastoral communities, where males who inherit their father's land and herds tend to be more successful in attracting a wife (Wilkins & Marlowe 2006), than in hunter-gatherer societies, where resource accumulation is less important (Destro-Bisol et al. 2004; Wood et al. 2005). One interesting related point is that a shift to patrilocal societies and female-biased dispersal may have occurred since the agricultural revolution, which started approximately 10 000 years ago, since modern hunter-gatherers (which are often seen as models for pre-agricultural societies) are characterized by similar patterns of male and female dispersal or occasionally male-biased dispersal (Wilkins & Marlowe 2006). The relationship between patrilocality and female-biased dispersal is however, not apparent in highly endogamous patrilocal populations from the Indian subcontinent, which questions the universality of this hypothesis (Kumar et al. 2006). Male-biased dispersal has been documented in connection to matrilocality (Bolnick et al. 2006), which is rare in human societies compared to patrilocality, and immigration seems to be much less regulated in matrilocal compared to patrilocal populations (Hamilton et al. 2005a). MBD tends to be more associated with historical events than with cultural practices, for example the introgression of European Y chromosomes, but not mtDNA, in the Americas post 1492 (Mesa et al. 2000; Seielstad 2000; Bolnick et al. 2006; see Bosch et al. 2003; Al-Zahery et al. 2003 for examples from other regions).
An important outcome from recent studies of human dispersal is that patterns seen at the local scale may not reflect those at a larger geographical scale (Kumar et al. 2006), and that large geographical scale patterns are likely to be representative of long-term demographic processes, whereas local-scale patterns detect events in the recent history of that region (Wilkins & Marlowe 2006). This could have important implications for studies of natural populations that wish to determine if the relative rates of male and female migration have changed over time, for example in response to climatic events, habitat fragmentation or anthropomorphic factors.