Original reference:
Moore, J. (1984). Female transfer in primates. Int. J. Primatol. 5: 537-589.

1998 Eprint note -- This paper was intended to do two things:

--Document the widespread phenomenon of female transfer, thus challenging the common idea that mammalian social groups are necessarily composed of related females; and
--Examine the implications female transfer has for understanding the origin of primate sociality, which is (IMHO) the main reason to care about dispersal--for the light it can shed on sociality itself.

On the whole, saying two things in one paper does not seem to have worked; when the paper is cited it is almost invariably simply to support the empirical point that females transfer. If you'd like to boldly go where not many seem to have gone ;-) skip ahead here to sociality and/or mutualism. And if you just want the bottom line: Conclusions


Key words: dispersal, social organization, kin selection, predation

Jim Moore, Anthropology Department, Harvard University, Cambridge, MA USA 02138
[Current 1998: Anthropology Dept, UCSD, La Jolla CA 92093-0532]

Intergroup transfer by males is nearly universal among social primates. Furthermore, among the most frequently studied monkeys - savanna baboons and Japanese and rhesus macaques - females typically remain in their natal groups, so troops are composed of related matrilines. These facts strongly support two major theories: 1) that kin selection is a powerful force in patterning sociality (if one is to live in a group, one should prefer a group of one's relatives), and 2) that the ultimate explanation for intergroup transfer is the avoidance of inbreeding depression (though both sexes would prefer to live with kin, one sex has to disperse to avoid inbreeding and for a variety of reasons the losing sex is generally male). Substantial rates of transfer by females in social species with routine male transfer would cast doubt on both ideas. In fact, evidence reviewed here indicates that female transfer is not unusual and among folivorous primates (e.g., Alouatta, the Colobinae) it seems to be routine. In addition to casting doubt on the demographic significance of inbreeding avoidance and favoring mutualistic and/or game theory interpretations of behavior over nepotistic ones, this finding supports the hypothesis that predator detection is the primary selective pressure favoring sociality for many primates. Finally, while female bonding [sensu Wrangham, R. W. (1980), Behaviour 75: 262-299] among primates appears to be less common than generally believed, the observed correlation between female transfer and morphological adaptations to folivory provides empirical support for Wrangham's model for the evolution of female-bonded groups.


Long-term studies of Japanese and rhesus macaques (Itani 1975, Sade et al. 1977) and savanna baboons (J. Altmann et al. 1977, Ransom 1981) have found that social groups in these species are organized around stable female matrilines, as is common in many mammals (Eisenberg 1977). Typically, single females do not leave their natal group (Packer 1979, Sugiyama 1976). When group fissions occur, close maternal relatives tend to segregate (Koyama 1970, Missakian 1973b, Nash 1976, Chepko-Sade and Sade 1979) so that, at least under some conditions, the average degree of relatedness (r) within daughter groups is higher than it was in the original (Chepko-Sade and Olivier 1979, but see Duggleby 1977, Melnick and Kidd 1983). In contrast, intergroup transfer by males is routine (Drickamer and Vessey 1973, Sugiyama 1976, Packer 1979). The behavioral and evolutionary consequences of female non- transfer have received considerable attention (e.g., Kurland 1977, Wade 1979); this attention, coupled with long term data on these cercopithecines, has led to the belief that female primates generally do not transfer. Consequently, the genetics of matrilineal groups have been used as models for species in which patterns of intergroup transfer have not been adequately established (e.g., Hrdy 1977 pp. 317-326), and fieldworkers faced with the disappearance of young animals tend to assume that females have died while males have transferred to another group (e.g., Dunbar and Dunbar 1976).

Wrangham (1980) attempted to trace this tendency toward female sociality to its hypothesized basis in feeding strategies. Following Emlen and Oring (1977) and Bradbury and Vehrencamp (1977), he argues that females will distribute themselves in time and space primarily in accordance with ecological factors, and male distribution and strategies will then map onto the distribution of females (see also Wittenberger 1980). For species that rely on large food patches, organized, cooperative groups of females will be able to displace single or non-cooperating individuals. "Selection is therefore considered to favor those who maintain permanent bonds and travel with their established allies" (Wrangham 1980, p. 268). Cooperation, Wrangham believes, will be most important for species with both "growth diets" distributed in large but discrete, defendable patches (e.g., fruiting trees) and "subsistence diets" of lower quality food that is evenly and widely distributed (e.g., mature leaves). Thus, during growth periods it is advantageous to be in a cooperative group to defend patches, and during harsher times the even distribution of the subsistence diet reduces feeding competition within the group.

Having established a compelling model for the origin of cooperative female groups, Wrangham goes on to consider the most probable composition of these groups. "The choice of individuals as preferred allies depends on which partners will raise inclusive fitness by the greatest amount. Other things being equal, individuals should cooperate with the closest available kin ..." (p. 268). This combination of kin selection logic and the observed demography of a half- dozen species has encouraged the view that primate social groups can be classed as either female-bonded (the majority of species) or male-bonded (e.g., chimpanzees), with affiliative behavior and cooperation within "the sex that does not transfer" being based on nepotism. Because transfers are rare relative to observations of affiliative behavior, this picture is often stood on end and "the sex that is affiliative" is assumed to remain in its natal group (see Walters 1981). However, as pointed out by Glander (1980) in his discussion of mantled howler monkeys, inferred nepotism cannot be invoked to explain behavior in species in which both sexes routinely transfer. To the extent that cooperation and affiliation depend on kin selection and nepotism, species in which female transfer is routine should be behaviorally distinguishable from those in which it is rare (cf. Crockett, 1984). Wrangham (1980) used the absence of any such clear differences to argue that female bonding, based on kin selection, is routine in primates and he specifically considers howler monkeys to be female- bonded despite "occasional" dispersal by females. However, more than 50% of immigrating or emigrating mantled howlers reported since Carpenter (1934) have been females (Moore, in preparation [1998 Eprint: This tabulation was never formally written up]).

The observation that stable female groups are not always kin based is not new (e.g., Klingel 1972) or, perhaps, very important. The fact that years of research have failed to discover systematic behavioral differences between female-bonded and non-female-bonded primates is important. If kin selection is necessary for complex sociality to evolve (as is sometimes argued), consistent large differences in intragroup r between species should be clearly reflected in their behavior. Failure to detect such differences calls for reevaluation of theory and/or observational methodology and analysis.

Based on inclusive fitness logic and the known stability of macaque and baboon matrilineal groups, Wrangham characterizes "female bonded" (FB) groups as follows:
1) Females typically breed in their natal group.
2) Intergroup transfer by males is routine and by females rare.
3) Intragroup relations among females are differentiated and consistent.
Criteria (1) and (2) relate to female matrilines, and are therefore traits associated with a secondary prediction of Wrangham's model (that it is better to cooperate with kin than non-kin). Criterion (3) relates directly to the potential for female cooperation, which need not be based on kinship (see Axelrod and Hamilton 1981).

While I agree completely with Wrangham's ecological model of FB groups, I believe the secondary emphasis on kinship is unnecessary. There is evidence of substantial female intergroup transfer in at least 7 of the 25 FB species he lists. If females transfer, groups will be made up of cooperating but unrelated individuals/matrilines; members of such groups would be female bonded but not matrilinealy related. According to kin selection theory, such groups should exhibit profound differences in social behavior when compared with truly matrilineal social units.


After a review of the literature on primate intergroup transfer, I constructed a preliminary chart similar to Table I and sent it to 18 researchers who had field experience with the 11 species on the chart. Their responses were incorporated into Table I; one species, Theropithecus gelada, was deleted after this first round. Hopefully, then, although the entries are still largely qualitative rather than quantitative, they do represent some sort of concensus.

In addition to the ten species listed in Table I, I came across references to female transfer or solitary females in twenty-one species for which there is very little published information on demography; these are listed in Table II. Although these scattered observations are not "statistically significant" (see below) indicators of transfer rates, in many cases they are all that is known for a species. I hope that this paper will encourage other workers to publish behaviorally as well as statistically significant observations.

Tables I and II present an underestimate of the total incidence of female transfer for four major reasons. First, I have not attempted a truly exhaustive literature review. Many references to transfers or solitary individuals occur in passing, during discussions of other facets of behavior, making it very difficult to ferret out all pertinent observations. Second, unusual occurrences may be underreported. Male dispersal is considered the mammalian norm (Greenwood 1980); thus, a fieldworker seeing two solitary males and one solitary female may be inclined to report routine male emigration with occasional peripheralization of (probably ill) females (see also Rasmussen 1981). Third, females may immigrate with less associated fighting and a shorter solitary period between groups than do males in species where both sexes are known to emigrate (e.g., Schaller 1963, Struhsaker and Leland 1979, Starin 1981, Estrada 1982, but see Sekulic 1982a; Harcourt 1978). Ironically, we might thus be more likely to miss seeing female transfers because they are more "routine" and uneventful than male transfers in species where both occur. Finally and most importantly, individual recognition of all members of a group is often extremely difficult (Aldrich-Blake 1970). When only some individuals are known, they are usually the adult males (e.g., Struhsaker 1975, Marsh 1979a; see Rowell 1974) who are typically larger, more scarred, and less abundant. Thus, females who disappear are less likely to be positively identified among animals sighted elsewhere (Crockett, 1984).

The following terms and concepts are used throughout this paper:

(1) Emigration. Emigration is departure from one's breeding unit. This paper focusses on natal emigration - departure from the breeding unit in which one was born (see Greenwood 1980) - and distinguishes emigration by an individual adult female from group fission in which several females leave their group as a unit (offspring or males may accompany females in either case).

(2) Immigration. Immigration is entry into an existing breeding group, or (rarely) formation of a breeding group by joining other same-sex emigrants (e.g., Cebus capucinus, Table II).

(3) Transfer. Transfer is emigration followed by immigration. Crockett (1984) restricts 'transfer' to entry into troops which have produced offspring, thus excluding entry into non-breeding predominantly male groups as well as, incidentally, cases of 'emigrant fusion' (cf. C. capucinus). I have chosen to include 'emigrant fusion' as a form of transfer because it also results (eventually) in breeding-group membership of unrelated individuals; as does Crockett's, my definition excludes joining a nonbreeding group or acting as a solitary foundress (but see below).

(4) Female-Transfer (FT) Species. A species is considered FT if it is polygynous and a significant (see below) percentage of observed group changes has been due to emigrations and/or immigrations by females. More emigrations than immigrations have been observed; this is not surprising since most potential immigrants in a population are unhabituated and may choose to avoid a studied group with its observer. Note that this definition thus includes some species in which female immigration has not been observed (3 out of 18 in Table III), and in some of these, females may not in fact transfer - i. e., they may emigrate and either individually found new groups or die. This point is important and is discussed further under Group Size.

(5) ?T Species. For a number of primates there are indications that females might routinely transfer, but the data are indirect. For example, Dunbar and Dunbar (1976) report a subadult female C. guereza who disappeared after being attacked by the group's adult male. They assumed she had died, but subadult female emigration resulting from male attacks has been reported for several FT species (Lippold 1977, Rudran 1973). Species for which there is indirect evidence for female transfer or where female transfer is strongly suspected on comparative grounds [e.g., Ateles spp. because of general similarities to chimpanzees; Klein and Klein 1975, Wrangham 1980, van Roosmalen 1984) are designated ?T.

(6) "Not-Female-Transfer" (NFT) species. These are well-studied species such as Papio anubis or Macaca fuscata in which female transfer is clearly atypical.

(7) Species with Insufficient Data. This category includes both (a) species for which there is little relevant demographic information (e.g., Nasalis larvatus, several Presbytis spp.), and (b) species such as Lemur catta (see Jones 1983) which, on the basis of work with a limited number of troops/populations, appear likely to prove NFT but for which the sample is still too small to demonstrate a negative result.

(8) "Significant" Rates of Transfer. The theoretical importance of female transfer hinges on the word significant as used above. Given any set of field observations, there are two questions that I have no answer to, but which must be asked:
(a) Are the observations statistically significant ? For example, only one immigration - by a female - has been observed in P. melalophos (E. Bennet personal communication) and clearly not much can be made of "100% female transfer (N=1)", other than to observe that if one saw only a single transfer among rhesus monkeys it would almost certainly be by a male.
(b) Assuming that the incidence of female transfer can be accurately estimated from the data, what level of transfer is theoretically significant ? Kin selection theory makes no explicit predictions about a lower limit to [average] r within a group, below which nepotism cannot be invoked to explain generalized affiliative and/or cooperative behaviors such as inter- matriline grooming or group territoriality. A 50% transfer rate must be significant in this sense, but what about 5% ?

Neither of these questions can be adequately answered today; neither of them has been asked prior to this. Statistically significant rates of transfer by either sex are elusive; we have very little demographic information on the vast majority of primates, with reasonable sample sizes for only a handful. This handful is made up for the most part of large-group terrestrial omnivores - savannah baboons and some macaques - which are precisely those species in which female transfer is expected to be rarest (see Folivory and Group Size). Many other primates, though, live in small groups high in the forest canopy and observation of these species is consequently difficult and their demography poorly understood (Aldrich-Blake 1970). If only large, sure samples are used to categorize FT and NFT species, there will be a strong bias against recognizing the extent of female transfer. To counter this bias, I have been deliberately liberal in classing species as FT (e.g., P. melalophos are considered FT on the basis of one observed transfer, and C. ascanius are termed ?T because two investigators independantly noted possible female transfer and solitary females).

Ultimately one would clearly like to know the proportion of females who typically transfer and the proportion of troops made up of transferred (=unrelated) females, for each primate species. Just as clearly, we do not have these data yet and readers should examine Table III and judge the existing data carefully. This paper draws attention to a theoretically important and probably widespread phenomenon, but because of limitations in the data available now (and undoubtedly for years to come) it must take a heuristic rather than definitive approach. By this approach I have probably included some NFT species in the FT and ?T categories. Such errors should obscure any existing correlations between female transfer and other demographic, ecological, or behavioral traits; any patterns found (Patterns) should be all the more robust for these errors.

Regarding the question of theoretically significant levels of female transfer, I have arbitrarily considered species "FT" if there is reason to think that more than about 10% of females change troops during their lifetime. For most of the FT species listed in Table III, I suspect that the true figure is much higher (P. entellus may be an exception). This figure is probably close to an order of magnitude greater than the observed female transfer rate for the best-studied NFT species. Hopefully, now that the question is asked and its importance demonstrated, someone will find a theoretical answer to it (cf. Bertram 1983, Packer and Pusey 1983).

Finally, I want to make it clear that this is a review of female transfer. In the majority of primates, male transfer is routine if not universal and the "FT" designation implies nothing about the presence or absence of male dispersal. The widely held view that only one sex "needs" to disperse in order to avoid inbreeding has promoted the dichotomization of species into exclusive "female transfer" and "male transfer" categories. The inbreeding avoidance hypothesis is discussed (and rejected) under Inbreeding and is dealt with in greater detail elsewhere (Moore and Ali 1984).

Clutton-Brock and Harvey (1977) present a summary of demographic data for thirty-four polygynous primates. The authors caution against using these figures as a reference source, but the data will suffice for a rough comparison of FT and NFT species. I used their data (with additional sources as noted) to create a sample of 59 species, listed in Table III. For many of the species and/or parameters listed, sample sizes are small and patterns (or deviations from patterns) should be considered foci for further research rather than established facts.


In this section I review features that either (a) are theoretically predicted to promote transfer by females, or (b) became apparent during the assembly of Table III. The primary prediction is that the incidence of female transfer will be associated with folivory (Wrangham 1980). Discussing his own observations of female transfer in red colobus, Marsh (1979b) suggested that female transfer was at times a means of avoiding infanticidal males. Infanticide is a rarely observed event that is theoretically expected to occur primarily in species with unimale breeding groups (when it occurs at all) and so I have considered the distribution of female transfer relative to both observed infanticide and to unimale troop organization. Finally, Ali (1981) argued that females in nonterritorial species would be able to transfer more easily than those of territorial species, due to greater familiarity with both neighbors and neighbors' ranges; I include a brief discussion of territoriality. Although the data - and more importantly, the definitions - are inadequate for testing the last two hypotheses, I call attention to them because they have important implications for understanding primate sociality. A functional relationship between female transfer and unimale territoriality would suggest that such species are 'overgrown blackbirds' and that the logic of polygyny threshold models should apply to them (see Mate and Range Choice).

While making Table III, it quickly became clear that FT species tend to live in relatively small troops, and that many are colobines with "flamboyant" natal coats and frequent allomaternal behavior. The post hoc discovery of an association between group size and female transfer proved valuable and is dealt with at length in this section and in the Discussion. Natal coats and allomaternal behavior were more recondite, but are briefly discussed in the hope that someone else may see a functional connection (if there is one).


Wrangham (1980) suggests that female transfer will occur in species with relatively uniform, monotonous and low-quality "growth" diets, e.g., folivores specializing on mature leaves. Unfortunately, factors such as variable chemical defence strategies, dietary opportunism, interplay between temporal and spatial patchiness, methodological uncertainties (e.g., foraging time vs. bulk consumed vs. energy content as dietary measures), and interpopulation dietary differences (extensively discussed in Montgomery 1978, Clutton-Brock 1977a, b) render quantitative characterization of the effective patchiness or content of a species' primary diet essentially unavailable. Diet is assumed to affect social organization, but it is harder to measure diet accurately than to determine demography and I have not attempted to review primate foraging data directly. It is possible to measure morphological features that can be used as indicators of dietary adaptations; though a step removed from the variable of interest, use of morphological indices avoids "unreal" variance introduced by evolutionarily recent diet shifts and opportunistic population differences in diet (see Milton 1981). One such index is the "coefficient of gut differentiation" (Chivers and Hladik 1980). The authors used measures of gut weight, surface area, and volume from a wide variety of mammals to establish an index that reflected known dietary variation. The one giving maximum separation between dietary groups was:

surface area (stomach + caecum + colon)
surface area (small intestine)

This ratio is largest among herbivores and smallest among piscivorous cetaceans. They have ranked 78 mammals according to this index, with "higher values reflecting a tract dominated by stomach and/or large intestine (for digesting leaves)", and lower values for species in which "the small intestine predominates (for digesting animal matter)"; frugivores tend to have intermediate values. Twenty eight of these species are social, polygynous primates. Considering only these 28 primates, eight of the 14 species ranked above the median value (the "more folivorous") are FT, vs only two out of the lower 14 (the "less folivorous") (X^2 = 3.9, p < 0.025, median test, one tailed). The highest ranking NFT species is M. sinica (eleventh out of the 28); no value is available for the closely related FT M. radiata. The lowest ranking ("least folivorous") FT primate is C. capucinus, at number 27.

This analysis ranks degree of "folivory" (i.e., gut differentiation index); it is not based on qualitative classification of species as "folivores" or "frugivores". Although these terms are conceptually useful, they have no generally accepted quantitative definitions (e.g., are howler monkeys "folivores" or "frugivores" ? - see Milton 1978). Consequently, the hypothesis being tested here is that there should be an association between folivory and female transfer - not that "folivores" are FT and "frugivores" are NFT.


Ali (1981) suggests that female transfer among Macaca radiata dilutta is a consequence of their highly overlapping home ranges; females are more familiar with the neighbors' ranges as well as with the neighbors, so the cost of switching groups is lowered. Mitani and Rodman (1979, Table II) have divided a sample of primates into territorial and nonterritorial species, which forms the basis for column No. 1 in Table III. No clear relationship between female transfer and territoriality is visible, but (1) the list does not distinguish female territoriality from male defence of females, and (2) territoriality is both hard to define (Kaufmann 1971, 1983, Verner 1977) and environmentally labile (e.g., Yoshiba 1968, Hamilton et al. 1976).


With few exceptions (the addition of the "SM/MM" category) I followed Clutton-Brock and Harvey's (1977) division of species into single male (SM) and multimale (MM) social groups in Table III. This division is clearly problematic. Some species show considerable intergroup variability in the number of resident adult males; such variability is especially marked among the colobines (Crook 1972). In addition, Eisenberg et al. (1972) argue that apparently multimale troops of A. palliata, P. entellus and others are in fact functionally unimale. Despite these difficulties, female transfer and "SM" social organization appear to be (weakly) associated (Table IV). This possible relationship suggests that qualitative classification of species' breeding systems may indeed be useful; it is not yet clear whether the modal organization or the variability (cf. Crook 1972) of a species is the more informative.

Table IV: Female Transfer and Number of Breeding Males

           FT      NFT         ?T & Insufficient Data
SM       7        1              11
MM       9        6              19

N = 53; X^2 = 1.86, not significant

Female transfer does occur under unusual circumstances in NFT species (see Female Transfer in NFT Species); similarly, infanticide by adult males occurs more often in some species than in others but no taxonomic group appears immune to the phenomenon (e.g., Busse and Hamilton 1981, Collins et al. 1984; see Angst and Thommen 1977, Hrdy 1979). Because both are unusual and opportunisti&cally observed behaviors, it is impossible to quantify correlations between frequency of infanticide and frequency of female t ransfer. Both seem commonest in Presbytis andAlouatta and relatively rare among the cercopithecines.


Hrdy (1976, 1977) listed a total of 13 species in which infants have highly visible, "flamboyant" natal coats. Four of these are FT species, two ?T and no relevant demographic information is available for the other seven. Most are in the genus Presbytis, and twelve are colobines, so phylogenetic and ecological factors may both be involved in this association (cf. Clutton-Brock 1974, Gartlan 1973). A further complicating factor is that we do not really know what is functionally "flamboyant" to the monkeys and their predators. Hrdy (1976) used "flamboyant" to refer "... to striking differences from adult coloration perceptible at a distance...", but listed as flamboyant only species whose natal coats are lighter in color than adults'; she classes P. entellus (a silver-grey monkey with a black natal coat) as "discrete but discreet" (1976: p. 144). Is a black infant on a silver P. entellus less flamboyant than a white infant on a mainly black C. guereza? A proper correlation is impossible without explicit and meaningful categories; in their absence one is limited to discussing patterns.

The same problem applies to the association between female transfer and allomaternal behavior (see Hrdy 1976, Quiatt 1979, Horwich and Manski 1975, McKenna 1979). Again, though not all FT species show allomaternal care of young infants, out of seven species listed by Hrdy as showing allomaternal behavior within 10 days of the infant's birth, 4 are FT and only 1 is NFT (Table III). The distinction between transfer of neonates and transfer of 2-week old infants is somewhat artificial, and allomothering itself is probably not a unitary phenomenon (Hrdy 1976); these issues are discussed further below.


If females are distributed according to resources and males are secondarily mapped onto the distribution of females (Wrangham 1980, Wittenberger 1980) then discussions of ecology and group size should be based on numbers of adult females/troop, not total troop size. For some species, direct counts of adult females (AF)/troop were used; for others, I assumed an adult:immature ratio of 0.5 (cf. Dittus 1979 - 0.43; Rudran 1979 - 0.47; Sugiyama 1964 - 0.61) and calculated the average numbers of AF/troop from data in Clutton-Brock and Harvey (1977). Combined, this gave a rough estimate of AF/troop for 49 of the species in the sample. Readers familiar with primate demographic data need no warning concerning this procedure and the data upon which it is based. These data suggest a pattern, but the real and artifactually introduced variance is great. Further work will hopefully reduce the artifactual variance, and it remains to be seen whether the patterns are strengthened or weakened by that process.

FT species tend to live in smaller groups (ca. 6.4 ± 4.2 AF/troop) than do NFT species (ca. 8.9 ± 2.7 AF/troop) (Table III). Kibale red colobus (ca. 17.9 AF/troop) and silvered leaf monkeys (ca. 13.0 AF/troop) live in large groups and seem to demonstrate that small size is not neccessary for female transfer; at 4.4 AF/troop, vervets indicate that small size is not a sufficient condition. It should be noted, though, that other studies have found vervets in larger troops (Cheney 1981: 7.7 AF/troop; Whitten 1982: 10.5 AF/troop), and P. cristata in smaller ones (based on Crockett Wilson and Wilson 1976: 4.8 AF/troop). It remains to be seen whether such intersite variability is noise in the system or the truly interesting demographic phenomenon.

An important point is raised here -- if the optimal troop size is based on only 3 or 4 adult females, single-female emigration from small troops may be homologous with troop fission in species with larger troops. In such cases, emigrant females would found new troops or die and, in the absence of immigration, FT troops would be based on single matrilines. This is a crucial issue, because if FT females also immigrate (i.e., truly transfer) then FT troops will often be composed of unrelated females. In one case the average coefficient of relatedness r is higher within FT troops than within NFT troops, and in the other it is lower. The consequences of such different values of r are presumed to be profound (e.g., Kurland 1977, Wade 1979, Breden and Wade 1981). Female immigration has been observed less frequently than female emigration, but often enough that true female transfer can legitimately be viewed as a phenomenon worth investigating (Table III). If female emigration- only species can be positively identified, comparisons of their social behavior with that of true FT and NFT species may greatly illuminate the significance of kin selection among primates.


In trying to explain the incidence of female transfer among primate species, it is presumably helpful to ask the question, Which individuals transfer? In the last section patterns among species were examined; in this, patterns within species are discussed. First I review cases of female transfer in the NFT macaques and baboons. If folivory, group size and female transfer are functionally related (see Discussion), it is no accident that the common decision to study large troops of terrestrial, generalist monkeys led to a vast number of data on a few NFT primates and very few data on FT species. Ironically, therefore, the only species for which we have large samples of individual observations of female transfer are those in which the phenomenon appears rarest. The extent to which intraspecific patterns can illuminate interspecific ones is unclear and readers should judge for themselves.

Under Age, Rank and Reproductive State in this section I apply the parameters that seem important intraspecifically - age, rank, and reproductive state - to the data available for FT species.


Occasional intergroup shifts by females have been reported for such "NFT" primates as Macaca mulatta (Altmann 1962, Vandenbergh 1967, Brereton 1981), M. fuscata (Burton and Fukuda 1981, Sugiyama and Ohsawa 1982), Papio anubis (Rowell 1969, Packer 1979), and P. cynocephalus (Hausfater 1975, Rasmussen 1981). Most of these observations represent only temporary shifts of several days to several weeks' duration, and many occurred under unusual circumstances: the establishment of the Caribbean rhesus colonies (Altmann 1962, Vandenbergh 1967), the initial stages of habituation (Rowell 1969, Rasmussen 1981), or following severe human disturbance of the monkeys (Sugiyama and Ohsawa 1982). Despite the variable associated factors, there is a fairly clear pattern -- NFT females shift groups primarily when they are sexually receptive and/or if they are peripheral and possibly under nutritional stress.

The majority of the observed intergroup shifts occurred when females were sexually receptive or were cycling subadults. At La Parguera, it is clear that temporary and permanent group shifts by females during the early 1960s were related to instability caused by introductions, but the effect was pronounced only during the breeding season (Vandenbergh 1967). Vandenbergh presents data on the seasonal timing of female and male shifts (his Fig. 3, p. 188); only 5 of 43 observed female shifts occurred during the nonbreeding months (X^2 = 12.9, p < 0.001). The two temporarily shifting females observed by Altmann (1962) and the one reported by Brereton (1981) all moved during the mating season. Most of the Japanese macaques discussed by Burton and Fukuda (1981) consorted with extragroup males during their absences, and in 9 of the 14 cases of female "desertion" of the troop reported by Sugiyama and Ohsawa (1982), shifting occurred during the mating season (these 14 cases include several repeat moves and moves by more than one female, and cannot easily be quantified). Among baboons, the 5 possible transfers reported by Rowell (1969) were all of young females who were about to start cycling (who apparently transferred as a group); 2 out of 3 temporary shifts by adult/subadult females seen by Hausfater (1975) were in the early stages of tumescence; and Rasmussen (1981) found a significant overrepresentation of swollen females in the 12 who joined his study troop. Discussing this pattern, Burton and Fukuda, Brereton, and Rasmussen all conclude that permanent or temporary female group shifting represents a mechanism of female choice, most likely for mate quality. While this explanation is reasonable, it invites the question, "why do females in these species so rarely choose ?"; as Rasmussen points out, relatively large numbers of shifts during relatively short periods of time (compared to total observation time on the population/species) suggests that some environmental factor is involved. If females are transferring to avoid predators (Rasmussen 1981), feeding competition (Sugiyama and Ohsawa 1982), or other factors, they might well time their shifts to coincide with estrous -- in effect using estrous as a passport to assure their favorable reception by strange males (cf. Pusey 1979).

Other cases of female transfer appear related to intragroup competition and perhaps simply an idiosyncratic personality. Sugiyama and Ohsawa (1982) found that most troop desertions occurred following cessation of a provisioning program, and were by young, peripheral females whose mothers had been trapped. This certainly suggests a feeding competition/exclusion scenario, although direct aggressive expulsion was not observed. Finally, the single adult female P. anubis who transferred at Gombe (Packer 1979) was exceptionally shy, skittish, noninteractive and peripheral (Moore, personal observations); whether her personality was cause or consequence of her transfer is unknown.


Harcourt (1978), Pusey (1979, 1980), and Jones (1980a, b) have described multiple cases of female transfer by known individuals and thus have been able to directly examine the significance of changing sociodemographic status for female transfer strategies; Marsh (1979a) and Haddow (1952) also discuss these problems based on observations of large numbers of unknown/partially known individuals. The patterns reported by the above authors seem generally applicable but most other species' samples are small and less detailed. In this section, therefore, I will only briefly discuss the "typical" female transfer(s) rather than tabulating all observed cases. The most important conclusion reached here is that different females transfer for different reasons, most apparently tactical - i.e., for short term or proximate motives - (for example, avoiding an infanticidal male) rather than strategic or ultimate (e.g., avoiding inbreeding). For reviews of the characteristics of dispersers in non- primates, see Gaines and McClenaghan (1980), Gauthreaux (1978), Lidicker (1975), and Moore and Ali (1984).

Age. Emigration by nulliparous young adult females is common and has been emphasized by several authors, in part because it "fits" the inbreeding avoidance hypothesis (see below). However, Harcourt (1978), Pusey (1979, 1980), Jones (1980a,b), Marsh (1979a), and Haddow (1952) also observed transfers by prime and old females, and it is difficult to assess the effects of age on transfer strategies without better life tables: the predominance of young adult transfer may be partially due to the predominance of young adults. Jones (1980a) did show that young and old females were more likely to emigrate than prime individuals, and points out that intragroup competition for resources will produce just this pattern of dispersal. Indeed, there are observations of subadult females being aggressively expelled from their natal troops (see below), and no other general hypothesis adequately accounts for emigration of very old females. However, young females might also transfer to avoid inbreeding, to chose mates, or to chose a territory, and different reasons will likely apply in different cases; also, at times prime adult females transfer (Marsh 1979a). To the extent that the relative qualities of home ranges remain stable over periods of time corresponding to a monkey's life, resource choice might be predominant among young emigrants searching for a place to settle down. Where male takeovers occur, mate choice might lead to episodic transfers by all ages, but especially by prime females who can more easily enter the group of their choice. Intragroup competition may lead to emigration by subordinates, who are most often subadult or old in age-graded hierarchy species.

Rank. Except for Jones' work on mantled howlers (see Expulsion), little is actually known about the relation of rank and transfer in female primates. Low ranking animals may be forced out of the group, and very high ranking individuals (of species in which rank is based directly on competitive ability) may be free to go where they choose. The only predictions one can make are that (1) high and low ranking females will emigrate for different reasons, (2) high ranking females will probably be more successful at immigrating than will low ranking females if the population is near K, and (3) members of the middle class will, as usual, tend to be conservative and to try to stay where they are.

Reproductive State. In contrast to the strong tendency for shifting NFT females to do so when sexually receptive, there is no clear pattern among the FT species. Chimp females tend to transfer during estrous (Nishida 1979, Pusey 1979, 1980) and transfer by sifakas of both sexes occurs mainly if not exclusively during the breeding season (Jolly et al. 1982) but these seem to be the only FT species for which this is true. For example, Sekulic (1982a) describes a solitary female red howler who was cycling and copulated with troop males, but during her study of mantled howlers, Jones (1980) found clear support for "[T]he observation among workers in Costa Rica ... that dispersing females are frequently pregnant or accompanied by offspring." Again, this variation probably reflects different reasons for shifting: expelled females may have little choice of timing; females choosing a mate or range might transfer during estrus; females avoiding an infanticidal male would transfer while lactatingor, possibly, pregnant.

Though understandably hard to confirm, there is an intriguing suggestion that pregnant females emigrate/transfer at a higher than expected rate in some FT species (Haddow 1952, Jones 1980a; scattered isolated observations), although in others female emigrants are usually nullipares (e.g., Crockett, 1984). If pregnant females are over-represented among emigrants, the phenomenon may be (1) an epiphenomenon (e.g., of feeding competition, if pregnant females are more easily expelled), (2) a result of local resource competition (Silk 1983), or (3) the result of some benefit acruing to a disperser who is pregnant (vs. emigrating for the same reason while nonpregnant). The advantages of a fetus to its dispersing mother could include: a potential mate if the female colonized totally new habitat (cf. Lidicker 1975), a potential ally in a new group of unrelated individuals, or a second set of coadapted genes which could promote inbreeding at the female's destination, with any of these being accomplished without risking a vulnerable infant during the transfer (thanks to W. Shields for the inbreeding suggestion). For some small mammals, there is also a possible overrepresentation of pregnant individuals among the subset of dispersers who are female and healthy (Lidicker 1975), so the phenomenon could be general.

Finally, some observed female transfers in gorillas and chacma baboons followed reproductive failure (death of an infant) (Harcourt 1978, C. Anderson personal communication, respectively). If the two were linked, some female transfer among primates may be analogous to mate and/or site desertion by birds (see Greenwood and Harvey 1982).


Three major hypotheses have been advanced to explain dispersal patterns in vertebrates: inbreeding avoidance, mate/range choice, and intrasexual competition leading to expulsion. In addition, Drickamer and Vessey (1973) and Packer (1979) have shown that males may transfer to increase their opportunities to mate. In this section I discuss all four hypotheses relative to the data presented on female transfer. Both female choice and female-female competition appear to play a significant role in female transfer among primates; inbreeding avoidance and (not surprisingly) mating opportunities do not. These hypotheses have also been evaluated by Harcourt (1978) and the interested reader should refer to that paper for further discussion and somewhat different conclusions.


Harcourt (1978) and Pusey (1980) have argued that female transfer in gorillas and chimpanzees (respectively) is a behavioral strategy for the avoidance of inbreeding depression. This is the most commonly accepted ultimate explanation for male natal transfer in primates (e.g., Itani 1972, Packer 1979) and for natal dispersal in mammals and birds in general (Greenwood 1980, Maynard Smith 1978). While this hypothesis might explain female transfer among chimpanzees in those populations wherein males do not transfer, it is less satisfactory for the other species in Table I and II, in which male transfer is also routine (Marsh 1979a,b, Starin 1981, Crockett, 1984). Routine transfer of breeding males between polygynous groups minimizes within-troop inbreeding (Melnick and Kidd 1983) so female transfer is not likely to be a response to cumulative inbreeding. The possibility of father-daughter incest avoidance remains, but reported average male tenure lengths of from 2.25 to about 5-6 years for langurs and howlers (Sugiyama 1967, Hrdy 1977, Rudran 1973, 1979) suggest that the opportunity for incest rarely occurs in these species, at least (Crockett, 1984); the age of first conception for wild Presbytis entellus is about 4 years (Dolhinow et al. 1979, C. Vogel, personal communication). Furthermore, behavioral observations of females being expelled or peripheralized from their natal group (Rudran 1973, Dunbar and Dunbar 1976, Lippold 1977, Jones 1980a) and of intragroup infanticide (Goodall 1977, Fossey 1976 cited in Hrdy 1979) indicate that many females are avoiding aggression, not inbreeding, when they emigrate. Finally, it is arguable whether avoidance of moderate inbreeding (as distinct from incest) has had a significant effect on dispersal patterns of any animals. It is more likely that dispersal patterns have determined the potential severity of inbreeding depression in different species (see Bengtsson 1978, Smith 1979, Shields 1982, Moore and Ali 1984).

It is well worth noting that the inbreeding avoidance hypothesis of natal transfer is a purely "ultimate" one, requiring positive selection for transfer. No proximate stimulus (other than maturation) should need to be invoked to explain its occurrence. In contrast, the other hypotheses discussed below are all "proximate" ones, based on responses to specific stimuli and requiring selection for individuals who can evaluate situations and decide upon an appropriate course of action; e.g., an attacked female can either risk continued intragroup hostility or she can risk the uncertainties of transfer. Such conditional transfers presumably involve some form of intelligence to a much greater degree than that implied by the inbreeding avoidance hypothesis.


A number of hypotheses for the evolution of polygyny have been proposed (see S. Altmann et al. 1977). The most widely applicable of these are the "competitive female choice" (S. Altmann et al. 1977) model, originally proposed by Verner (1964) and elaborated by Orians (1969), and the "cooperative female choice" model suggested by S. Altmann et al. (1977). If females are choosing to shift between troops in order to maximize their RS, then models for the evolution of polygyny may be applicable to understanding primate social organization. Ralls (1977) has argued against indiscriminate application of the Verner-Orians (competitive) model to mammals because three of its conditions are not often met in this class. The model assumes: (1) there is a need for male parental investment (PI), uncommon in most mammals; (2) females choose males, which Ralls considers probably untrue for polygynous pinnipeds and hamadryas baboons (but see Bachmann and Kummer 1980); and (3) females raise their young within a male's territory, depending on its resources, which is not the case for many polygynous mammals (Wilson 1975, Eisenberg 1981). For most of the primates, though, these conditions hold (assuming that male territorial defence and protection from predators or other males can be considered PI, and that female transfer is prima facie evidence for female choice). Within this mammalian order, at least, the competitive female choice model cannot be automatically rejected

The competitive model proposes that males control varying amounts of resource neccessary to females, and females compete among themselves to join the most successful males ("resource defence polygyny", Emlen and Oring 1977, Bradbury and Vehrencamp 1977). While the logic of this hypothesis is compelling, in practice it is extremely difficult to determine what key resources males are defending (Lenington 1980), though broad patterns of critical resource type can be inferred from interspecies comparisons (e.g., nest site vs. food, Wittenberger 1976). Another difficulty is that females may be selecting superior males for their (presumably superior) associated territories (Garson 1980, but see Colias 1979), selecting sites for their (presumably superior) associated males (Borgia 1981), or directly selecting superior males (Downhower and Brown 1980) or resources (e.g., colonial nesting birds, Wittenberger 1976). The expected covariance of male quality (which may be genetically based, benefitting the female's offspring as well as herself, or purely developmental, benefitting only the female -- Borgia 1981) and range quality has led most researchers to explicitly combine the two into the "quality of the breeding situation" (Wittenberger 1976). This is probably appropriate for species in which males invest directly in each individual female/offspring; under such conditions, both resource and male investment are depreciable and females should compete for them. However, when the only male investment is nondepreciable (e.g., predator detection, territory defence), any interfemale competition will be over resources alone (S. Altmann et al. 1977). If male quality is most important, group size would be largely the outcome of male distribution and mating strategies. On the other hand, if male investment is low, group size would be determined primarily by female feeding strategies (Wrangham 1980) and the prime assumption of the competitive model -- that females compete with each other for group membership and that females prefer monogamy in the best available breeding situation -- is violated. It is in fact important to distinguish between female choice of mate or of range quality.

The cooperative female choice model points out that females may benefit from the presence of other females (up to a point); group size will be determined by females according to the nature of these benefits and males will then compete amongst themselves for access to these groups (S. Altmann et al. 1977; "female defence polygyny", Bradbury and Vehrencamp 1977, Emlen and Oring 1977; Wittenberger 1980, Wrangham 1980). Male quality might still covary with group size or range quality, but in this case it would be because large, healthy groups attract the best males, not vice versa.

Mate Choice. For primates in which recently immigrated males may commit infanticide (see Hrdy 1979), females will be under strong pressure to choose males who are likely to prevent such immigration for a long time (Marsh 1979b). Females may do this either by remaining in their natal troop and actively preventing weak males from immigrating (Packer and Pusey 1979, Moore, in preparation; cf. Cox and LeBouef 1977), or by transferring to a group with a strong male (Marsh 1979a, b, Wrangham 1979, 1982). Among the red colobus observed by Marsh and the gorillas Wrangham discusses, there was no evidence of "serious" aggression between resident and immigrating females, as would be expected if food were limiting and females were selecting a feeding range. It may be that feeding competition is minimized by resource patchiness (see Colobines vs. Cercopithecines), but if not, by elimination, females must be choosing males rather than ranges. Correlational support for the generality of this hypothesis comes from the apparent association between female transfer and infanticide by males (see Single Male/Infanticide). However, in some cases it appears clear that food is limiting and that females are choosing (or being excluded from) groups on the basis of resource availability (see below).

Range Choice. If food supplies are unpredictable in a patchy and changing environment, females might transfer between groups in an attempt to track resources (Marsh 1979a, b). This suggests that "groups" are defined by one or more resident males who are site-faithful (otherwise, presumably the entire group would move with the resource base, i.e., migrate). Male site- faithfulness is the pattern found among most polygynous birds (Greenwood 1980 and references therein). However, among most FT species males disperse at least as much as do females and therefore might be expected to join in long- range group movements if these occurred. Also, as Marsh argues, lack of resistance to female immigrants indicates that the females he observed were not trying to protect their food supply, which they should do if resources were scarce (see above).

Though Marsh's rejection of the range choice hypothesis seems appropriate for the cases he observed, several caveats should be noted. First, even lethal "aggression" is not always overt (Marler 1976) and his immigrant females may have suffered from undetected subtle harrassment, exclusion from feeding sites, etc. (cf. Dittus 1979, 1980). Second and more important, there have been observations of resistance to potentially immigrating females in other species (Jones 1980a, Pusey 1980, Sekulic 1982a). These contrasting observations may perhaps be reconciled by recalling that the environment is not static. Population densities are not determined by optimal conditions, but by sporadic and largely unpredictable "crunches" -- e.g., droughts (Southwood 1977, Wiens 1977, Cant 1980, Moore 1983). A resident's attitude toward an immigrant will inevitably depend more on her assessment of current conditions than on her "expectations" regarding an uncertain future (Wittenberger 1981) and during a good period the cost of expelling the newcomer may outweigh the potential benefit of not having to compete with her during a future crunch.


The range choice hypothesis and the expulsion hypothesis both hold that females leave a troop in order to improve their situation vis-a-vis the daily environment. In the range choice scenario social factors are considered insignificant relative to the female's decision; according to the expulsion hypothesis social factors -- especially resource competition -- are paramount. The distinction is primarily heuristic, since in practice resource competition and resource availability are inextricably linked. As used here, expulsion includes both aggressive rejection and "quiet" exclusion from resources (displacements etc.) (Marler 1976). It is clear from even a brief review of the literature on vertebrate demography that expulsion is at least proximately responsible for the majority of natal dispersal by both sexes (reviews: Lidicker 1975, Gauthreaux 1978, Gaines and McClenaghan 1980, Dobson 1982). Low-ranking individuals may suffer from decreased access to environmental resources (cf. Dittus 1980, Gauthreaux 1978) and from spiteful harrasment which can inflict direct and obvious costs (e.g, Silk 1980; cf. Pierotti 1980) or indirect and subtle costs via endocrinological stress (Dunbar and Dunbar 1977, Keverne et al. 1982). At some point these costs appear greater than the cost of emigrating (predation, lack of shelter, etc.), and the individual leaves (Lomnicki 1978). Among rodents, at least, most probably die (Gaines and McClenaghan 1980, Lidicker 1975).

Howard (1960) distinguished between innate and environmental dispersal ("pre-saturation" and "saturation", respectively; Lidicker 1975). Environmental dispersers are those who are expelled by resource competition; innate dispersers emigrate without any visible social/environmental impetus. Howard points out that environmental dispersal needs little "explanation" while innate dispersal is somewhat paradoxical, since apparently large, healthy individuals should have no reason to move. Subadult male primates often become peripheral with no sign of being forced from the group, and Packer (1979), Itani (1972) and others have used this observation to support the idea that resource (in this case, mate) competition cannot explain natal dispersal. However, aggression toward maturing subadults can be severe and even fatal among primates (Simonds 1965, Struhsaker and Leland 1979) and natural selection should favor a tendency to avoid inevitable conflict by emigrating before being attacked. Dominance ranks are probably based on social factors as much as on innate competitive ability (Rowell 1974, Wade 1978) and so it is not surprising that young males, subordinate and often peripheral in their natal troops, may attain high rank following transfer (but see Packer 1979:23). Emigration by adult, high ranking males (e.g., Itani 1972, Whitten 1982; but see Henzi and Lucas 1980) is clearly a different phenomenon and may represent a form of "bet-hedging" (Gillespie 1974, Rubenstein 1982) (Moore and Ali 1984; see also Hamilton and May 1977). It is clear though that much dispersal/transfer can be explained either proximately or ultimately by expulsion. No complex ultimate explanation is necessary for the phenomenon of subordinate individuals dispersing or dieing; they are simply playing out bad hands and often losing (Williams 1966:218, Lomnicki 1978). These and other issues connected with primate dispersal are discussed further elsewhere (Moore and Ali 1984).

Jones (1980a,b) has presented a detailed account of female transfer among mantled howler monkeys; young of both sexes actively challenge older same-sex individuals and either rise in rank or emigrate. Young emigrants are able to join other troops; old emigrants (who have lost to younger challengers) were not observed immigrating. These older individuals apparently either die or form new groups. All of the transitions Jones observed were accompanied by aggression, and of nine observed emigrations, six were preceded by coalitional attacks in which two (usually young) individuals targeted a third (usually old) (1980a). These coalitions were sometimes directed against a relative of one member. Other observations of intrasexual expulsion are listed in Table I. Rarely, intersexual expulsion occurs: following a male takeover, the new adult male may aggressively expel subadults of both sexes from the troop (Rudran 1973, Lippold 1977). Hrdy (1977:278) has suggested that feeding competition between prereproductive and adult females would lower the adults' reproductive success (and hence that of the new male); given short male tenure this cost might justify the expulsion of a potential mate. Whether this interpretation is correct or not, it is clear that these young females are actively driven from their natal troop.


Non-natal male transfer among several species appears to be an attempt to maximize access to sexually receptive females (Drickamer and Vessey 1973, Packer 1979). Such transfer by dominant males is here distinguished from emigration by subordinates who leave because they are denied access to mates. It may be that these dominant emigrants are looking for troops with more females than their current one -- mating opportunities -- or that they are bet- hedging (see above). Finally, Richard (1974) and Kurland (1977) have suggested that female primates will prefer to breed with non-natal males because these males have demonstrated their ability to survive the stress and danger of the transfer process; females should mate only with males who had passed the test (cf. Zahavi 1975).

In contrast, although females may compete with each other for access to particular adult males (e.g., Seyfarth 1976, Robinson 1982) there is no indication that female primates ever seriously lack for mating opportunities (see Trivers 1972), even when no males are resident in their group [grey langurs (Moore, personal observations)].


Colobines vs. Cercopithecines

McKenna (1979) has summarized behavioral differences between colobines and cercopithecines (roughly speaking, FT and NFT respectively) and suggests that folivory reduces intragroup feeding competition among colobines, thus reducing the importance of dominance among females and permitting the relaxed, loose-knit society and allomothering that characterize this group. He points out that an important feature of colobine society is the relative lack of importance attached to kinship in the formation of social bonds; for the competitive macaques, kin selection favors cooperative groups of female relatives. This lack of emphasis on kinship and dominance allowed the evolution of allomothering, since mothers need not fear the death of their infants at the hands of highly dominant, competitive females (McKenna 1979; see also Hrdy 1976).

Although their diet may render colobines less behaviorally competitive, unrelated individuals are almost by definition genetic competitors and it is something of a paradox that matrilineal macaques should resist related allomothers who cannot be trusted while FT colobine mothers freely let other females handle their neonates. Similarly, if one accepts Hrdy and Hrdy's (1976) hypothesis that the age-graded female hierarchies found in grey langurs result from altruistic abdication by older females, then one must accept the occurrence of greater altruism among individuals less closely related on average than are the nepotistic macaques. These paradoxes suggest that "selfish allomother" hypotheses (Wasser and Barash 1981, Vogel in press, Hrdy 1976) may be correct, and that age-graded hierarchies are the outcome of competition and decreasing competitive ability among old females (Jones 1980a). Knowledge of species' demography is crucial to our interpretation of observed behavioral differences (Riedman 1982).

The above paragraph compares colobines with cercopithecines, yet some colobines don't fit the FT prototype (e.g., P. entellus and C. badius are both found in large multimale troops over much of their ranges), and a number of cercopithecines are here considered FT or ?T. These "anomalous" species provide the most interesting tests for the behavioral significance of female transfer. For example: female transfer has been observed in Macaca radiata (Rahaman and Parthasarathy 1969, Ali 1981, Pirta, personal communication); artificially introduced female M. arctoides were readily accepted by a feral troop (Bertrand 1969) in marked contrast to the aggressive rejections observed in M. mulatta (Southwick et al. 1974) and passive intolerance of M. fascicularis (Angst 1973); and M. sylvanus' transfer patterns appear to be unique (Taub 1980). These three species are the only single-mount ejaculators in Macaca, and Shiveley et al. (1982) have suggested that this copulatory pattern is the result of (apparently) low rates of male transfer, hence (inferred) greater genetic relatedness and (observed) low rates of open competition among males within troops (see also Wade 1979). Remarkably little is known about wild arctoides (Roonwal and Mohnot 1977) and radiata males do transfer (Ali 1981), so more data are needed before this hypothesis can be adequately evaluated. M. arctoides is the only macaque with a flamboyant natal coat (Hrdy 1976) and McKenna (1979) has called attention to the general similarity of peer relationships and infant development in radiata and the colobines. It is notable that both Wade (1979) and Shiveley et al. (1982) consider intermale tolerance in radiata a consequence of inbreeding and hence high average r within groups, rather than representing sib or half-sib cohorts (J. Altmann 1979) within an outbred society. Without knowing typical rates of female transfer in these species it is hard to interpret behavioral observations. These apparent cross-taxa concordances of behavior, morphology and demography circumvent the confounding effects of phylogeny on tests of ecological theory (see Gartlan 1973) and richly deserve further study.

Female transfer, optimal group size, and the origin of groups

There are numerous potential costs and benefits to living in a social group (reviews by Alexander 1974, Bertram 1978). The benefits seem divisible into two categories: (1) improved feeding efficiency (including, for primates at least, the ability to compete successfully with other groups) (cf. Wrangham 1980), and (2) increased ability to detect and/or avoid being eaten by predators (Alexander 1974, Rowell 1979, van Schaik and van Hooff 1983). Rodman (1981) points out that groups may be larger than optimal for individuals because the inclusive fitness cost of excluding kin (who have little chance of joining another group if the habitat is saturated) may be greater than the individual cost of retaining related competitors. However, I believe this is only true if there is a cost to excluding kin - i.e., a relative is worse off alone than in a group of two or more - and hence inclusive fitness mathematics are insufficient to create groups. An individual fitness advantage is required.

While both classes of benefit are probably important (Rubenstein 1978), it is always somehow more satisfying to be able to say which is more so. Following Wrangham, I accept "the principle that evolutionary pressures on social systems can be ordered with respect to the importance of their effects" (1980:263) and consider female feeding strategies the ecological starting point for understanding the function of groups in different primates (Wrangham 1979, 1980).

Wrangham's (1980) model for cooperative female sociality via intergroup competition seems to explain the function of NFT troops, which tend to be large, competitive, frugivorous and nepotistic (e.g., rhesus macaques). However, many FT primates are folivores living in smaller troops. If individuals join groups in order to compete with other groups and if intragroup competition is low among folivores (Wrangham's model; cf. the cooperative female choice model of S. Altmann et al. 1977) then one would expect these species to live in relatively large troops. Most do not (as shown under Group Size). However, as folivores (see Folivory) they may be, in effect, "small gorillas" and the logic Wrangham applies to gorillas should apply to them as well. If they are adapted to a food distribution that is relatively uniform and constant, according to Wrangham's feeding competition model females of these species should be solitary. Since they are not, a separate explanation is needed for the formation of troops in small-group FT species. There are at least two possible explanations -- females may form groups to escape (a) infanticidal males or (b) predators (Wrangham 1979) (see Table V).

Table V: Troop Function and Optimal Troop Size in Primates: Hypotheses
1) Intergroup competition at resource patches favors groups; large size favored by competitive escalation (Wrangham FB species). Works well for NFT species
2) Female groups form around males who protect them from infanticidal males (Wrangham, Marsh).
a) Resource patchiness minimizes intragroup competition, so polygyny arises due to minimal cost (cf. Waser, Crook, Altmann).
FT: Possible but patchy resources should favor 1.
b) Group size determined by the density of resources in the area that is economically defendable by a male (Crook et al.). FT: Possible but see Table VI; possible method/measurement problems.
3) Females form groups with each other as an antipredator strategy, and males are 'tacked on'; group size is a compromise between vigilance efficiency and feeding competition. FT: Probable but relies on numerical relationship that is at present untestable.

Van Schaik (1983) regressed the infant:adult female (AF) ratio against number of AF/troop for a set of 27 censusses of 14 primate species. Twenty-two of the 27 slopes were negative, suggesting that reproduction--and presumably, therefore, feeding efficiency--is maximized only in the smallest groups and hence that sociality exerts a uniformly negative effect on foraging. By elimination, he argues, "avoidance of predation confers the only universal selective advantage of group living in diurnal primates," and hence Wrangham's (1980) model is incorrect. Van Schaik explicitly excluded species Wrangham considered non-female bonded; however, by the criteria used in this paper, his sample includes 6 FT, 2 ?T, 4 "no data" and only 2 NFT primates. He therefore inadvertantly has provided evidence of intragroup competition within FT troops, but has not tested Wrangham's model. In fact, the infant/AF regressions for the 3 NFT censusses have an average slope of +0.0476 vs. -0.0723 for censusses of FT and ?T species (N=16) (U=5, p < 0.05, two-tailed). Thus, these data provide limited support for Wrangham's hypothesis, as well as for the importance of predation pressure for FT primate sociality (see below).

In species in which males may commit infanticide following male replacements, females would benefit by joining a strong male who will prevent such replacements (Wrangham 1979). Observed elevation of female transfer rates in red colobus following a male replacement supports this mate choice explanation for female transfer (Marsh 1979b). In this model, group size is determined either by resource patchiness or by the area a single male (or cooperative male group, e.g., chimps) can defend.

Resource Patchiness. If resources are patchy in space and time, an individual will require a number of patches to ensure a dependable food supply. If each patch is larger than the individual can utilize at any one time, there may be very little feeding cost to forming groups (Waser 1977; see also Crook 1972, Altmann 1974). Maximum group size would be determined by intragroup competition based on the size and distribution of resource patches.

The major difficulty with the resource patchiness hypothesis of group sizes is that one would expect patchiness to be associated with intergroup competition and hence escalation in average troop size (Wrangham's model). It is possible that intermediate patchiness, intermediate dependance on patches (e.g., 'folivore/frugivores'), or energetic constraints on folivores lead to small, FT groups while quantitatively greater patchiness/dependance on patches promotes a qualitative shift to larger NFT troop organization. Testing this hypothesis will be difficult and I do not attempt it here.

Economically Defendable Area. Crook et al. (1976) suggest that troop size may be determined by resource density in the area a male (or cooperative males) can economically defend from other males (cf. polygyny threshold models, discussed above under Mate and Range Choice). Folivores may be energetically constrained to small home ranges (Clutton-Brock and Harvey 1977), but leaves are relatively abundant; group size would be a complex function of resource density and quality, with a ceiling set by males' ability to defend a range.

If most/all FT species have troop sizes based on males' ability to defend an area, there should be a positive association between female transfer and the 'index of defendability' defined by Mitani and Rodman (1979). This index, D, is the ratio of the average day range length to the diameter of a circle with area equal to the average home range. Values of D > 1 are logically and empirically associated with territoriality (Mitani and Rodman 1979). Female transfer is apparently not related to D (Table VI), but before rejecting the Crook et al. hypothesis it should be noted that both the FT/NFT classification and the values of D calculated by Mitani and Rodman are based on relatively sparse data; failure to find an association between two such dichotomies may be due to lack of data more than to lack of association.

Table VI: Territory Defendability and Female Transfer
Taxa D >= 1 D < 1
FT 1) P. entellus (Yoshiba 1968)
2) A. seniculus
3) P. verreauxi
1) P. entellus (Jay 1963)
2) A. paliatta
3) C. b. tephrosceles
4) M. radiata
5) P. troglodytes
6) G. gorilla
NFT 1) C. aethiops 1) E. patas
2) M. mulatta
3) P. anubis
4) P. cynocephalus
D = 'index of defendability' (Mitani and Rodman 1979). See text for explanation.


The second major hypothesis regarding FT species is that females join other females in order to increase predator detection efficiency; males are something of an afterthought, competing amongst themselves for access to exiting groups. The antipredator model is based on the assumption that groups can better detect/confuse/intimidate predators and/or that individuals are sheltered from predators by the presence of other individuals who may be taken instead (Bertram 1978 and others). Members of a group should prefer some optimum group size greater than one, reflecting a balance between intragroup feeding competition and anti-predator strategy. This optimum size has been experimentally and theoretically sought in numerous studies of flocking in birds (Pulliam 1973, Powell 1974, Seigfried and Underhill 1975, Bertram 1980, Elgar and Catterall 1981) and in mammals (Berger 1978, Leighton-Shapiro 1980; see Dimond and Lazarus 1974, van Schaik et al. 1983). Such studies have repeatedly found a strong negative correlation between individual vigilance (eg., glance rates) and group size for small groups, but the relationship is not linear; above a certain size most flocks show fairly constant individual glance rates. Pulliam (1973) showed mathematically that, for a series of realistic parameters, groups of 5-6 have a better than 90% chance of successfully detecting an attacking predator. If attacks are frequent, the cumulative probability of the predator winning a round are increased and so larger flocks may be favored. For infrequent attacks, though, the simple model should hold -- predator detection efficiency rises rapidly with increasing group size up to groups of about five, then levels off. Elgar and Catterall (1981) were the first to explicitly test Pulliam's model, and their data on sparrows strongly support it, differing primarily in that the inflection point - at five/flock - is sharper than predicted.

Data from sparrows, doves, starlings, bighorn sheep, and rhesus monkeys all indicate that predator detection is most efficient (i.e., maximizes the detection ability/added competitor ratio) at group sizes of about 4 - 8. As shown above (under Group Size), the average number of adult females/FT troop is 6.4; excluding Kibale red colobus and P. cristata (where this number is more than twice as large as in most other FT groups), this average is 5.2 (N=16, Table III). This result is not necessarily inconsistent with the anti-infanticide hypothesis, but could not have been predicted by it. It is fully consistent with and predicted by the hypothesis that troops among most FT species are based on groups of females who form groups in order to more efficiently detect predators. The advantage of such groupings depends on relative proximity, so that one individual's alarm reaction or call can convey specific information to the others -- they can see in what direction she is orienting/fleeing, and so take appropriate action. For many species, such a small, non-dispersed group of females would be defendable by a single male, and male infanticide could follow (Hrdy 1974, 1979).

The anti-predator and anti-infanticide hypotheses roughly correspond to the cooperative and competitive female choice models of S. Altmann et al. (1977). According to the anti-infanticide hypothesis, no bisexual group would be too small; a female would tolerate additional females only because of low costs to doing so. In contrast, the anti-predator hypothesis implies that groups could indeed be too small; members of such groups should encourage immigration with affiliative behavior toward strangers (Rodman 1978). Oppenheimer's (1968) observation of three female Cebus capucinus from two troops joining together and forming a new territorial group - without a male - is inconsistent with the anti-infanticide hypothesis, and there are some indications that hamadryas females may encourage immigration by other females (H. Kummer, personal communication). Little other pertinent information is available.

The chief difficulty of the anti-predator hypothesis is that troop size variability within FT primates is not well explained; though the FT average of 6.4 AF/troop agrees well with the prediction, this average is based on a range of 1.9 to 17.9 AF/troop; excluding outliers, the range is still 1.9 to 9.7. An analogous problem holds for intraspecific variability. van Schaik et al. (1983) found a negative correlation between party size and height in the canopy for M. fasciculari, and suggest that larger groups are favored near the ground because of increased risk from terrestrial predators. They argue from this result that intraspecific variation in primate party sizes may be explicable by the predation hypothesis. Although the significance of predation by raptors and phenological constraints on party size in the upper canopy need to be examined more carefully, these findings represent one possible solution to the problem of variation in group sizes among FT species. It will be difficult to fully test this hypothesis without accurate species- and population-specific measures of 'predator pressure', which may be impossible to gather.

In summary, current theories hold that primate gregariousness must have evolved in response to either feeding competion, predation pressure, or male infanticide. Groups that formed in response to feeding competition should be female bonded, so significant rates of female transfer in some species are prima facie evidence supporting the predation or infanticide hypotheses for those species. It is extremely difficult to conclusively distinguish these later two hypotheses, but comparative evidence based on group sizes and vigilance rates gives somewhat more support to the predation argument.


Female transfer, kin selection and mutualism

There is a growing body of evidence that individuals respond differentially to kin and non-kin in a wide variety of organisms, and primates are clearly no exceptions (reviews in Bekoff 1981, Holmes and Sherman 1982). The mechanisms by which individuals recognize kin are not clearly understood but include the "coefficient of familiarity" (Bekoff 1981) and possibly learned or innate phenotype matching (Wu et al. 1980 [eprint note: Fredrickson & Sackett 1984 (J. Comp. Psychol. 98:29-34) attempted to replicate Wu et al, and concluded the original result was a Type I error], Small and Smith 1981, Holmes and Sherman 1982). This differential and normally preferential treatment of kin has been shown to have genetic as well as demographic consequences in several primate species (see Richard and Schulman 1982). Attendant kin selection may have been a primary force in the evolution of social behavior itself (West-Eberhard 1975, Wade 1979), and Waser and Jones (1983) consider adult association with kin a "prerequisite" for complex sociality. Given all this, the problem is clear: why are some troop-living primates essentially matrilineal, as kin selection theory seems to predict mammalian groups should be (Wrangham 1980, 1982; but see Wasser 1982), while the FT species apparently are not ?

The key seems to lie in the foraging strategies of females and hence in the function of the groups themselves. Briefly and typologically, FT species tend to be folivores, living in groups which apparently function to detect predators; these groups are limited in size by intragroup feeding competition. The benefits of early predator detection do not depend on costs to conspecifics; FT species are, in general, "non-interference mutualists" (Wrangham 1982). In contrast, NFT species tend to be generalists with intergroup competition for patchy resources favoring large troops. Again, troop sizes are limited by intragroup competition but whereas FT troops need only attain a sufficient size (for predator detection), NFT troops will be under pressure to grow larger than their neighbors (i.e., selection acts on individual members of the troop who by their behavior then effect appropriate changes in group size). For the NFTs, the primary benefit of group living depends on costs inflicted on other conspecific groups; in Wrangham's terms, they are "interference mutualists". As Wrangham (1982) demonstrates, such interference mutualists should favor stable kin-based groups, while "extreme" non-interference mutualists may form unstable groups with little or no bias toward living with kin. He goes on to conclude, however, that "(t)here are no clear cases of NIM (non-interference mutualism) causing female grouping in primates. Possibly they occur in species with unstable groups such as some ungulates or ostriches ... , for which defence against predators may be a critical factor favoring NIM" (p. 279). If the small groups found among most FT primates have in fact evolved for predator detection rather than territory defence, FT species do represent such cases and non-kin membership is consistent with Wrangham's model. The FT-NIM-diet relationship can be tested: I have considered grey langurs (P. entellus) and howler monkeys (A. palliata and A. seniculus) to be FT species, but in all three species females participate in agonistic intergroup encounters and are hostile toward non-group females who are consequently excluded from resource patches (Ripley 1967, Hrdy 1977, Jones 1980a, Sekulic 1982a, b, Crockett 1984); all thus appear to be interference mutualists. For mantled howlers, at least, female transfer is well documented. Either female transfer does not result in an "evolutionarily significant" number of mixed-lineage troops, or interference mutualism does not necessarily favor kin-based groups. Factors other than kinship may influence partner choice even in interference mutualists (Wrangham 1982); one goal of this review is to stimulate research into the nature and generality of such other factors.

"Other factors" may promote the formation of non-kin-based groups, but individuals in such groups may have at least one close relative in the group (e.g., 2 sisters with 2 unrelated females). J. Altmann et al. (1977) point out that kin selection should be more readily observable and identifiable in groups composed of both kin and non-kin than in those composed solely of kin, and it is therefore not at all clear exactly how observed behavioral differences between FT and NFT species should reflect the operation of kin selection in different social environments. It is clear that systematic comparisons of FT with NFT species should greatly improve our understanding of the relative importance of kin selection in social evolution.


If, as argued above, FT and NFT species differ significantly in the kinship structure of social units, we should expect systematic behavioral differences between the two clusters of species. Failure to detect them would imply that either our descriptions of behavior have not adequately distinguished the nepotism we assume is present among relatives from the competition we assume must be prevalent among nonrelatives, or many behaviors we have labelled "nepotistic" in macaques and baboons actually represent a simple preference for the familiar and predictable, regardless of degrees of relatedness (preference for the familiar: Marler 1976, Kummer 1978; see also Washburn and Hamburg (1965), Bernstein and Gordon (1974), Green and Marler (1979), and especially Myers (1983)).

Hamilton (1964) revolutionized behavioral biology with the concept of inclusive fitness. At about the same time, primatologists were beginning to recognize the importance of matrilineal relatedness in macaques and, somewhat later, baboons (see Kurland 1980, Richard and Schulman 1982) and this combination of observation and theory gave rise to the prevailing view of stable mammalian groups as being based on female kinship ties. Observed exceptions such as zebras (Klingel 1972), spearnose bats (McCracken and Bradbury 1977), male lions (Packer and Pusey 1982), dwarf mongoose (Rood 1983), and coatis (Russell 1983) are all too often considered only exceptional cases (see also Ligon and Ligon 1983 for non-kin communal breeding in birds). Furthermore, most studies of nepotism have compared behavior towards "kin" with behavior towards "non-kin" (e.g., Silk 1982); attempts to correlate degrees of nepotism with values of r have mostly found strong kinship effects when r >= 0.2 and very little, if any, discrimination in the range 0.0 < r =< 0.2 (e.g., Kurland 1977, Kaplan 1978, Sherman 1981, Kareem and Barnard 1982; Massey 1977 emphasizes the difference between the 0.25 and 0.125 classes of relatives but does not compare the 0.125 class with the 0.0 class). S. Altmann (1979), Rubenstein and Wrangham (1980), and Sherman (1981) discuss possible theoretical and demographic explanations for this failure to find much nepotism in lower ranges of r. Although not conclusive, the evidence summarized in this review suggests that while kin selection may be a very powerful force among close relatives (r >= 0.2), for many species it may be relatively weak or even negligible between more distant ones (r =< 0.2). Regardless of the implications for kin selection per se, this evidence indicates that mutualisitic social groups which may be stable for periods of several years are not necessarily kin-based, and the widespread occurrence of female transfer s uggests that Jolly et al.'s (1982) characterization of Propithecus verreauxi groups as "loosely bound aggregations of individuals which may have little long-term core of kin" may apply to many other social animals as well.



This paper is the result of my getting carried away on a paragraph in a paper written with Rauf Ali on the tenuous relationship between dispersal and inbreeding avoidance. I thank Rauf for many discussions on the topic of female transfer, starting during a visit to his field site at Mundanthurai, Tamil Nadu, where he has watched female bonnet macaques switch groups and where he showed me a number of extragroup female Nilgiri langurs. A number of people responded generously to my first chart and to many questions about female transfer; I am especially grateful to the following for their suggestions and observations: Elizabeth Bennett, Glynn Davies, Robin Dunbar, Kenneth Glander, Sandy Harcourt, Sheila Hunt Curtin, Charles Janson, Hans Kummer, Hartmut Loch, Toshisada Nishida, Dana Olson, R. S. Pirta, John Robinson, Ranka Sekulic, Yukimaru Sugiyama, Marc van Roosmalen, Christian Vogel, and Kathy Wolf. The paper also profitted greatly from discussions with Janice Chism, Mark Leighton, Deborah Manzolillo, Dana Olson, Rudi Rudran, Joan Silk, Karen Strier, Kathy Wolf, and Richard Wrangham, and especially from critical readings of various drafts by Sarah Blaffer Hrdy, Carolyn Crockett, Clara Jones, Mark Leighton, Barb Smuts and several reviewers. Finally, I thank my advisor, Irven DeVore, for not questioning the months spent on a topic rather distantly related to my (original) thesis, and Andrew Hill for his unfailing encouragement. Fieldwork in India was supported by NSF BNS-7923014 and by NSF BNS-7908267 to D. B. Hrdy.


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