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Anita. Behav., 1980, 28, 1140-1i62 MATING SYSTEMS, PHILOPATRY AND DISPERSAL IN BIRDS AND MAMMALS BY PAUL J. GREENWOOD School of Biological Sciences, University of Sussex, Brighton, BN1 9 QG* Abstract. Many species of birds and mammals are faithful to their natal and breeding site or group. In most of them one sex is more philopatric than the other. In birds it is usually females which disperse more than males; in mammals it is usually males which disperse more than females. Reproductive enhancement through increased access to mates or resources and the avoidance of inbreeding are important in promoting sex differences in dispersal. It is argued that the direction of the sex bias is a consequence of the type of mating system. Philopatry will favour the evolution of cooperative traits between members of the sedentary sex. Disruptive acts will be a feature of dispersers. Faithfulness to a site or group is a well documented trait of many species of birds and mammals. It is particularly striking among adults which return to breed in the same area in successive years. Migratory birds provide perhaps the most striking illustrations. In the colonially nesting common tern Sterna hirundo over half the returning adults reoccupy their previous mating territory (Austin 1949, 1951). Site fidelity also occurs in more sedentary species of birds (Werth 1948). Among mammals, primates are often faithful to territories or home ranges, and boundaries between adjacent individuals or groups can be stable for long periods (Jolly 1972). Migratory species (e.g moose Alces alces), like birds, often return annually to the same summer range (Houston 1974). Although many species are philopatric, only a proportion of individuals of any species is faithful to one locality. The dispersal of the remainder may be voluntary or enforced, environmentally determined or innate (Howard 1960). The importance of dispersal is widely appreciated. It is increasingly identified as having a major role in both population regulation (Lidicker 1975) and spatial distribution (Taylor & Taylor 1977). It can have substantial effects on the genetic structure of populations. Since dispersal is a prerequisite for gene flow, widespread movement may disrupt local adaptations; any restriction may promote inbreeding and the genetic differentiation ofneighbouring groups (Wright 1943, 1946). Recently the consequences of dispersal (or lack of it) to the evolution of social and disruptive behaviour have been discussed (Hamilton 1964, 1972). *Present Address: Departmentof Adult and Continuing Education and Department of Zoology, University of Durham, Durham. 1140 This review examines dispersal in birds and mammals. In most species juveniles are more prone to dispersal than adults. A detailed discussion of age differences in dispersal can be found in Baker (1978). In addition, there are often sex differences in dispersal in both of these age classes. Reference has been made to the predominance of male dispersal in many species of mammals (Lidicker 1975; Clutton-Brock & Harvey 1976; Packer 1979), but it seems less well known that a sex bias in the opposite direction is more commonly recorded in birds (Greenwood & Harvey 1976a; Greenwood 1978; Baker 1978). A number of evolutionary hypotheses have been proposed to explain the occurrence of sex differences in dispersal, particularly for the male bias in mammals. These hypotheses will be considered in the light of the converse pattern of female biased dispersal in most birds. Certain modifications to these hypotheses will be suggested which stress the importance of mating systems as a prime determinant of any sex bias in dispersal and the direction of the bias. The extent to which any general theory can satisfactorily account for the exceptions to the prevalent pattern of dispersal within the two groups is discussed. The final section deals briefly with the different effects that male and female biased dispersal have on species' social structures. Terminology Any discussion of dispersal is beset with problems of terminology. Authors vary in their use of terms as a result either of the topic or the organism of their research, The most widely used definition of dispersal is that by Howard (1960): 'Dispersal of an individual vertebrate is the movement the animal makes from its point of origin to the place where it reproduces or GREENWOOD: MATING SYSTEMS AND DISPERSAL would have reproduced if it had survived and found a mate.' This refers only to juveniles undergoing a permanent movement from birth site to first breeding or potential breeding site and can perhaps more correctly be termed natal dispersal This can be distinguished from breeding dispersal which is the movement of individuals, which have reproduced, between successive breeding sites. The definitions do not specify that the dispersal is reproductively successful. Gross dispersal refers to the permanent movement of individuals to a new location irrespective of whether or not they reproduce after dispersing. When an individual has reproduced following dispersal the movement can be described as effective (Greenwood 1978; Shields 1979; see also below). (For a radically different view of terminologies see Baker (1978).) Methods Details of dispersal in birds and mammals are shown in Tables I-IV. Species mentioned in the tables will only be referred to by their common names in the text. The lists are probably not exhaustive, but examples have been extracted from the literature irrespective of the presence or absence of any sex bias in dispersal. Where one sex is labelled as the predominant disperser it does not imply that dispersal is an exclusive characteristic of that sex. In several instances sex differences in dispersal have been extrapolated from the information available, e.g. song thrush (Davies & Snow 1965), orang-utah (Rodman 1973; Horr 1975). In most cases (see below) examples have only been used when studies have been sufficiently detailed for the presence or absence of a sex bias to be detected. For some species data are available on both natal and breeding dispersal; in the remainder the details are either for adults or juveniles. When studies of the same species have produced different results these have been included in the tables. Almost invariably natal dispersal is more extensive and over longer distances than breeding dispersal. Consequently sex differences in dispersal are derived from comparisons within each of these categories and they may not be comparable between categories. For example, the breeding dispersal of adult female pied flycatchers is further than that of adult males. Similarly, the natal dispersal of females may be further than that of males (Haartmann 1949). However, the natal dispersal of males is considerably further than the breeding dispersal of adult females. 1141 There are three major problems in classifying patterns of dispersal. First, natal dispersal refers to individuals which have not yet reproduced, breeding dispersal to those which have reproduced. Such an unambiguous separation cannot always be made from the data available. This is particularly true for small mammals where the age, size or reproductive condition of a disperser does not necessarily indicate whether it is undergoing natal or breeding dispersal (Myers & Krebs I971). However, when members of a population have been designated as juvenile and adult I have assumed that the former should be classified as natal dispersers and the latter as breeding dispersers. Second, sex differences in natal or breeding dispersal may not be expressed in effective dispersal if the predominant dispersing sex suffers a higher rate of mortality. Similarly, there could be a sex bias in effective dispersal in species for which no sex difference in gross dispersal has been found. Unfortunately, very few studies (Greenwood & Harvey 1976a, b; Leuze 1976, and in press) have shown that the costs of dispersal may act differentially on the sexes. As a result the majority of examples in the tables indicate differences in gross dispersal. The importance of differential costs and benefits of dispersal between the sexes will be considered later. Third, age and sex differences in dispersal may vary with population changes in species subject to wide fluctuations in density (Myers & Krebs 1971). In these instances I have attempted to derive an overall average of dispersal for the different categories. Dispersal in Birds The data for natal and breeding dispersal of birds are shown in Table I, and the results are summarized in Table II. Female biased natal dispersal occurs in the majority of species; only three are male biased. Breeding dispersal also occurs predominantly in females. Two studies of one species have produced different results. Haartmann (1949) noted female biased natal dispersal in the pied flycatcher whereas similar dispersal of both sexes was recorded for a different population by Berndt & Sternberg (1969); their results for breeding dispersal were similar. The most detailed studies of dispersal in birds have been those on the pied flycatcher and great tit (see references in Table I). In a Scandinavian population of the flycatcher, 7% of males as compared with 2 7o of females breed for the first time within their territory of birth. Among adults, 93 % of males but only 37 % of females 1142 ANIMAL BEHAVIOUR, 28, 4 O _= i ~o O'~ O e.,,. oo O oo oo oo ,"4 t,~ O~ o e~ r~ o O rtJ O. Q I § | § § I § + § + + + + + § § § + + § + +i o~ c--. + ~-I r~ 9~ ,,a eo r~ ~~ r o --& = 'x:l o O U I: r "x:l ~ eo .o 0~ r,~ 'x:~. "O "t:l o ~ ~ GREENWOOD: MATING SYSTEMS AND DISPERSAL 1143 O 0~ r~ E o dd I o 0 t"-I O~ o ~ ~ ~ 0 0 I ._~ ~ ~ 'Oo e, o 8 0 ,.~ § I § § § + 4- § +l+ § + I + 0 + + + + + + -t- § § § + + § I I I 0~ g. 3 r~ ~~~ ~ I I I 0 Ii ,.0 I ~ 0 o ~ .-~ N ~ o o~ 0 d o 0 r~ 0 t o 'O EO o 1144 ANIMAL BEHAVIOUR, return each year to their first nesting locality: 61% of females nest in a different place each year. Among females, those which nest unsuccessfully due, for example, to predation, undergo greater breeding dispersal than those which do raise a brood (Haartmann 1949). Predation of eggs or fledglings has been implicated as a factor promoting the greater breeding dispersal of females in a number of other species (e.g. yelloweyed penguin, Richdale 1957; reed warbler, Catchpole 1972). In the great tit, 25 % of males and 10 % of females have their first territory on, or adjacent to, their natal one. The modal number of territories moved from birth to first breeding site is from one to two in males and from two to three in females (Greenwood et al. 1979a). Among adults, both sexes are as faithful to their former territory after a successful breeding attempt the year before when re-pairing either with the same mate or a new bird after the death of a previous mate. However, following a divorce, 80 % of males but only 40 % of females breed within one territory's width of their previous year's nest site. Divorce occurs between at least 29 % of birds which have the possibility of re-pairing with the same individual (Harvey et al. 1979). The pied flycatcher and great tit are both woodland passerines which defend feeding territories. Sex differences in dispersal are not, however, restricted to species of a particular ecology or habitat. In the herring gull 77% of males which return to the colony of their birth breed within their natal sub-colony whereas the comparable figure for females is 54 %. A larger proportion of females than males are also recruited into a colony other than that of their birth (Chabrzyk & Coulson 1976). Likewise in the colonially breeding red-billed gull, kittiwake, and Manx shearwater, there is a greater tendency for females rather than males to disperse from tlleir natal colony (Mills 1973; Wooller & Coulson 1977; Brooke 1978, respectively). Table II. The Numbers of Species and Families of Birds with Female Biased, Male Biased and No Sex Difference in Natal and Breeding Dispersal Predominant Dispersing Sex Breeding Natal Male Female Both Male Female Both Species Families 3 1 21 11 6 5 3 1 25 14 1 1 28, 4 Striking examples of sex differences in natal dispersal occur in several species of communally breeding birds. In several species of babblers most females leave their natal group prior to breeding. The majority of males remain as members of their group of birth (Zahavi 1974; Gaston 1976, 1978). A similar sex bias occurs in the Florida scrub jay, which lives in stable groups consisting of a breeding pair and their young of previous years. The non-breeding offspring assist in the feeding of related nestlings. Accession is patrilineal and a male which inherits its natal territory, or one adjacent to it, pairs with an immigrant female (Woolfenden 1975; Woolfenden & Fitzpatrick 1978). The absence or infrequency of breeding dispersal is a feature of this type of communal breeding system. Greater female n a t a l dispersal is not however an invariable rule among such species. The Mexican jay lives in social, stable and sedentary units of 8-22 birds. Each unit defends a territory within which one to four pairs may nest simultaneously in separate nests (J. L. Brown 1974). The majority of offspring remain within their natal unit to breed and both sexes are equally represented among the few which do disperse to nearby groups (J. L. Brown, personal communication). Exceptions to the prevalent pattern of female biased dispersal in birds have been reported in only one family, the Anatidae. The lesser snow goose is the best documented example of male biased natal and breeding dispersal (Cooke et al. 1975). As with many other species of geese and ducks, pair formation occurs during spring migration or on the wintering grounds. At such times, individuals from different colonies may intermingle and pair; males return to the females' natal colony to breed. This is the pattern of dispersal in males nesting for the first time and adults re-pairing after the loss of a former mate. There are a number of other species of Anatidae in which the faithfulness of females to previous nest sites is well known (e.g. Sowls 1955; Gates 1962; Doty & Lee 1974). In most of these, however, the relative patterns of dispersal of males and females are unknown. Baker (1978) in fact has overestimated the amount of evidence for male biased dispersal in ducks. However, o n e species, the pintail, does have male biased dispersal and there is suggestive evidence for similar patterns in two others, the common shelduck and long-tailed duck (Young 1970; Alison 1975, 1977). Over 90 % of bird species are monogamous or at most only facultatively polygamous (Lack GREENWOOD: MATING SYSTEMS AND DISPERSAL 1968). Because of this, the information on dispersal is predominantly for those species with this type of pair bond. An exception is the whitebearded manakin, a lek species. Male manakins aggregate in groups of up to 60 birds at traditional arenas during the breeding season. There is intense competition to achieve lek status, but once an individual has established a display territory, it is usually resident for a prolonged period. There is very little male movement between leks. Breeding females, on the other hand, are much more mobile, frequently mating at different leks in different seasons (Lill 1974). Dispersal in Mammals The data for natal and breeding dispersal in mammals are shown in Table III, and the results are summarized in Table IV. Male biased natal dispersal occurs in the majority of mammals; only five are female biased. Breeding dispersal also occurs predominantly in males. The breeding systems of mammals vary from the comparatively open asocial dispersions of numerous species of small rodents to the semiclosed, highly structured social units typical of many primates (Eisenberg 1966); a number of both types are monogamous (see Kleiman 1977). Sex differences in dispersal are not confined to species with a particular social structure, although social structure may influence the degree of difference in dispersal between the sexes (see below). In some rodents, similar and substantial proportions of juveniles of both sexes m a y leave their natal area, particularly in those species which undergo marked fluctuations in density. These species often have dispersal biased in favour of males in older age classes (Krebs et al. 1976). Male biased natal dispersal is a characteristie feature of sciurid social systems (Lidicker 1975). In a number of species, females remain close to their birth site and occupy home ranges adjacent to their mothers and siblings (Yeaton 1972; Sherman 1977; Dunford 1977). This arrangement was probably the incipient evolutionary stage in the progression to the more complex matrilineal units of marmots, where females may remain within their maternal group (e.g. yellowbellied marmot, Armitage 1973, 1974). In those species in which males do not apparently maintain exclusive access to one or a number of females during the reproductive period, breeding dispersal is male biased. Conversely, male-female relations are stable and long-lasting in marmots and prairie dogs, and adults of both sexes may 1145 disperse together (King 1955; Armitage 1974). For example, new coteries are almost invariably established by adult black-tailed prairie dogs, leaving offspring to retain the natal burrow (King 1955). Studies of primates have yielded perhaps the most detailed information on natal and breeding dispersal in mammals. Several species exemplify the semi-closed polygynous societies in which movement between groups is often a characteristic of the male. Examples range from the multimale troops of the olive baboon (Packer 1979) and Japanese monkey (Itani 1972; Sugiyama 1976) to the single male troops of the Hanuman langur (Hrdy 1977). Of 50 olive baboons which transferred between troops in a nine-year period only two were females. In addition, all males left their natal troop prior to breeding (Packer 1979). Similarly, in the Japanese monkey the majority, if not all, of males undergo natal dispersal (Itani 1972). Although the majority of highly social polygynous mammals have male biased dispersal, it is not an invariable rule. The plains zebra is one species in which natal dispersal occurs in both sexes. It has a harem breeding system consisting of one stallion and one to several mares with foals. Young males leave voluntarily and join bachelor groups; young mares are abducted by stallions during oestrus (Klingel 1969). A similar pattern of dispersal occurs in the hamadryas baboon (Kummer 1968). In monogamous species (e.g. dik-dik, lar gibbon) offspring of both sexes leave their natal territories. For example, a male gibbon which reaches sexual maturity is driven out by its father, a female by its mother (Carpenter 1940). The conventional interpretation is that both sexes have dispersed or transferred (Itani 1972; Packer 1979). In the absence of more detailed information, I have acceded to that classification. However, by analogy with the situation in monogamous birds, it could well be that one sex is more likely than the other to breed closer to the natal territory. Only recently has female biased dispersal been documented in mammals. Currently, five species have been reported with this pattern for natal dispersal and two for breeding dispersal, but with long-term studies in progress more can be expected. Most individuals undergoing natal dispersal are female in one species of lagomorph, the pika (A. T.~Smith 1974, 1978). In the field vole, natal dispersal is male biased but adult females change breeding sites more readily than ANIMAL 1146 BEHAVIOUR, 28, 4 !! O'~ § iI § § i it0 ~0 GREENWOOD: MATING SYSTEMS AND DISPERSAL 1147 I I O 02 O g~ Ox ~o t~ O~ O~ .~1 84 ~ ~.~ r/2 O~ ~D o~ t~ Ox o r 4' o~84 o0 06 § O t + + + q- + + -q- O + + + + + g~ § § § § o § r !' + + + -~ + § § -~+1§ + o~ O "O eD t~ o O _o'," I O ._= ~ ~ ~~ :r, t~ I 9 o ~ ~d ._= O o .o ANIMAL 1148 BEHAVIOUR, 28, .4 ~L p,,,. 0 0 o r~ O -1 t~ i O0 i ~z I § + § + + ! ~. + § § § + Jr + § § + + § + § + e~ 0 I O e~ "O .~ ol "to GREENWOOD: MATING SYSTEMS AND DISPERSAL do males (Myllym~iki 1977). More marked sex differences in dispersal occur in the chimpanzee and the wild hunting dog. Male chimpanzees live in patrilineal communities in which several adult males share a common home range that may encompass the overlapping and smaller ranges of females. At various times females may associate with males from two adjacent communities, and nulliparous females transfer permanently to a new community from their natal one (Pusey, in press; Nishida, in press). African wild dogs have a social organization consisting of one reproductive pair and their pups plus a cooperative group of non-breeding adults (usually male) which assist in the rearing of the young. Female biased natal dispersal is divisible into two components. First, all female offspring leave their natal pack and males usually remain. Second, although females (often sisters) frequently transfer together, only one female eventually breeds in each pack; the remaining individuals may subsequently undergo further natal dispersal (Frame & Frame 1976). The sex difference in dispersal in the gorilla is likewise associated with patrilineal inheritance, although some males do leave the unit of their birth. The gorilla social system is, in terms of reproduction, effectively a single male group. An old silverback male is eventually replaced by a younger one born into the unit and which is probably its son. Those males which disperse attempt to attract females and thus form a new group. On the other hand, nearly all females leave their natal group at maturity and about half join an established unit, the remainder a lone male (Harcourt et al. 1976). The final example is the white-lined bat. Single males defend foraging territories and harems o f females are distributed among them. Tannenbaum (1975) has shown that male offspring often establish territories close to their parental one whereas only a small fraction of females breed in the vicinity of their birth site. Table IV. The Numbers of Species and Families of Mammals with Female Biased, Male Biased and No Sex Difference in Natal and Breeding Dispersal Predominant Dispersing Sex Natal Breeding Male Female Both Male Female Both Species Families 45 23 5 4 15 7 21 6 2 2 2 2 1149 Factors Promoting S e x Differences in Dispersal What are the salient ecological or behavioural factors that account for the apparent differences in sex biased dispersal between birds and mammals ? The problem is not one of producing alternative hypotheses for birds and mammals per se; rather it is to identify underlying similarities that may account for female biased as opposed to male biased dispersal, irrespective of the vertebrate class. To help to clarify the problem this section has three purposes: (i) to discuss a number of recent evolutionary explanations for sex differences in dispersal; (ii) to highlight a number of factors that are known to influence dispersal and the reasons why they may or may not promote a sex bias; and (iii) to evaluate whether these factors can satisfactorily account for the direction of the sex bias. Sex Chromosomes Females are the heterogametic sex in birds; males are the heterogametic sex in mammals. Whitney (1976), extrapolating from Hamilton (1972), proposed that sex chromosome asymmetries would result in the evolution of greater female sociality in mammals and male sociality in birds. Criticisms by Kurland (in press), on the basis of the probable outcome of intra-genome conflict, make the hypothesis largely untenable as an explanation for the matrilineal social structure common in mammals or the patrilineal organizations of communal birds. Likewise it cannot be considered as a basis for differential dispersal of the sexes, Nor is it likely that the presence of sex-linked deleterious genes would result in the preferential avoidance o f inbreeding by the heterogametic sex. In addition, there is no clear cut division between the two taxonomic groups of female biased as opposed to male biased dispersal. Finally, there are simpler explanations for the observed sex bias in sociality between some birds and mammals that take into account sex differences in dispersal (see below). Dominance A second general theory for sex biased dispersal is that by Gauthreaux (1978). He has produced a behavioural dominance theory to account for age and sex differences in dispersal. Notwithstanding that subordinate and young individuals are frequent dispersers, his view that male dominance over females provides a causal explanation for greater female dispersal is erroneous. Males are dominant to females in some contexts in many species of higher vertebrates (see 1150 ANIMAL BEHAVIOUR, Wilson 1975; Rails 1976), but that fact could hardly account for dispersal being female biased in most birds and male biased in most mammals. Among the exceptions to this male-female relation are the spotted hyena, where females are dominant to males yet males disperse (Kruuk 1972), and in birds of prey, where the larger females are dominant to males yet female biased natal dispersal occurs, in the sparrowhawk (Newton, personal communication) and the hobby (Fiuczynski 1978). Environmental Change A sex bias in dispersal is unlikely to be associated with major changes in the distribution of resources (e.g. food, breeding sites) if both sexes would benefit from moving (see Baker 1978). An interpretation of the high level of dispersal in the greenfinch is based on the relatively unpredictable nature of its food supply (Greenwood & Harvey 1977). Likewise, a marked skew in the sex ratio of dispersers compared to the population as a whole should not be apparent when species, such as small rodents, are at or above the carrying capacity of their habitat, unless male and female thresholds to change are different or the life history of a species in a fluctuating habitat facilitates the transport of progeny by only one of the sexes (see Lidicker 1975). Species of birds and mammals have a wide diversity of life histories. Despite the marked differences in the modes of reproduction between the two taxa, it is unlikely that environmental change affects them in sufficiently different ways to account for the general patterns of sex biased dispersal. In fact, it appears that sex differences in dispersal occur most markedly in species inhabiting stable and predictable habitats, which is not to say that all species in such habitats will have a sex bias. Population Density Dispersal may have a major role in the population control of many species of birds and mammals. Individuals forced to disperse are frequently the socially subordinate, younger and weaker members of the population (for reviews see Archer 1970; Watson & Moss 1970; Lidicker 1975). High or increasing population densities may be associated with high levels of dispersal (Myers & Krebs 1971). The question that concerns us here, however, is whether fluctuations in density alter the relative patterns of male and female dispersal. In other words, is there a consistent sex bias within a species irre- 28, 4 spective of population size ? Some small rodents may experience substantial changes in density within and between breeding seasons. Such species also provide examples where the sex ratio of dispersers may vary over time (e.g meadow mouse, Myers & Krebs 1971; Townsend's meadow mouse, Krebs et al. 1976), although changes in the sex ratio do not appear to be closely aligned to changes in population density. In species less subject to wide variations in population size, an underlying sex bias in either natal or breeding dispersal is not markedly altered by density changes (e.g. greater male than female dispersal in the yellow-bellied marmot (Armitage 1973) and the round-tailed ground squirrel (Dunford 1977)). Nevertheless, it would be wrong to assume that changes in density produce equivalent effects on different components within a population. In the great tit, increased breeding density is related to increased effective natal dispersal of males, measured in terms of the number of territories moved. Females, on the other hand, have a similar pattern of effective natal dispersal each year with no comparable density effect. Even so, within the upper and lower limits of observed breeding densities, greater male than female dispersal has been noted in only one of 12 years (Greenwood et al. 1979a). To summarize, although population density can affect the degree of sex bias in dispersal, there does not appear to be a consistent pattern whereby changes in species' densities accentuate or diminish underlying sex differences in dispersal. Avoidance of Inbreeding Since Lincoln (1934) many authors have felt that the dispersal of offspring from their natal group or area functions, in part, as an inbreeding avoidance mechanism (e.g. Howard 1960; Lidicker 1962; Itani 1972; Bischof 1975; Greenwood & Harvey 1976a). Nevertheless, there is only a limited amount of field evidence from vertebrates to substantiate laboratory work (Sittman et al. 1966; Hill 1974) that close inbreeding is harmful. Great tits which mate with close relatives have a lower than expected nesting success (Greenwood et al. 1978). The viability of offspring sired by a male olive baboon which mated with probable female relatives was substantially less than that of outbred young (Packer 1979). To what extent then are sex differences in dispersal a result of avoiding such matings 9. Unfortunately there are very few species for which good data are available, The study by Packer (t979) of the olive baboon is the best so GREENWOOD: MATING SYSTEMS AND DISPERSAL far. The reproductive activity of males prior to natal dispersal is low in the troop of their birth and they do not compete for access to females. These males are attracted to oestrous females in neighbouring groups and females may solicit the attention of potential dispersers. Despite the fact that there may be difficulties in joining a new troop due to the aggression of resident males, the costs of male natal dispersal are less than the probable costs of inbreeding. Similar patterns of voluntary dispersal of pubescent males in a number of primate species may have an equivalent function (e.g. Japanese monkey, Itani 1972; rhesus monkey, Drickamer & Vessey 1973), though in others inter-male conflict may be a proximate cause of subordinate male dispersal (e.g. toque monkey, Dittus 1975). Inbreeding avoidance also provides a possible explanation for the female natal dispersal which occurs in several social mammals. In the plains zebra, males may have tenure of a group for sufficiently long for their own daughters to come into reproductive condition: Indeed, Klingel (1969) considers the prominent oestrous posture of young mares within their natal group to be a means of eliciting their abduction by unrelated stallions. Female transfer also occurs in the gorilla, where a son may take over the natal group when his father dies (Harcourt et al. 1976). An alternative explanation for female transfer in the gorilla as a means of reproductive enhancement is given by Baker (1978). Females move to groups with a high ratio of silverback males to females. Baker argues that this will result in greater protection from predators to the transferring female. However, it seems more likely that the initial impetus for leaving the natal group is to avoid inbreeding and that choosing the best available group is a secondary advantage. In the two species of mammals in which males are philopatric and form cooperative kin groups (African hunting dog, chimpanzee), the dispersal of females has also been interpreted as an inbreeding avoidance mechanism (Packer 1979; Pusey, in press). Although there are exceptions, the prevailing means of avoiding inbreeding in mammals is through male dispersal. Packer (1979) believes that the asymmetry originated and is maintained through the advantages to males of gaining access to a large number of females (see below). In birds, inbreeding avoidance is achieved in highly social cooperative species by female natal dispersal (e.g. Zahavi 1974; Woolfenden 1975; Gaston 1976, 1978; Woolfenden & Fitzpatrick 1151 1978) and may also contribute to the asymmetry in dispersal in more asocial species (Greenwood & Harvey 1976a; Greenwood et al. 1978). Whether the dispersal functions to prevent close inbreeding has yet to be elucidated but it is a possible interpretation. The fidelity of a high proportion of both sexes to their natal group in the Mexican jay (J. L. Brown, personal communication) may be a rare example of endogamy in higher vertebrates. Whilst it is probable that sex differences in dispersal in some species are maintained by the detrimental effects of inbreeding, it is obvious that the avoidance of such matings does not provide much insight into the direction of the sex bias. In polygynous species the costs of inbreeding are probably greater for females than for males, as a consequence of the larger investment by the former in offspring and their more limited reproductive potential (Clutton-Brock & Harvey 1976; see also Bengtsson 1978; Maynard Smith 1978). If inbreeding avoidance is the sole basis for dispersal then the sex subject to the greater cost of inbreeding should be more likely to disperse. This is clearly not the case in mammals, where most species are polygynous. In monogamous birds, on the other hand, females disperse even though the costs of inbreeding are probably similar for males and females. Access to Mates and Reproductive Enhancement The problem of which sex should benefit most from dispersal has been considered by CluttonBrock & Harvey (1976) and Packer (1979), and briefly by Trivers (1972) and Wilson (1975). (A much more detailed synthesis by Baker (1978) is discussed in the next section.) Taking polygynous mammals as the example, the arguments have normally proceeded along the following lines. Females invest heavily in offspring and are the limiting sex; males invest relatively little and compete for access to females. Greater benefits thus accrue to males gaining access to a large number of females than vice versa. One means of achieving this is through greater mobility, even at the expense of an increased risk of death if this is offset by reproductive enhancement. Since intra-sexual competition is also more intense among males than females, a large proportion of males may be denied access to females: hence greater male dispersal in search of available mates or a pre-reproductive period spent peripheral to groups of females. The information that is available on polygynous mammals certainly makes these hypotheses 1152 ANIMAL BEHAVIOUR, appear plausible. Female rhesus monkeys live in stable groups and sexually mature males frequently transfer between them during the breeding season. Those males which copulate the most within one group are more likely to transfer to another. There is also a tendency for the breeding dispersal to be from groups with few available females to those with a larger number (Lindburg 1969; Drickamer & Vessey 1973). A similar picture emerges from Packer's (1979) detailed study of the olive baboon. Breeding males which have above average reproductive activity in one troop regularly transfer into troops with larger numbers of oestrous females. Among adult male grey squirrels, a higher proportion of copulations is achieved by mobile individuals (i.e. those undergoing greater breeding dispersal) than sedentary ones (Thompson 1977). Considered in isolation, the explanations for male biased dispersal in mammals may seem entirely appropriate. However, extrapolation of the hypotheses to birds would similarly predict greater male dispersal even though the majority of species are monogamous. About one third of male great tits are suspected of not breeding in their first year (Bulmer & Perrins 1973) and the inter-year differences in natal dispersal are consistent with the view that competition for territories is more severe among males than females (Greenwood et al. 1979a). Nevertheless, female natal dispersal is greater than that of males. In the pied flycatcher, the female bias in dispersal is more pronounced in populations where a higher proportion of males are polygynous (cf. Haartmann 1949; Berndt & Sternberg 1969; Baker 1978), whereas inter-male competition in mammals is associated with greater male dispersal (e.g. Sugiyama 1965; Sadleir 1965). Likewise, reproductive enhancement through dispersal is more characteristic of females in many species of sedentary birds since they move more readily than males between breeding sites following unsuccessful nesting attempts (Haartmann 1949; Richdale 1957; Catchpole 1972; Darley et al. 1977). Mating Systems and Dispersal This section presents the hypotheses for the evolution of sex differences in dispersal based on current interpretations of avian and mammalian mating systems. Before proceeding with the hypotheses it is worth drawing attention to a recent publication by Baker (1978) which discusses at length intraspecific variation in the inci- 28, 4 dence of dispersal. Baker deals extensively with age differences in dispersal and variations in the tendencies to disperse between species living in groups, in homes ranges and those undergoing seasonal migrations. Independently, we have reached similar conclusions for the evolution of sex biased dispersal in birds (Greenwood & Harvey 1976a; Greenwood 1978), although the occurrence of greater female dispersal is much more widespread than that indicated by Baker (1978) if one considers more recent information than was available to him. We differ in our explanations for the evolution of male biased dispersal in mammals. Baker (1978) concentrates mainly on intra-sexual variation in mammalian dispersal but also stresses the importance o f polygamy and greater female investment in resources and offspring in contributing to a male bias in dispersal. Some of the arguments are similar to those of Clutton-Brock & Harvey (1976) and Packer (1979). I have attempted to derive a more general hypothesis for sex biased dispersal within the broader framework of the recent reappraisals of vertebrate mating systems (e.g. Bradbury & Vehrencamp 1977a; Emlen & Oring 1977). This attempt has been aided, in part, by access to information (unavailable to Baker) on the social structure and dynamics of a number of species of mammals with female biased dispersaI. Resource Defence and Female Biased Dispersal One feature common to bird species with female biased dispersal is that the male defends a resource which is of paramount importance to the acquisition of a mate or to the rearing of offspring. Competition between males for females is mediated through their ability to hold a resource rather than their capacity to defend females. Female choice of mates is effectively superimposed upon a mating system that involves the division of resources by males. The resources themselves need not be of direct benefit to the female, but could simply provide her with a means of assessing the quality of a male. Such a resource defence system (see J. L. Brown 1964; Emlen & Oring 1977; Bradbury & Vehrencamp 1977a) provides little scope for male desertion, but does not necessarily mean that males contribute to the rearing of offspring when considerable expenditure is required to secure and hold a resource. Nevertheless, resource defence mating systems, especially in birds, are often monogamous with both parents helping to raise young. In other words, monogamy and female biased GREENWOOD: MATING SYSTEMS AND DISPERSAL dispersal can both be a consequence of a resource defence mating system. I propose that the philopatry of males is the result of two factors. First, the comparative ease with which a male can acquire the resources necessary to attract females. This assumes that an individual is more able to establish a breeding territory in its natal area than elsewhere. It could be facilitated through familiarity with the locality that would by implication engender costs to dispersing to unknown areas (e.g. lower feeding rates, higher risks of predation). A further possibility is that prior residency or familiarity are important factors, in terms of inter-male competition, in the acquisition of a territory. In some instances the securing of a resource could be assisted by the close proximity of relatives. Philoparry would thus be a consequence of resource competition with the advantages accruing to the sedentary rather than the dispersing individual. In the event of selecting and holding a substandard territory, there would be little opportunity to vacate an area to seek a better one (breeding dispersal). This should be particularly evident when competition for resources is high and a proportion of males are prevented from breeding (for a similar viewpoint see Baker 1978). The second factor that may impose philopatry on males may be the result of female choice. Though females may refrain from breeding with close relatives they may preferentially mate with males of as similar a genotype as possible without incurring the costs of inbreeding depression (Shields 1979). Males which disperse may be able to acquire a territory but not a mate because they are recognized or ignored as unfamiliar. Both proposals are amenable to experimentation, though the second factor may be of lesser importance in producing sex differences in dispersal. It could however explain why both sexes in many species have a tendency to be philopatric. A mating system that results from the partitioning of resources by males prior to the selection of mates by females should result in female dispersal. Females do not normally have the costly constraint of establishing a territory. Instead they have the capacity to choose between the available resources of different males. Females will have greater flexibility both as juveniles undergoing natal dispersal and as adults enhancing their reproductive success by breeding dispersal. When females are the limiting sex, their potential for rejecting particular males or the resources they hold should be greater than a male's potential for rejecting a female. By impli- 1153 cation, the costs of male dispersal are extremely high and where dispersal has evolved primarily as an inbreeding avoidance mechanism, females rather than males would be expected to leave their natal site or group. Evidence to support the hypotheses for the evolution of female biased dispersal is largely circumstantial. Supportative data can be extracted piecemeal from a number of studies. Population density in the great tit is positively related to the number of territories moved by natal dispersing males but not females, suggesting that competition for territories is more intense among the former. There is additional evidence that males preferentially occupy their natal territory when there is the chance to do so (Greenwood et al. 1979a). Whether males prevented from breeding in their natal area are less successful in securing a territory elsewhere is unknown. The greater philopatric tendencies of males in species such as the great tit may be a step on the evolutionary route to the patrilineal cooperative systems of species such as babblers and the Florida scrub jay. In these, a male's breeding options are restricted to assisting in and eventually inheriting the natal group, budding off from the natal territory or attempting to form a new group by attracting females. Females, on the other hand, may succeed in joining another group (Zahavi 1974; Woolfenden 1975; Gaston 1976, 1978; Woolfenden & Fitzpatrick 1978). The reluctance of individuals in many species to undergo breeding dispersal even though their initial reproductive site is inadequate (e.g. Tenaza 1971) is not surprising if the costs of dispersal are high. When males are the primary resource defenders their options should be considerably fewer than those of females. Both sexes usually reoccupy or retain sites following successful nesting attempts. Females in a number of species have a greater tendency to move to a new location following unsuccessful breeding attempts (e.g. Haartmann 1949; Richdale 1957; Catchpole 1972). They should also be expected to disperse when subject to variability in the quality of nesting areas (e.g. Verner 1964) and when there are no long term advantages from re-pairing with the same individual. In this context it is worth noting the greater effective natal dispersal of females in polygynous populations of the pied flycatcher (Haartmann 1949) compared to monogamous ones (Berndt & Sternberg 1969). This could indicate a higher variance in the quality of the resources defended by different 1154 ANIMAL BEHAVIOUR, males in the former group both within and between breeding seasons (see Orians 1969). Selection of good territories by females or a reluetance to mate bigamously with a male could well be the source of greater female dispersal. A parallel situation prevails in the white-bearded manakin, where males compete for positional status in one lek whereas females have the capacity to choose different males both within and between leks (Lill 1974). A number of species of mammals with female biased dispersal have a mating system which seems similar to that of most birds. In the whitelined bat, single males control access to a large foraging range which serves to attract groups of females (Tannenbaum 1975; Bradbury & Vehrencamp 1977a, b). Competition for male territories is intense and the acquisition of a territory and subsequently a harem near to the natal one by male offspring may be mediated by the presence of the parental male; females disperse in this species: The social dynamics of the gorilla are analogous to those of cooperative birds (see above). Females which disperse can join adjacent groups; males either inherit their natal group or have to establish a new one (Harcourt et al. 1976). In the pika, the territories of a male and female overlap in the breeding season to become one common area. Juvenile males live close to their birth site, but peripheral to the defended patches of vegetation, until a vacancy arises. Natal dispersal is more likely to occur among females and they often pair with single males defending a territory (A. T. Smith 1978). Again, this arrangement appears similar to that of monogamous territorial birds with male philopatry and female biased dispersal. It is uncertain whether the chimpanzee and wild hunting dog, both with cooperative male groups and female transfer, should be included amongst those with a resource defence mating system. A large number of ungulates do have resource defence systems (Owen-Smith 1977), but it is in territorial mammals of this kind that extensive information on dispersal is lacking. For instance, the majority of ungulates in Table III do not have this type of mating system. There is some evidence from the study of the white rhinoceros by Owen-Smith (1975) that females do wander through male territories; those males holding larger, better quality areas achieve most matings. Female flexibility in choosing between the different defended areas of males has been reported in a number of other ungulates (e.g. Jarman 1974). Whether this means that dispersal is biased in 28, 4 favour of females and that males are more philopatric is unclear. Mate Defence and Male Biased Dispersal In many species of mammals the social system is not one in which males defend resources in order to attract females. Instead, females form the stable nucleus with males as an adjunct to it adopting strategies to maximize their access to females. This type of mating system is rare among birds (Emlen & Oring 1977) with the probable exception of the Anatidae (see below). The defensibility of females and not resources has been considered a key component in the evolution of the males' reproductive tactics (Emlen & Oring 1977; Bradbury & Vehreneamp 1977a). Male dispersal can be viewed as a consequence of the dispersion of females. Thus the hypotheses of Baker (1978), Clutton-Brock & Harvey (1976) and Packer (1979) for the origins of male biased dispersal in the majority of mammals can perhaps be modified. These authors consider sex differences in dispersal to be derived from polygyny, where males invest little in offspring and gain most from dispersal, while females invest heavily and should gain most from being sedentary. With this asymmetry and the additional possibility that males may be uncertain of their offspring (Alexander 1974) it is not difficult to envisage the evolution of the matrilineal social structure commonly found in mammals (see Eisenberg 1966). The crucial point, however, is that a matrilineal social organization and male biased dispersal are not inextricably linked. What is important is that mate dispersal is a consequence of a mating system in which males do not primarily determine the distribution of females by partitioning resources amongst themselves. Instead it is the distribution of females that influences the dispersion of males. The origins of such a system may well be derived from marked differences in parental investment by the sexes, where philopatry is more advantageous to females than to males. It does not necessarily follow though that a matrilineal structure consisting of mobile groups of females cannot be retained when males do defend resources to attract females. In other words, male biased dispersal cannot automatically be assumed to be a consequence of polygyny. Instead, it depends upon the means through which the polygyny is achieved (cf. resource defence single male harem of the whitelined bat with female dispersal (Bradbury & Vehrencamp 1977a, b) versus mate defence single GREENWOOD: MATING SYSTEMS AND DISPERSAL male/multi-female troops of the Hanuman langur with male dispersal (Hrdy 1977)). A mate defence system with male biased dispersal is well exemplified by the open social organization of the round-tailed ground squirrel (Dunford 1977). A female during pregnancy and lactation maintains sole use of her home range. During the mating season, ranges are permeable to males which compete for non-exclusive access to females. (This species also illustrates the fact that females in some species can prevent competition for food from males during the period of maximum investment in offspring.) Among mammals with more structured and closed organizations, males may temporarily or semipermanently append themselves to a group of sedentary females and for a period have exclusive access to them (e.g. Kaufmann 1962; Lindburg 1969; Schaller 1972; I. & O. Douglas-Hamilton 1975; Hrdy 1977; Packer 1979). In species of birds with male biased natal or breeding dispersal, the mating system also appears to be one of mate defence. In the lesser snow goose and the long-tailed duck, males do not arrive on the breeding grounds unmated and partition the available habitat into territories. Instead, pairs form on the wintering grounds before the nesting season (Alison 1975; Cooke et al. 1975). Male long-tailed ducks do defend small areas in the early part of the breeding cycle, but these are of little value to females which commonly nest in an area other than that defended by their mate. A female's investment in offspring is considerably greater than a male's, and the male often deserts while she is incubating (Alison 1975). A male's reproductive tactics are geared to maintaining access to the female prior to egg laying and not to any associated resource. In both the lesser snow goose and the shelduck, male parental duties are more extensive and entail the defence of resources and a longer association with offspring and young (e.g. Young 1970). Nevertheless, a mate defence mating system, particularly in monogamous species, does not exclude the possibility of males adopting additional strategies, such as the defence of feeding areas, to maximize their reproductive success. The crucial point is that in the absence of a mate such actions during the breeding season are superfluous. It is therefore females which determine the dispersion of males. Conversely, for a resource defence mating system, comparable actions are essential for the attraction and acquisition of mates. 1155 Problems In at least two species of mammals, natal dispersal is male biased even though males defend resources to attract females. Male yellow-bellied marmots defend overwintering sites important for hibernation, allowing access by females but excluding other males (Downhower & Armitage 1971). In the vicuna, males hold feeding territories with an average harem of four females. Dispersal is male biased although young females also leave their natal unit (Koford 1957; Franklin 1974). There may be two reasons for these sex differences in dispersal. First, in marmots, the harem system has probably evolved from the matrilineal organization common in other sciurids in which male dispersal is to be expected. As a consequence, they may have retained the earlier mode of dispersal. In other words, the mating system may be primarily one of mate defence but secondarily resource defence. Second, in both the marmot and vicuna, male dispersal may be a direct result of the degree ofpolygyny. When most females can be monopolized by relatively few dominant males and breeding sites are a limiting resource, then a high proportion of subordinate males may be excluded. Females, though, should retain the propensity to select males on the quality of their resources. Natal dispersal may be biased in favour of males whereas effective natal dispersal could be biased in favour of females. These two species illustrate more general problems for a comparative survey of dispersal. Very few studies have distinguished between gross and effective dispersal (see Methods). A study of the water vole by Leuze (1976, and in press) is a mammalian exception; the costs of female dispersal are much higher than male dispersal. Conversely, in the blackbird, the costs of male dispersal are probably higher than female dispersal (Greenwood & Harvey 1976b), Differential costs are crucial components in the proposed relationships between mating systems and sex biased dispersal (see also Baker 1978). Both sexes will derive benefits from familiarity with an area. Which sex disperses may be the outcome of a conflict between the sexes, where the relative costs and benefits of dispersal and philopatry to the sexes determine the outcome. Until more studies are available which have distinguished between gross and effective dispersal it will be difficult to assess the veracity of the hypotheses for the evolution of sex biased dispersal. Even so, it may be unrealistic to expect all species to fall within the proposed framework. Exceptions 1156 ANIMAL BEHAVIOUR, will include those already mentioned and others which have been inadvertently assigned to the wrong mating system, pattern of dispersal or both. More detailed studies of mammals with female biased dispersal and birds with male biased dispersal should be illuminating. However, further examples of birds or mammals with the prevalent mating system and sex biased dispersal of their taxon will not constitute tests of the hypotheses. A comparative survey of another taxon (e.g. fishes, reptiles) would be a more appropriate as well as independent test. The Consequences of Philopatry and Dispersal The philopatry of individuals to their natal group or area produces conditions that facilitate the evolution of altruistic traits among close relatives (Hamilton 1964, 1971, 1972). Perhaps the most striking example so far reported in mammals is the alarm calling of females for the benefit of their immediate offspring and other same-sex relatives in Belding's ground squirrel; here females are sedentary and males disperse (Sherman 1977). In the patrilineal Florida scrub jay, male offspring remain in their natal group longer than females and during that time assist in the rearing of broods other than their own. Some of the males eventually inherit their natal territory (Woolfenden 1975, and quoted in Emlen 1978). No doubt many more examples of sex biased cooperation or altruism will be discovered. These should be predominantly male biased in birds and female biased in mammals as a result of the differences in dispersal between the two groups. Nevertheless, it should not be assumed that relatives will automatically derive benefits from their close proximity. For example, male great tits which nest in territories adjacent to those of close relatives do not have a reproductive success higher than expected (Greenwood et al. 1979b). However, it still remains possible that the securing of territories in relatively asocial monogamous birds can be assisted by relatives nearby, by analogy with the situation for males in the Florida scrub jay (Woolfenden & Fitzpatrick 1978) and probably also for females in Richardson's ground squirrel (Yeaton 1972). The likelihood that relatives are in close association is reduced by dispersal unless related individuals which disperse remain together. This is the case in the lion, where male siblings leave their natal group at the same time and they copulate with the same lionesses in a new pride following successful dispersal (Bertram 1975, 1976). The estimated average degree of related- 28, 4 ness between reproductive males in a pride is greater than that between females (Bertram 1976). This result is probably rather unusual in species with male biased dispersal. The proximity of unrelated individuals as a result of dispersal may have profound consequences. It is not surprising that various disruptive acts accompany such movements, particularly when the interests of philopatric and dispersing animals differ. Infanticide by males taking over groups has been observed in a number of species of mammals. The evolutionary significance of such action has been extensively reviewed by Hrdy (1974, 1977). In summary, it may be advantageous to incoming males to kill unrelated offspring and curtail further maternal investment when, as a consequence, females come into oestrus and are mated by the new males. A successful takeover by males may also result in the expulsion (enforced dispersal) of resident males (e.g. I-Ianuman langur, Hrdy 1977). In the purple-faced langur, males in high density populations do not have access to female groups for long enough for juvenile females to reach maturity during their tenure; young females are also expelled (Rudran 1973). It has been argued that this enforcement of female natal dispersal reduces competition for food within the group (Hrdy 1977). Actions by dispersing males may jeopardize the immediate reproductive success of both resident males and females. Less attention has been paid to the strategies employed by dispersing females. Males would be expected to accept incoming adult females and possibly dependent female offspring if there was a high probability that the latter would reach maturity during t h e males' tenure. Resident females should attempt to repel incoming females. If females are successful in gaining admission to a group, then disruptive or at least non-cooperative actions may occur between them and other unrelated females within the group, The possibility of infanticide cannot be excluded. Sex biased philopatry may also have important consequences for other life history traits. In the thick-tailed bushbaby, sedentary females occupy home ranges adjacent to those of close relatives. If it is assumed that females are competing for resources then they are more expensive to produce than males. In line with this assumption, secondary sex ratios are biased in favour of males which disperse ,(Clarke 1978). Clearly, where males are the philopatric sex and compete with each other the opposite bias in the sex ratio GREENWOOD: MATING SYSTEMS AND DISPERSAL would be predicted. The sex ratio bias should reverse in situations where offspring of the philopatric sex are cooperating rather than competing with close relatives. The need for appropriate data to test these hypotheses is clear. A more detailed discussion of the evolutionary consequences of philopatry and sex biased dispersal in relation to mating systems can be found elsewhere (Greenwood, in press). Conclusion The observed sex differences in natal and breeding dispersal in birds and mammals are associated with a number of interrelated variables: t a x o n o m y , differences in the sex chromosomes, the pair bond and mating systems. There is no justification for believing that the predominance of female biased dispersal in birds and male biased dispersal in mammals is the product of some taxonomic constraint, i.e. alternative and evolutionarily stable means o f solving similar problems. N o r is there a basis for assuming that the asymmetry in the sex chromosomes is the source of the bias. Neither could satisfactorily account for the exceptions in the two classes. We are therefore compelled to investigate the significance of the difference in behavioural or ecological terms. The broad distribution of the 1157 traits indicates that the answers must also be sought on a similarly broad base that transcends species-specific life history idiosyncracies. The vast majority of birds are monogamous; the majority of mammals are polygamous. Most of the former have female biased dispersal, the latter male biased dispersal. I have argued though that both the nature of the pair bond and the sex differences in dispersal are a consequence of the type of mating system. (I have not dealt in detail with the more complex problem of why species have a particular mating system (see Emlen & Oring 1977; Bradbury & Vehrencamp 1977a; Bradbury, in press).) Resource defence by one sex to attract members of the other sex will not only favour m o n o g a m y but also philopatry of the former (resource defender) and greater dispersal of the latter. A mate defence mating system, in which members of the limited sex are primarily concerned with gaining access to and defending members of the limiting sex, will favour polygamy, the philopatry of the limiting sex and greater dispersal of the limited sex. A summary of the salient features of dispersal associated with each mating system is shown in Table V. Whether mating systems prove to be the best predictors of sex biased dispersal awaits further field observations and experiments. Table V. Mating Systems and Dispersal in Birds and Mammals: A Summary of the Main Features Associated with Resource Defence and Mate Defence Mating Systems Resource Defence Mate Defence High male investment in resources, in presence or absence of mate(s) Low male investment in resources, particularly in absence of mate(s) Low female investment in resources High female investment in resources Inter-male competition for resources Inter-male competition for mates Mainly monogamous (but includes leks .9) Mainly polygamous Male philopatry High cost to male dispersal ? Female philopatry High cost to female dispersal ? Greater female natal and breeding dispersal: (i) Reproductive enhancement - female choice of male resources (ii) Inbreeding avoidance Greater male natal and breeding dispersal; (i) Reproductive enhancement - increase access to females (ii) Inbreeding avoidance Evolution of patrilineal social organization Evolution of matrilineal social organization 1158 ANIMAL BEHAVIOUR, Acknowledgments M y m a j o r debt is to Paul Harvey a n d G e o r g i n a Mace who have been a n i n v a l u a b l e source of e n c o u r a g e m e n t a n d criticism d u r i n g the paper's long gestation. I a m also grateful to a n u m b e r of other people who, in diverse ways, have helped me clarify m y thoughts: J. M a y n a r d Smith, J. Bradbury, S. Vehrencamp, N. K n o w l t o n , W. Shields, P. Sherman, E. Mayr, T. C l u t t o n - B r o c k a n d J. Krebs. 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