Primate mating systems kin associations and cooperative behavior Evidence for kin recognition.код для вставкиСкачать
YEARBOOK OF PHYSICAL ANTHROPOLOGY 27:99-134 (1984) Primate Mating Systems, Kin Associations, and Cooperative Behavior: Evidence for Kin Recognition? SARAH GOUZOULES Rockefeller University Field Research Center, Millbrook, New York 12545 KEY WORDS Nepotism Kin recognition, Primates, Recognition mechanisms, ABSTRACT The degree to which cooperative behavior is kin-correlated in different primate species is reviewed. The mechanisms whereby individuals might recognize related conspecifics are also considered. Different mating systems, in conjunction with dispersal behavior, are hypothesized to produce particular patterns of kin association in primate groups. These patterns determine what classes of kin are likely to be distinguished, as well as which mechanisms of recognition would be predicted. Association or familiarity during development is concluded to be the most important mechanism of kin discrimination in the primates. Whether or not female sociality evolved principally through the mechanism of kin selection (see for example, Vehrencamp, 1979; Wittenberger, 1980),it is nevertheless well documented that, in many mammalian groups, female social interactions are predominately kin-structured. Clearly, under many ecological conditions favoring group-living, there are concomitant advantages to behaving cooperatively (or “nepotistically”) toward close relatives. Furthermore, as first noted by Hamilton (19641, mechanisms permitting the discrimination of related conspecifics should evolve where it is advantageous to favor kin. A growing number of studies have focused on “preferential” behavior toward kin and the mechanisms of kin discrimination or recognition in animals as diverse as sweat bees, wasps, and tadpoles, on one hand, and ground squirrels, mice, and macaques on the other. Although it was previously thought that most cases of kin recognition could be attributed simply to associative familiarity among individuals likely to be relatives (see Bekoff, 1981; Michener, 19831, the results of several recent studies suggest that more complex (higher-order) explanations for kin-recognition may be necessary in some species (see Holmes and Sherman, 1983). For a t least 25 years, female kinship has been widely viewed as one of the most important “organizing principles” in the distribution of social behavior in a number of primate species (Kawai, 1965; Kawamura, 1965; Hinde, 1976a,b; Seyfarth et al., 1978). Perhaps because of the general acceptance of this view, studies which have actually examined the abilities of primates to discriminate kin have lagged far behind those on other taxa. However, there does exist a large body of information on demographic events and life-history patterns for many primate species. To a lesser extent, information is also available on “kin-correlated’ behavior for those species that have been studied over several generations (most notably some Old World monkeys, e.g., the rhesus and Japanese macaque, and one of the great apes, the chimpanzee). The available evidence for kin-correlated behavior in nonhuman primates is subsequently related to recent theories of the probable selective pressures for, and mechanisms of, kin recognition. In the following sections, (1)the major Sarah Gouzoules’s current address is Yerkes Regional Primate Research Center Field Station, Lawrenceville, GA 30245. 0 1984 Alan R. Liss, Inc 100 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 27, 1984 findings of studies of kin recognition in some nonprimate species are reviewed, noting especially the mechanisms of recognition, (2) primate species are classified according to dispersal patterns and mating systems which, it is hypothesized, affect the probability that particular classes of kin will coexist, (3) the evidence for kincorrelated behavior in different species is discussed, and (4) the evidence provided by a few recent laboratory studies for possible “innate” recognition of certain classes of kin in primates is considered. PATTERNS AND MECHANISMS OF KIN RECOGNITION IN NONPRIMATE SPECIES Several recent reviews of kin recognition’ are available (Bekoff, 1981; Blaustein, 1983; Holmes and Sherman, 1982,1983; Lacy and Sherman, 1983; Michener, 1983). Field and laboratory studies have demonstrated that the ability to discriminate unfamiliar siblings and nestmates from unrelated, unfamiliar conspecifics apparently exists in a wide variety of species: sweat bees, Lasioglossum zephyrum (Buckle and Greenberg, 1981, Greenberg, 1979);honeybees Apis mellifera (Breed, 1981,1983; Getz and Smith, 1983);social wasps, Polistes fuscatus (Pfennig et al., 1983;Ross and Gamboa, 1981); American toads, Bufo americanus (Waldman, 1981); Cascade frogs, Rana cascadae (Blaustein and O’Hara, 1981, 1982; O’Hara and Blaustein, 1981); spiny mice, Acomys chirinus (Porter and Wyrick, 1979; Porter et al., 1978, 1983); deermice, Paramyscus leucopus (Grau, 1982);and several species of ground squirrels: Arctic ground squirrels, Spermophilus parryii (Holmes and Sherman, 1982; see also McLean, 1982);Belding’s ground squirrels, S. beldingi (Holmes and Sherman, 1982; Sherman, 1980, 1981); and Richardson’s ground squirrels, S. richardsonii (Davis, 1982). In many studies, particular attention has been focused on modeling the mechanism(s) likely to facilitate discrimination of kin (Beecher, 1982; Blaustein, 1983; Lacy and Sherman, 1983).Most authors (e.g., Bekoff, 1981; Blaustein, 1983; Holmes and Sherman, 1982; Sherman, 1980; see also Hamilton, 1964) have discussed four possible, but not mutually exclusive, mechanisms of kin recognition: (1) spatial distribution; (2) familiarity through (often developmental) association; (3) “phenotypic matching”; and (4) “recognition alleles.” Blaustein (1983) notes that most theoretical discussions of kin recognition have emphasized the mechanisms of phenotypic matching and recognition alleles (see Blaustein, 1983; also Lacy and Sherman, 1983, for a discussion of the debate over these mechanisms). Beecher (1982) points out that these two mechanisms have sometimes been regarded as constituting “innate” recognition (i.e., not learned). However, while reliable contextual information may not be available in the process of phenotypic matching, a “learned” component often is (e.g., a n odor in sweat bees (Kukuk et al., 1977) or a song in pinon jays, Gymnorhinus cyanocephalus (McArthur, 1982)).Bekoff (1981) and Holmes and Sherman (1982) have pointed out that the consequences of kin discrimination, regardless of the mechanisms of recognition, are likely to be significant. In other words, the evolution of nepotism is probably not evolutionarily constrained by particular cognitive or sensory abilities of discrimination; rather, sensory capacities allowing kin recognition evolve to facilitate nepotism and prevent its misdirection (Sherman, 1980). The most widespread and important mechanism for sibling recognition in mammalian species appears to be familiarity through association (Bekoff, 1981; Michener, 1983; Sherman, 1980). In several studies the supposition that familiarity is the mechanism of recognition is supported by the fact that “errors” in the discrimination of genetic relatives apparently occur naturally, though at low rates. For example, in both Belding’s and Richardson’s ground squirrels, cues acquired during rearing, when young share burrows, are apparently the primary basis for subsequent “kin” identification. Should the young accidently wander into the burrows of nonrelatives ‘Following Lacy and Sherman (1983) the terms “recognition” and “discrimination” will be used interchangeably. Note, however, that “recognition” does not imply the ability to discern exact degree of genetic relatedness. Gouzoules] PRIMATE KIN RECOGNITION 101 prior to weaning, a situation that involved some 3% of all juveniles observed over a 2-year study period in Belding’s ground squirrels (Sherman, 1980), they are subsequently treated and behave as if their new littermates were kin (Michener, 1983; Sherman, 1980). Furthermore, these “displaced” individuals treat their true kin as if they were unrelated individuals (Sherman, 1980). These natural “mistakes” provided the impetus for a series of field experiments in which a large number of unweaned young were exchanged between burrows and their subsequent behavior observed (Holmes and Sherman, 1982).Association prior to weaning was implicated as the most important mechanism for dam-offspring and sibling recognition. However, in the case of ground squirrels, association during development is probably not the sole mechanism involved in kin recognition. In both Arctic and Belding’s ground squirrels, there is field and laboratory evidence of discrimination between maternal half-sibs and full-sibs, as well as evidence of discrimination between nonlittermate sibs and non-kin (Holmes and Sherman, 1982; see also Davis, 1982, for Richardson’s ground squirrels; and Grau, 1982, for deermice). These findings from studies of ground squirrels point to a n issue that is potentially important when primate kin-directed behavior is considered, i.e., despite the apparently unarguable importance of developmental association in the patterning of cooperative behavior, especially among females in certain primate groups, there may also be more subtle discrimination of kin in the absence of such association. Discussions of kin recognition in most nonprimate species center upon parentoffspring and sibling recognition. In the nonprimate species studied to date, there is little evidence for recognition of kin beyond these categories of relatedness. Sherman (1980, 1981; see also O’Hara and Blaustein, 1981) has discussed in detail how demographic events, particularly dispersal and mortality, are likely to affect the extent to which nepotism will occur. Sherman’s argument is that nepotism is unlikely to be expressed among classes of relatives that encounter one another infrequently due to the action of extrinsic selective factors affecting mortality and dispersal. Even when classes of kin that usually do not co-occur encounter one another, Sherman predicts that they will not treat one another as kin. The evolution of nepotistic behavior as well as the mechanisms facilitating recognition of kin, therefore, depend upon both what is “reproductively ideal” (relatedness) and what is “socially possible” (demographic coexistence) (Sherman, 1981). For example, although nine different categories of matrilineal relatives co-occur at least occasionally in Sherman’s population of Belding’s ground squirrels, preferential behavior extended through only a few of the closer categories. An analysis of the population’s demographic patterns revealed that close relatives were more likely to be alive simultaneously, to “co-occur,” than distant kin (Sherman, 1981). Thus, the “historical infrequency” of interactions with distant relatives may have been the most important factor in limiting nepotism (Sherman, 1980). Interestingly, Sherman (1980) speculated that in long-lived, highly social species, such as many primates, it is possible that more distant kin have had a greater historical potential for cooccurrence and thus may be recognized. In contrast, Altmann and Altmann (1980) have suggested that only with the population growth caused by the recent artificial provisioning of some primate groups have more distant kin been generally available for interaction. This point will be discussed in more detail below. A similar and related argument, i.e., demographic coexistence, has been suggested to account for patterns of recognition between males and putative offspring in sciurids (Armitage and Johns, 1982; Hoogland, 1982, 1983; McLean, 1983; see Michener, 1983, for a review). Variables such as dispersal, territoriality, and reproductive behaviors, including mating system, apparently all influence the extent to which nepotistic behavior has evolved in male sciurids (Armitage and Johns, 1982; Michener, 1983). The evidence seems to implicate simply spatial association during a critical period as the principal mechanism in the evolution of male nepotistic behavior (see also Labov, 1982). Where males continue to maintain territories subsequent to the breeding season and where their (probable) young are born and mature in burrows on those territories, males are more likely to perform nepotistic acts, such 102 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 27, 1984 as alarm calling or territorial defense, e.g., Arctic ground squirrels, yellow-bellied marmots (Marmota flauiuentris), and hoary marmots (M. caligata) (Barash, 1975; Armitage and Johns, 1982; McLean, 1983). Male black-tail prairie dogs (Cynomys ludouicianis) also alarm-call when resident in their natal coteries in the presence of nondescendant kin (Hoogland, 1983). In summary, studies of the sciurids have revealed a number of factors that appear to influence the expression of nepotism and the probable mechanisms of kin recognition. These include demographic events such as dispersal and mortality, mating system, and other reproductive variables. Such factors both limit the number, kinds, and categories of kin available for interaction and may also dictate selection for the particular mechanism of recognition. Therefore, a consideration of demographic and social variables seems a logical first step in the examination of primate kin recognition. PRIMATE MATING SYSTEMS AND THE STRUCTURE OF KINSHIP A number of models for the evolution of mating systems in birds and mammals have been presented in recent years (Bradbury and Vehrencamp, 1977; Emlen and Oring, 1977; Wittenberger, 1979). Several authors have discussed, in particular, the influence of patterns of female sociality on the evolution of mating systems (Stacey, 1982; Vehrencamp, 1979; Wittenberger, 1980; Wrangham, 19801.’ While it may not be necessary to invoke kin selection as the principal mechanism of the evolution of female sociality (e.g., Wittenberger, 19801, it is clear that, with the establishment of female groups and female philopatry, kin selection is likely to be of considerable importance in structuring behavior. Although Wittenberger (1980; see also Wrangham, 1980)has hypothesized that male reproductive strategies may be constrained by the evolution of female sociality, male mating patterns, in turn, should have an important effect on the structure of kinship within female groups. Several hypotheses about the configuration of female kinship in primate species exhibiting different mating systems are subsequently offered. In general, mating systems in the primates do not co-vary with phylogeny; species exhibiting monogamy, polygyny, and promiscuity3 can be found among both the prosimians and the apes. Monogamy in primates is rare; by far the majority of species are polygamous: either polygynous or promiscuous. Within polygamous species, however, considerable variation occurs with respect to several important reproductive parameters as well as in gross group structure and individual behavior. Taken together these variables may be critical for determining characteristic patterns of kin association. Table 1 presents a classification of primate species according to mating system and a number of related reproductive and social variables. Some species appear under more than one heading because it is known that in different areas of their range and/or under diverse environmental conditions they exhibit different social structures. In considering each of the broad categories of primate mating systems and associated social organizations, the objective is to describe (where it is known) and to speculate upon (where it is not known) the relevant patterns of lifetime kin association likely to result from these systems. %Several attempts have also been made to correlate variation in primate social systems with ecological variables (e.g., Clutton-Brock, 1974; Clutton-Brock and Harvey, 1977, 1978; Crook, 1970; Crook and Gartlan, 1966; Eisenberg et al , 1972; Wrangham, 1980). Richard and Schulman (1982) recently reviewed papers that have discussed the evolution, including both selective pressures and mechanisms, of different primate social organizations. The present treatment is concerned less with the extrinsic factors that have selected for species-specific demographic and social patterns, and more particularly with how these latter patterns might themselves influence or “predict” the evolution of different mechanisms for the discrimination of kin. It is important to note, however, that ultimately, complex and interacting environmental constraints such a s predation and resource distribution probably underlie the fundamental social determinants (territoriality, group size, dispersaliphilopatry) of both social organization and kin structure in a population. “For a detailed description of mammalian mating systems, see above references. Here mating systems are distinguished by the number of breeding adults typically present in groups of a given species. Monogamous and polygynous groups are both characterized by the presence of a single breeding male. They are distinguished by the number of breeding females, with monogamous groups containing a single breeding female and polygynous groups from two to several females. Similarly, both polygynous and promiscuous groups contain several adult females and are distinguished by the number of breeding males, with promiscuous groups typically containing several sexually mature breeding males. Female and Male Female and Male Family groups Dispersing sex Solitary Population structure Monogamy Polygyny/ Promiscuity Mating system Not applicable Yes Yes Yes Yes Yes No No No True breeding seasonality? (synchrony) Lemur mongoz (mongoose lemur) Hylobates klossii (Kloss’s gibbon) Symphalangus syndactylus (siamang) Callicebus moloch (dusky titi) Callicebus torquatus (yellow-handed titi) Callitrix jaccus (common marmoset) Saguinus oedipus (cotton-top tamarin) Leontopithecus rosalia (golden lion marmoset) Aotus triuirgatus (night monkey) Indri indri (indri) Galago senegalensis (lesser bushbaby) Peridictus potto (potto) Microcehus murinus (lesser mouse lemur) Lepilemur mustelinus (sportive lemur) Cercopithecus neglectus (deBrazza’s monkey) Nasalis concolor (proboscis monkey) Hylobates lar (white-handed gibbon) Pongo pygmaeus (orangutan) Galago demidouii (Demidoff s bushbaby) Galago alleni (Allen’s bushbaby) Galago crassicaudatus (thick-tailed bushbaby) Representative species TABLE 1. Primate mating systems and dispersal patterns Budnitz and Dainis (19751, Pollock (1979) Tattersall (19761, Harrington (1978) Moynihan (1976) Dawson (1977), Neyman (1977) Kleiman (1977, 1979) Kinzey (1977), Kinzey et al. (1977) Epple (19751, Box (1977) Moynihan (1976) Ellefson (1968),Roonwal and Mohnot (1977) Tenaza (1975, 19761, Tilson (1981) Chivers (1974, 1976) Charles-Dominique and Hladik (1971) Gautier-Hion and Gautier (1978) Tilson (1977) Charles-Dominique (1975, 1977) Martin (1972, 1973) MacKinnon (1979), Rodman (1979) Charles-Dominique (1977) Charles-Dominique (1977) Bearder and Doyle (19741, Clark (1978) Bearder and Doyle (1974) References 6 W 2 2 3 Q 0 Q z h *2 3Y 25 i 5 g 2 Female and Male Male One-male units (harems) Mult,imale, Multifemale One-male units (harems) Promiscuity Polymny Polywny Male > Female (?) One-male units wiin multimale DOUP Female > Male (?) Male Mating system Dispersing sex Population structure Cercopithecus campbelli lowei (Lowe’sguenon) Alouatta seniculus (red howler monkey) No Macaca radiata (bonnet macaque) Macaca sinica (toque macaque) Yes Yes Macaca mulatta (rhesus macaque) Yes Yes Yes (?) No Gorilla gorilla (gorilla) Macaca sylvanus barbary macaque) Macaca fuscata (Japanese macaque) Cercopithecus mitis (blue monkey) No No Cercopithecus ascanius (red-tail monkey) Presbytis entellus (Hanuman langur) Presbytis guereza black and white colobus) Presbytis .johnit (Nilgiri langur) Presbytis senex (purple-faced langur) Theropithecus gelada (gelada baboon) Erythrocebus patas (patas monkey) Papio hamadryas (hamadryas baboon) Representative species No No No No No Yes No No True breeding seasonality? (synchrony) TABLE 1. Primate mating systems and dispersal patterns (continued) Lindburg (1971), Boelkins and Wilson (1972) Drickamer and Vessey (1973) Sugiyama (19711,Click (1980) Dittus (1977, 1980) Burton (1972),Taub (1980) Kawai et al. (1967 ), Norikishi and Koyama (1975) Harcourt (1978, 1979) Rudran (19791, Sekulic (1982) Roonwal and Mohnot (1977), Rudran (1973) Struhsaker (1977). Struhsaker and Leland (1979) Struhsaker and Leland (19791, Butynski (1982) Bourliere et al. (1970) Poirier (1970a,b) Sugiyama (19671, Hrdy (1977) Clutton-Brock (1975), Oates (1977) Hall (1965),Struhsaker and Gartlan (1970) Dunbar (1980) Kummer (1968),Sigg et al. (1982) References rp zm -a h3 $ .$ c) 80 b 20 5 b w b 2 % a 3 k 0 0 z i> c +A Multimale, Multifemale Female Promiscuity Lemur catta (ring-tailed lemur) Lemur macaco (black lemur) Miopithecus talapoin (talapoin monkey) Saimiri sciureus (squirrel monkey) Macaca nemestrina (pigtail macaque) Macaca arctoides (stumptail macaque) Papio cynocephalus (yellow baboon) Papio ursinus (chacma baboon) Papio anubis (olive baboon) Cercopithecus aethiops (vervet monkey) Macaca nigra (Celebes black ape) Cercocebus atys (sooty mangabey) Cercocebus albigena (grey-cheeked mangabey) Alouatta seniculus (red howler monkey) Alouatta palliata (mantled howler monkey) Ateles geoffroyi (black-handed spider monkey) Presbytis entellus (hanuman langur) Presbytis cristatus (silver-leafmonkey) Colobus badius (red colobus monkey) Pan troglodytes (chimpanzee) Yes No No No No No No No No No No No No No No No No Yes Yes Yes Macaca fascicularis (crab-eating macaque) Yes Fleagle (1977) Struhsaker (19751, Marsh (1979) Nishida (19791, Goodall (1983), Wrangham (1979) Eisenberg and Kuehn (19661, Eisenberg (1976) Sugiyama (1967),Jay Furuya (1965)(1962),Wolf and Tokuda et al. (19681, Hadidian and Bernstein (1979) Bertrand (19691, Hadidian and Bernstein (1979) Altmann and Altmann (19701, Altmann et al. (1979) Cheney and Seyfarth (19771, Seyfarth (1978) Ransom and Rowell (1972), Packer (1979a,b) Struhsaker (1967). Cheney and Seyfarth (1983), Whitten (1983) Hadidian and Bernstein (1979) Hadidian and Bernstein (1979) Chalmers (19681, Struhsaker and Leland (1979) Neville (1972),Rudran (1979) Glander (1980) Gautier-Hion (19711, Rowell (1973) Moynihan (1976) Petter (1965), Jolly (1966) Jolly (1966, 1967) Furuya (19651, Hadidian Bernstein, and (1979) K 2 E 5 La 1 r 8 G E 9 106 YEARBOOK OF PHYSICAL ANTHROPOLOGY IVol. 27, 1984 Dispersal and inbreeding in primates Several authors have pointed out that, with few exceptions, female primates are generally “philopatric,” i.e., they remain in either their natal home range andor group throughout their lives (Greenwood, 1980; Harcourt, 1978; Waser and Jones, 1983). Male primates, on the other hand, generally disperse from natal areas a t sexual maturity and may continue to disperse (transfer between groups) throughout their lives. These demographic patterns of female philopatry and male dispersal in primates, as well as in other mammals, have generally been attributed to selection for the avoidance of inbreeding (see Greenwood, 1980). Although some recent data on migration in a few species of primates suggest that some level of consanguineous breeding occurs (see Cheney and Seyfarth, 1983, for a review), it is nevertheless clear that inbreeding is avoided chiefly by male migration rather than by complex mechanisms of recognition of nonmaternal kin (see Smith, 1982a,b; also Packer, 1979a; Pusey, 1980).Thus, as Holmes and Sherman (1982) note, differential dispersal is one mechanism for avoiding, and thereby, “recognizing,” kin. Solitary primates So-called “solitary” primates exhibit either polygynous or promiscuous (“overlap” promiscuity, Wittenberger, 1979) mating systems. These are considered separately from the group-living primates because patterns of interaction among conspecifics in solitary species are clearly fundamentally different from those in group-living ones. As Waser and Jones (1983)have most recently pointed out, “solitary” refers to animals that are usually found alone, rather than to the absolute absence of social interactions. Individuals of solitary species in a population may indeed recognize one another and associate in certain ways and at certain times. Waser and Jones (1983) note that in many philopatric solitary species parental influence on the reproductive success of offspring may even continue beyond the time of sexual maturity. Female home ranges in most solitary primates overlap considerably while those of males are usually larger, exclusive, and encompass one to several females’ ranges (e.g., bushbabies, Galago sp., Charles-Dominique, 1977; orangutans, Pongo pygmueus, Horr, 1977; Rodman, 1973). Mature males are generally intolerant of one another, but females may be tolerant of neighboring females. The length of time mature males occupy territories and mate with local females is unknown. Thus, the extent of co-occurrencebetween males and their offspring is unclear for most solitary species. At sexual maturity, however, males generally disperse from the natal area while females, though they establish their own ranges, are essentially philopatric. On this basis, a number of authors have speculated that females occupying adjacent home ranges in a population are likely to be related, often mothers and daughters or sisters (Charles-Dominique, 1977; Clark, 1978; Horr, 1977). The kin structure in populations of most solitary primate species is predicted to be a dispersed, matrilineal one, based on a pattern of male dispersal and female philopatry. Thus, the following might be expected: (1) possible recognition and discrimination of close maternal relatives in a population, and (2) little or no male investment in offspring. Groupliving primates Monogamous species Few primate species exhibit monogamy (Table 1).Several reviews of the evolution of avian andor mammalian mating systems have considered the conditions under which monogamy might be predicted to occur (Emlen and Oring, 1977; Kleiman, 1977; Orians, 1969; Ralls, 1977; Wittenberger, 1979; Wittenberger and Tilson, 1980). Most discussions have centered on the necessity and extent of male parental invest- Gouzoules] PRIMATE KIN RECOGNITION 107 ment to the survival of young. Social units in monogamous species are typically composed of a n adult male and female, apparently bonded for life, and their immature offspring of various ages. In some New World monogamous species (Callitrichidae: the marmosets and tamarins), groups tend to be larger because offspring may remain in the group after maturation (”extended family groups”) (Epple, 1975; Kleiman, 1977; Moynihan, 1976), although only one (dominant) adult pair typically breeds in these species. Female marmosets and tamarins are usually very aggressive toward other females and may form dominance hierarchies in larger groups (Dawson, 1977; Epple, 1975). It has been recently suggested that tamarin groups may be more fluid than previously thought. Nonbreeding (subordinate) individuals, especially juveniles, may frequently transfer between groups in a population (Dawson, 1977; Neyman, 1977).The kin structure of these tamarin groups is not yet known. New World monkeys of the genera Callicebus (titi’s) and Aotus (night monkeys), as well as the Old World monogamous species (gibbon, Hylobates sp.; siamang, Symphalangus sp.; Mentawai leaf monkey, Presbytis potenziana), apparently do not form extended-family groups. Instead, young of both sexes disperse from the family group at maturity. In these monogamous species, adults generally become intolerant of like-sexed offspring as the latter approach sexual maturity. Offspring begin to become peripheral and eventually cease to associate with the parental group. Subadult males of most gibbon and siamang species are usually forced away from the group a t maturity but female offspring may not be peripheralized to the same extent, and perhaps move directly from the parental territory to that of a new mate (see Tilson, 1981, for a review; also Chivers, 1974).It is not yet known whether a similar process occurs in New World monogamous species. Recent data have suggested that parents may “bequeath” part of their range to maturing offspring (Chivers and Raemakers, 1980; Tenaza, 1975; Tilson, 1981) or actively aid young in acquiring adjoining territories (Tilson, 1981). In terms of kin association, monogamous groups are clearly unique among primate species: (1) the offspring of a monogamously mated pair are putatively full siblings, so the average degree of relatedness within the group will be high; ( 2 ) because assurance of paternity to males is strong, recognition of and investment in offspring by males is likely; and (3) to the extent that offspring occupy nearby home ranges, some degree of kin discrimination may extend outside the family group. Polygynous species Wittenberger (1979) has noted that, despite a n abundance of theories, it is still unclear what environmental factors would favor the evolution of polygynous mating systems. In the primates, the issue is complicated by the fact that social structure among polygynous species varies considerably. Polygynous species are characterized by social units containing one breeding male and several adult females with dependent offspring. However, within this definition, the social organization of groups varies from those species in which only one sexually mature male is ever present in a group (e.g., blue monkey, Cercopithecus mitis; patas monkey, Erythrocebus patas; purple-faced leaf monkey, Presbytis senex) to those in which mature males of different ages (and variable status) may coexist (so called “age-graded structure,” e.g., spider monkey, Ateles geoffroyi; gorilla, Gorilla gorilla; silvered leaf monkey, Presbytis cristatus). Presumably only the oldest, leader male has access to reproductive females in age-graded groups, although the certainty of paternity should not be as great as when only one sexually mature male is present in the group. Other polygynous species, such as gelada (Theropithecus gelada) and hamadryas (Papi0 hamadryas) baboons, fall somewhere in between these two patterns (Table 1). In the latter species, the basic group structure is a unit composed of only one adult male and several females. Males of such units are generally highly intolerant of one 108 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 27, 1984 another and female interactions are restricted to within the group. However, leader males do allow so-called “follower” males to associate with the unit and these males often interact (carry, groom) with the unit’s young. Also, one-male units coalesce at times into very large bands or herds. Males in polygynous species are often depicted as more intolerant of one another than are males in promiscuous species. However, male intolerance appears to be somewhat context-dependent. In some species (e.g., red howler monkeys, Alouatta seniculus; Hanuman langurs, P entellus), group structure varies between one-male and multimale groups, from population to population, or even within a single population. Also in some species (e.g., Hanuman langurs, gelada baboons), males lacking females band together into “bachelor” or “all-male” groups. All but one polygynous primate species (the gorilla) follow the common pattern of male dispersal and female philopatry, although the patterns of dispersal in gelada and hamadryas baboons also constitute special cases and are considered below. Thus in the majority of polygynous species, females usually remain in their natal group throughout life. Males first emigrate from natal groups a t or near sexual maturity, and fully adult group males may also emigrate, or may be forced out by encounters with other males. Struhsaker and Leland (1979) have summarized the male replacement rates for different polygynous species in the Kibale forest. Rates ranged from once in every 22.5 months for redtail monkeys (Cercopithecus ascanius) to once in every 36-48 months for black and white colobus monkeys (Colobus guereza). Male membership in groups is, therefore, quite fluid compared to that of females. With respect to the distribution of kin in polygynous species, the contrasting demographic profiles of males and females suggest: (1)Females should have networks of matrilineal kin within the group. The extent of the network as well as its exact composition depends on mortality rates for each agelsex class. In general, female anthropoids are long-lived, so the potential for relatively extensive lineal and lateral matrilineal kin networks should exist, as Sherman (1980) suggests. (2) Depending upon the length of male tenure, female kinship through paternal lines (patrilineal kin) may also be well developed in polygynous groups. That is, both paternal half-siblings, as well as full-siblings, may be distributed in fairly high proportions with respect to maternal half-siblings. Though the exact configuration of genetic relatedness amongst females depends upon male tenure, polygyny, in combination with female philopatry, should produce a group with a comparatively high average degree of relatedness. (3) In contrast to female kin association patterns, males will usually not have access to either the maternal or paternal kin networks in their natal groups after sexual maturity. Males should often be coresident with their offspring, and might be expected in invest in them. Female emigration in polygynous species (Table I).-Both male and female gorillas emigrate from their natal groups. Both sexes also subsequently transfer between groups; however, the rate of female transfer is considerably higher than that of males (Harcourt, 1978; Harcourt et al., 1976).Harcourt (1978)notes that once mature males have become established in a group they rarely transfer, whereas adult females may continue to do so. In fact the formation of new groups usually occurs when lone males or newly formed units attract females out of established groups (see Harcourt, 1978, for more details). Though some individuals in gorilla groups, especially leader males and females with several living offspring, are rather unlikely to transfer, the net effect of considerable group shifting by females is to diminish the average degree of relatedness in the group as a whole. Thus, in comparison to other polygynous species: (1) the matrilineal kin network among adult female gorillas should be poorly developed; and (2) gorilla leader males, on the other hand, are likely to co-occur with their young and some male offspring may remain in and “inherit” groups from their father (Harcourt and Stewart, 1981). Gouzoules] PRIMATE KIN RECOGNITION 109 The dynamics of male and female emigration in the polygynous baboons are extremely complex. In hamadryas baboons, females often leave their natal one-male units before maturity in the company of a young adult male (the pair forming a n “initial unit”) (Kummer, 1968; Sigg et al., 1982). Males also leave natal units and either join other young males in a “bachelor group” or become “followers” to onemale units from which they acquire juvenile females. Apparently almost all males eventually form one-male units within their natal “clan.” A clan is defined as a group of one-male units whose leaders are more spatially cohesive and interact more frequently with one another than with other males in the band. Kummer and Abegglen (1978; cited in Sigg et al., 1978) suggest that clans are formed of a n “agegraded hierarchy of obviously related males.” Thus, male hamadryas clans may actually be patrilines. Although females also tend to remain in natal clans, Sigg et al. (1982) note that their movements are constrained by the distribution of males. If there are relatively few males within the natal clan, females may transfer into another clan and apparently are usually not reluctant to do so. Thus, female kinship associations may be fairly weak in comparison to those of males. As adults, females do tend to transfer between units along with females with which they have previously associated, but these females are not necessarily related. Thus, although the exact nature of relatedness in one-male units of hamadryas may be highly variable and complex, a greater degree of relatedness probably exists among males than females within the clan. Patterns of emigration in gelada baboons resemble those of hamadryas in some ways, but differ in others. Again, males leave natal units and either join all male groups or become followers and subsequently acquire females away from one-male units (Dunbar, 1979a; Dunbar and Dunbar, 1975; Mori, 1979; Ohsawa, 1979). There does not appear to be a male clanlike patrilineal structure in geladas. Males may acquire units by fighting other males and/or “pirating” females. Recently Dunbar (1979b; see also Mori, 1979) has emphasized that, contrary to earlier impressions (e.g., Dunbar and Dunbar, 1975),juvenile females may often remain in their natal units. Unlike hamadryas units, those of geladas may consist primarily of matrilines whose members tend to be fairly cohesive, i.e., may transfer together. Male takeovers of entire units, or of matrilines from a unit, may be the most important mechanism of group formation. As yet, however, there is no long-term genealogical information to substantiate these hypotheses. Nevertheless, if these notions prove to be generally true, then despite superficial similarities, kin association patterns for both sexes may be fundamentally different in hamadryas and gelada baboons. In summary, the majority of polygynous primate species are characterized by a pattern of long-term female association with kin through both maternal and paternal lines in the natal group. This pattern might also be typical of the demography of gelada one-male units. In contrast, females in gorilla and hamadryas baboon groups are probably much less closely related. Male hamadryas, and to a lesser extent male gorillas, may live in close association with paternal kin. Males of all polygynous species will co-occur with offspring, to a greater or lesser extent, depending on length of tenure. Paternity assurance during tenure as a group leader should be fairly strong. Promiscuous species Eisenberg et al. (1972) distinguished between uni-male, age-graded, and multimale primate species on the basis of the degree of tolerance manifested among fully adult (similarly aged) males. The greatest degree of intermale tolerance clearly exists in the latter category of group structure. Multimale primate groups generally exhibit promiscuity, although the mating system is often one of “hierarchical promiscuity” (Wittenberger, 1979). As noted above, some species, such as red howlers and Hanuman langurs, can display either uni-male or multimale social structures. In these species, the degree of male tolerance may depend more upon immediate environmentalldemographic conditions than upon the species-specificmating system. 110 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Val. 27, 1984 Primate species that can be categorized as promiscuous vary considerably in terms of group dynamics and social behavior. For instance, while most Old World monkey promiscuous species form relatively cohesive groups, some New World species do not (Moynihan, 1976; see the review of Izawa, 1976).For example, spider monkey social structure has been described as “fission-fusion” (Klein and Klein, 19751, and as more prone to subdivision than are groups of howler monkeys (Alouatta) and capuchins (Cebus) (Eisenberg, 1976; Izawa, 1976; Izawa et al., 1979). The extremely large groups formed by squirrel monkeys (Saimiri sciureus) also frequently subdivide (Baldwin, 1968, 1971). Multimale groups in prosimians (e.g., ringtailed lemurs, Lemur catta) may also be more fluid than those of Old World monkeys, with males typically leaving groups during the mating season (Jolly, 1966).The degree of sexual dimorphism and the relative dominance of males with regard to females also differ considerably among species (e.g., Packer and Pusey, 1979). In terms of patterns of dispersal and philopatry, however, species with promiscuous mating systems closely resemble the majority of polygynous species. That is, males generally emigrate from their natal group a t maturity and they may also subsequently transfer between groups (e.g., baboons, Papio sp., Packer, 1979a,b; Japanese macaques, Macaca fuscata, Norikoshi and Koyama, 1974; Sugiyama, 1976; rhesus macaques, M. mulatta, Boelkins and Wilson, 1972; Meikle and Vessey, 1981; vervet monkeys, Cercopithecus aethiops, Cheney and Seyfarth, 1983). There is now some evidence in at least a few species that males may accompany or follow their male matrilineal relatives into new groups (Cheney and Seyfarth, 1983; Meikle and Vessey, 1981).Females, on the other hand, remain within their natal groups for life, in close association with matrilineally related female kin. Wrangham (1980: see Table 1) has correctly pointed out, however, that in most species where female philopatry has been assumed, females have not actually been observed from birth to “motherhood.” Male and female patterns of dispersal in chimpanzees (Pan troglodytes), red colobus monkeys (Colobus badius), and to a lesser extent, red howlers, and perhaps spider monkeys, differ from this pattern of female philopatry. Two principal consequences of promiscuity (as opposed to polygyny) in conjunction with male dispersal and female philopatry might be predicted: (1) Female relatedness within the group should be predominantly through maternal, rather than paternal, lines because sequential offspring are likely to have different sires. The incidence of full siblings should also be decreased. (2) Although males should still coexist with offspring, membership in the group a t the time of a n infant’s conception will not be, of itself, a reliable indicator of paternity. (3) Because social groups in promiscuous species typically contain several adult males, male migrants may have the opportunity to associate with their (male) relatives if there is simultaneous or sequential transfer into the same social group. However, these male associations are unlikely to be as pervasive or persistent as those of females. These hypothetical effects of a promiscuous mating system on patterns of kin association are likely to be variably expressed, depending upon other important reproductive parameters. Under certain conditions, for example, promiscuous species may actually approximate polygyny: a small group with its few adult males strictly arranged in a dominance hierarchy that determines mating success, pronounced sexual dimorphism, and aseasonally breeding females that provide males with cues to reproductive state (e.g., sexual swellings, vaginal odors, etc.), could all produce a situation of “effective polygyny.” Effective polygyny might be expected to produce patterns of kin association similar to those predicted for typically polygynous species. Altmann (1979) has modeled just such a case of effective polygyny in yellow baboons (l? cynocephalus) and concluded that cohorts of paternal half-siblings could be more numerous than maternal half-siblings under these conditions. Certain typically multimale species (e.g., baboons) would be more likely to “approximate polygyny” than others (e.g., rhesus and Japanese macaques). The single most important variable in limiting the extent to which a multimale group might Gouzoules] PRIMATE KIN RECOGNITION 111 approximate polygyny is probably breeding seasonality. Species which exhibit discrete breeding seasons (see Table 1)are characterized by the simultaneous receptivity or estrus of several to many reproductive females. A single, even high ranking, male may not be able to monopolize or fertilize all estrus females. Data indicating that several different adult males probably father offspring are accumulating for the seasonally breeding macaques (Chapais, 1983; Takahata, 1982). Thus, particularly in seasonally breeding multimale groups, female relatedness through matrilineal lines could be even further accentuated in comparison to relatedness through paternal lines. It has also been suggested that the average degree of relatedness within female matrilines and the genetic distance between matrilines could be increased by “lineage-specific female mate choice” (McMillan, 1979, 1980; Silk and Boyd, 1983). Thus, groups of related females might tend to mate with the same male or with related males. As yet, however, there is no evidence that lineage-specific mating occurs in multimale groups. Female emigration in promiscuous species (Table I).-In the Kibale Forest of Uganda, red colobus monkeys form relatively large multimale groups. Unlike the majority of promiscuous species in which females are lifelong sedentary members of their natal group, red colobus juvenile females emigrate and join other groups (Struhsaker and Leland, 1979). Many adult males, on the other hand, probably remain in their natal group for life, and Struhsaker and Leland (1979) suggest that these males may be closely related (presumably, especially through paternal lines). Mating in red colobus is apparently correlated with dominance status; thus, a cohort of males might be composed predominantly of paternal siblings. Juvenile females who transfer into groups are thought to be unrelated. Marsh (1979) has reported that in another population of red colobus in Kenya along the Tana River, groups typically contain only one or two adult males, and male takeovers of groups are common. This population also differs from that in Uganda in that it is adult females rather than juveniles who emigrate. Thus, in contrast to females of most other promiscuous primate species, red colobus females probably do not live in close association with matrilineally related individuals, and kin association patterns in this species may be fundamentally different from those of other promiscuous species. Red howler monkey females are also apparently more mobile than is generally the case in promiscuous species (Rudran, 1979). Both sexes, including juvenile females, transfer between groups, though the rate of female transfer in this species is probably not as high as that in red colobus monkeys. Nevertheless, female coexistence with matrilineal relatives may not be as prevalent in red howlers as in other multimale species. Similarly, in comparison to that of most promiscuous primate species, chimpanzee social organization is both more fluid and more complicated (see the following for details: Goodall, 1968, 1983; Nishida, 1979; Pusey, 1979, 1980, 1983; Tutin, 1979; Tutin et al., 1983). Chimpanzees do not form closed groups; rather they form “communities” or “unit-groups.” Individuals within the community form temporary associations or parties for traveling, foraging, and resting. There appear to be some differences between populations in the characteristics of these daily groups (Tutin et al., 1983). In terms of patterns of kin association, the most relevant aspect of chimpanzee social structure is that females generally transfer with the occurrence of their first estrus while males remain in their natal communities. Though some young females return to their natal communities, particularly if their mother is alive, others do not (Goodall, 1983; Pusey, 1979, 1980).Thus, chimpanzee communities are composed predominantly of mother-sexually-immature-offspring associations and a number of natal adult males. Chimpanzee males in a community should be related through paternal lines, although subgroups of males (brothers) will also be maternally related (see Goodall, 1983, for a n overview of chimpanzee population dynamics and social organization). Fedigan and Baxter (in press) have recently suggested the possibility of female emigration in spider monkeys, though they caution that the exact nature of female spider monkey relations is not yet known. 112 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 27, 1984 To summarize, although promiscuous primate species vary considerably with respect to a number of important reproductive variables, life-history patterns of males and females in most species indicate that groups are typically composed predominantly of natal females in association with matrilineally related kin. Patrilineal relatives should also co-occur but with less frequency than in polygynous groups. Males sometimes co-occur with offspring but paternity assurance, on the basis of group membership alone, will be weaker than in polygynous species. Adult males of most promiscuous species may coexist to a minor degree with male matrilineal kin. In contrast, chimpanzee males and red colobus males in some populations typically associate for life with male patrilineal and maternal kin. Females of these two species should co-occur only with dependent offspring and perhaps with adult sons. KIN-CORRELATED BEHAVIOR AND POSSIBLE MECHANISMS OF RECOGNITION ‘?Inan area of behavioral biology i n which rigorous assessments of genetic relatedness are absolutely critical, tenuous, forced ex post facto reconstructions of genealogies are (too) frequently being used not only to summarize the results of particular studies, but furthermore, and perhaps in a more injurious way, also to rewrite and reformulate evolutionary theory. ” (Bekoff, 1981: 307-308) The implications of the patterns of kin association hypothesized as resulting from different primate mating systems for the evolution of particular mechanisms of kin discrimination will be considered in this section. To the degree that behavior is kincorrelated in different species, how is the discrimination of kin likely to occur? In most studies of “kin recognition” in nonprimate species, recognition has been defined by some degree of preferential behavior directed differentially among individuals on the basis of genetic relatedness. A key point in these studies is that the degree of genetic relatedness among subjects has usually been known. By contrast, in only a very few studies of behavior in nonhuman primates has complete information on genetic relatedness been available. In some long-studied species (e.g., rhesus and Japanese macaques, chimpanzees) female genealogies have been well documented, but patrilineal relationships have not. More recent studies of genetic differentiation between subgroups of rhesus populations have provided indirect evidence of patterns of individual relatedness in groups (McMillan and Duggleby, 1981; Melnick and Kidd, 1983; Olivier et al., 1981). Finally, a few laboratory studies of either individuals or of groups with unnatural social compositions have provided information on genetic relatedness (Berenstain et al., 1981; Small and Smith, 1981). In general, as noted by Bekoff (1981), theoretical predictions of kin association as well as hypothetical explanations of the observed distribution of behavior, have far exceeded what is actually known of genetic relatedness in primate groups. Unfortunately, this lack of information has sometimes led to a circularity of reasoning in causal explanations of behavior. For instance, several authors have made assumptions about female relatedness on the basis of behavior and subsequently discussed behavior in terms of relatedness (see Bekoff, 1981; Walters, 1981). Hence, in the following section this pitfall is avoided by pointing out whether kinship is actually known or not, as well as by emphasizing studies where kin relations are known. However, some speculations about the probability and mechanisms of kin discrimination in primate groups are also presented on the basis of the hypothetical patterns of kin association outlined above. In studies of nonprimate species, kin preference has frequently been evaluated by spacing patterns. In the sciurids, discrimination has also been measured in the field by rates of agonism, coalitions and alliances, and alarm calling, as well a s by contiguous spatial arrangement. In the lab, agonism and “exploratory” or “amicable” behaviors have been scored. These same behaviors are often used in describing primate kin relationships. Other important distinguishing behaviors include grooming, traveling and feeding together, and alloparenting and infant defense. These behaviors are primarily used to assess the extent of kin-correlated behavior in primate species. Gouzoules] PRIMATE KIN RECOGNITION 113 Solitary species As pointed out in the preceding section, the potential availability of related individuals in species with promiscuous mating systems is roughly equivalent, whether or not a species is solitary or group-living, i.e., a n essentially matrilineal structure based on male dispersal and female philopatry. Despite relatively similar mating systems among solitary primates, the extent to which individuals in a population interact socially probably depends upon other, ecological factors such as diet, predation, locomotory mode, sleeping sites, etc. Because females occupying adjacent ranges in populations of many prosimian solitary species are likely to be related, some degree of tolerance or even amicable behavior amongst these individuals might be expected. The data available, particularly on African bushbabies (reviewed and reported in Charles-Dominique, 1977; Clark, 1978), indicate that female galagos, in fact, often form “groups.” Similar behavior has been reported for the lesser mouse lemur (Microcebus murinus) (Martin, 1973). Though they are typically solitary foragers a t night, females with and without dependent young coalesce into sleeping groups (frequently sharing nestholes) during the day. Other social behaviors, such as reciprocal grooming and play, are also exchanged within these groupings. Even during solitary nocturnal foraging, females frequently travel at relatively close distances to other females. Recently matured daughters may also remain on their mothers’ territory for some time (Charles-Dominique, 1977; see also Clark, 1978).At the same time, however, females of one association are usually antagonist toward those of another (Charles-Dominique, 1977; Clark, 1978). Neither the solitary African lorisines (Potto) nor the solitary orangutan exhibit comparable tendencies to group, despite apparently similar mating and dispersal patterns. Some descriptions of orangutan social behavior have noted that females occasionally travel or feed with other females and/or immatures that are suspected of being relatives, though little social behavior is exchanged during such feeding encounters (Galdikas, 1979; MacKinnon, 1974, 1979; Rodman, 1973, 1979). The relative frequency of reported associations other than the mother-offspring unit varies between studies, and presumably between populations, but all observers agree that orangutans are essentially solitary. In none of the solitary primate species have males been reported to interact with or invest paternal care in offspring. In general, however, populations have not been sufficiently studied to adequately document male ranging behavior and possible association with older offspring over a number of years. Mechanisms of kin discrimination in those species where individuals do interact are likely to be of the “lowest” order; i.e., either spatial association (membership in the local population) or developmental association in cases of mothers and offspring. Although data are clearly too limited a s yet for an accurate assessment, some experimental studies of “group” formation in Demidoff s and Allen’s bushbabies by Charles-Dominique (1977) suggest that actual kinship is not necessarily important in determining membership. According to Charles-Dominique (1977:245): “Apparently, it is not the link of actual parental relationship but the fact of proximity of two females which become accustomed to one another (usually related to birth, of course, under natural conditions) which is responsible for creation of the social bond.” (emphasis mine) Galdikas (1979) similarly noted that the sporadic associations of orangutans did not correspond well to “simple” genealogical relationships. If the members of a population are usually related, then we may expect exchange of social behavior without necessarily expecting actual discrimination of related from nonrelated individuals (for further discussion of this mechanism, see Holmes and Sherman, 1982,1983). 114 YEARBOOK OF PHYSICAL ANTHROPOLOGY IVol. 27, 1984 Groupliving species Monogamous species Not surprisingly, cooperative social behavior is highly developed in monogamous species. However, nepotistic behavior does not necessarily persist throughout individuals’ lifetimes due to the dispersal of young of both sexes and in contrast to the pattern of female philopatry in most other group-living primates. Males of monogamous species generally contribute a greater amount of parental care to offspring than do males of polygamous species. Male parental care in monogamous primates ranges from infant carrying and food sharing (the New World Callitricidae, Brown and Mack, 1978; Kinzey, 1977)to simply territorial defense and perhaps assistance in the acquisition of a territory for a n offspring (the monogamous apes). Male siamangs also carry and groom older infants (Chivers, 1974,1976). Tilson (1981) has cautioned that, despite over 15 years of field observations on gibbons in Southeast Asia, much remains unknown about the social dynamics of reproduction in these species. However, it seems likely that once offspring have left the family group, acquired mates, and established territories, little if any social interaction occurs between groups. On the other hand, Ellefson (1974)noted “friendly relations” among neighboring groups in white-handed gibbons (Hylobates lar), and it is possible these groups were composed of individuals originally from the same family group. Another exception to this general trend may occur upon the death of a parent, when a n offspring of the same sex as the dead partner may return to the group and even mate with its parent (Tilson, 1981). Little, or even hostile, interaction between groups is also characteristic of New World nonextended family monogamous species (Cullicebus).In contrast, it is likely that young marmosets and tamarins continue to associate with families beyond maturity. The degree of cooperative behavior exhibited by these individuals may surpass any found in other primate species. Older offspring in Callitrichid groups usually help carry infants and may share food with their parents (Brown and Mack, 1978; Kleiman, 1979). Even mature offspring may continue to remain in the family group, delaying reproduction, and assisting with the rearing of young full siblings (Kleiman, 1979). This social pattern resembles that reported for several species of birds where older offspring help a t the nest (see Brown, 1978, for a review). Maturing tamarins may also move back and forth between natal and neighboring groups, suggesting that social interactions can extend outside the family group (Dawson, 1977; Neyman, 1977). Genetic relationships between these groups are, as yet, unknown. It was pointed out above that probably the most widespread and important mechanism of kin discrimination in nonprimate mammalian species is direct association during development. Sibling recognition usually occurs as a result of direct association during development or indirect association via a third individual, usually the mother (called “mediated” association by Holmes and Sherman, 1983). Male recognition of offspring probably depends upon prior association, or association in conjunction with copulation, with the mother. Similarly, there appears to be no reason to postulate a recognition mechanism that could operate in the absence of prior association to account for patterns of kin-correlated behavior in monogamous primate species. Membership in the family group is clearly a strong predictor of close genetic relatedness in these species. Also, if related family groups do tend to occupy adjacent territories in some monogamous species, it is likely that the recognition of previous or subsequent offspring as siblings could be a consequence of parental association (“third”-party association). Epple (1975) has described how tamarins separated from family members, sometimes for months, apparently recognize one another and interact affinitively. The fact that incestuous matings sometimes occur in gibbon family groups probably should not be viewed as evidence of a lack of “recognition,” but rather, a s Tilson (1981)suggests, an epiphenomenon of the process of territory transfer to a n offspring after the death of one of its parents. Gouzoules] PRIMATE KIN RECOGNITION 115 “(all)sisters under their skins!” -Rudyard Kipling, “The Ladies” Polygynous species Although relatedness within polygynous groups should not be as high a s that in monogamous groups, it is predicted to be well developed among females through both maternal and paternal lines. Unfortunately, there are as yet no field studies of polygynous groups in which actual genealogical information has been available. Nevertheless, a number of studies have yielded information on the patterning of behavior among females in polygynous species. In general, agonistic interactions among polygynous females have been reported to be far less frequent than among females in many promiscuous species (redtail, blue monkeys, Struhsaker, 1977; Struhsaker and Leland, 1979; patas monkeys, Rowell and Olson, 1983; black and white colobus, Oates, 1977; Nilgiri langurs (Presbytis johnii), Poirier, 1970a; Hanuman langurs, Hrdy and Hrdy, 1976; Jay, 1965; Sugiyama, 1976). Clearly, competition over resources among females in polygynous groups is not absent. Female dominance hierarchies have been described in Hanuman langurs (Hrdy and Hrdy, 1976)and patas monkeys (Loy, 1981; Rowell and Olson, 19831, and females of several species apparently displace one another at feeding sites (Struhsaker and Leland, 1979). However, the nature of female competitive behavior differs strikingly between polygynous and promiscuous species (see McKenna, 1979). For instance, noticeably absent from aggressive behavior in polygynous species are the coalitions that females frequently form against one another in multimale groups (see below). Female coalitions in polygynous groups are generally directed against males (Hrdy and Hrdy, 1976; Struhsaker, 1977) and toward other groups (Struhsaker and Leland, 19791, and in the case of red howler monkeys, toward extragroup females (Sekulic, 1982).Thus, it is only aggression toward other females in the group that is apparently minimized. While some studies have reported that rates of affinitive behaviors, especially grooming, also appear to be lower among females in polygynous species (see above references), grooming among red-tail, black and white colobus, and red howler females is fairly common (Neville, 1972; Struhsaker and Leland, 1979). Most intriguingly, rates of female-infant interactions (infant transfer, “aunting,” or “allomothering”) are extremely high and often unrestricted among females in polygynous groups. Hrdy (1976), Oates (1977), and McKenna (1979) review primate studies that have described infant care by nonmothers. The majority of species in which females are extremely permissive, even with very young infants, are polygynous. (Poirier [19681 has even observed cases of female Nilgiri langurs nursing nonorphaned infants along with their own.) McKenna (1979) suggested that major differences in the extent to which mothers allow their infants to be manipulated by other group females in the Colobines and Cercopithecines may ultimately be related to dietary differences between the two families. Major differences in diet were hypothesized to lead to variation in the degree to which females are competitive, as evidenced by the presence or absence of matrilineally structured dominance hierarchies. In fact, these differences in both female competitiveness and the tendency to transfer infants might derive more directly from the fact that most Colobines form polygynous groups in which females are likely to be more closely related than are females in the majority of Cercopithecine groups. Whether or not females in polygynous species also discriminate behaviorally, particularly with regard to potentially costly behavior such as joining alliances against infanticidal males or allowing newborn infants to be handled, among matrilineal and nonmatrilineal relatives (what might be called the “all animals are equal, but some are more equal than others” principle), is not known from field studies. However, Rowell and Olson (1983) have recently reported that matrilineal kinship 116 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 27, 1984 was a n important variable in the distribution of female social behavior in a captive group of patas monkeys, although the females also interacted frequently with nonmatriline members and rates of agonism among females generally were low. Coalitions against nonmatriline members were not reported. In this study, as well as in some others (e.g., Dunbar 1979b, 1983), actual categories of relatedness were not specified. Individuals were either classified as matriline or nonmatriline members, making it difficult to distinguish between mother-offspring interactions (“maternal” behavior) and those involving more distant relatives (“matrilineal” behavior). Putative matrilineal relatedness was not found to be important in dominance relations among Hanuman langur females (Hrdy and Hrdy, 1976). It seems clear that, on the whole, competitive behavior is minimized while cooperative behavior is broadly distributed among females in most polygynous species. These trends appear consistent with the patterns of kin association hypothesized in the preceding section. In two of the polygynous species in which females are not philopatric, hamadryas and gelada baboons, females appear to be more competitive, forming coalitions against one another and restricting affnitive interactions to certain individuals while excluding others in the unit (Dunbar, 1979b, 1983; Kummer, 1975; Stammbach, 1978). Although Dunbar (1979b, 1983) and Mori (1979) speculated that gelada units were composed of matrilines, this has yet to be confirmed. Hamadryas units are probably composed predominantly of unrelated adult females, but clans of male hamadryas, which may represent patrilines, tend to be spatially coherent subunits within bands (Sigg et al., 1982).As Kawai et al. (1983)point out, the social structures of gelada and hamadryas baboons, though superficially similar, are likely to be fundamentally different. Gorilla females, which normally transfer from their natal group, exchange few social behaviors, and in essence show passive tolerance for one another. Exceptions occur when individuals have been familiar during immaturity, apparently regardless of kinship (Harcourt, 1979). Harcourt (1979) attributes the general lack of aEnitive interaction among gorilla females to the fact that they are unlikely to be related. However, since unrelated females in other species, e.g., hamadryas and perhaps gelada baboons, apparently do interact, additional factors (e.g., diet, size) might also have been important in the evolution of female gorilla behavior patterns. Male-offpring interactions.-Males of most polygynous species are reported to have limited interactions with infants that are presumably their offspring (see Hrdy, 1976; Redican, 1976; Struhsaker and Leland, 1979). Hrdy (1976) distinguished indirect male investment, such as troop defense, and direct investment by defense or care of an individual infant. In general, polygynous males do not directly interact with infants, for instance by carrying, grooming, or defending them within the group. In some circumstances, however, male group defense against extragroup males probably represents a n important investment in infant survival. Although male gelada and hamadryas baboons do not interact with offspring as “follower” males, they may hold or carry infants and juveniles. But follower males often care for juvenile females who mature into a male’s first unit female. The most striking form of male-infant “interaction” in polygynous species is infanticide. Documented, if isolated, cases of infanticide have now been reported in several polygynous species: Colobines: Hanuman langurs (Hrdy, 1974, 1976, 1979); purple-faced leaf monkeys (Rudran, 1973);silvered leaf monkeys (Wolf and Fleagle, 1977);Cercopithecids: red-tail monkeys (Struhsaker, 1977);blue monkeys (Butynski, 1981); one New World species, red howler monkeys (Rudran, 1979); and gorillas (Fossey, cited in Hrdy, 1979). Notably, infanticide in gelada and hamadryas baboons has been reported only from captive or manipulated groups (Angst and Thommen, 1977; Rijksen, 1981). Patterns of infanticide vary between species. In some reports (Struhsaker, 1977) males have eaten recently killed infants, while in others (Rudran, 1979) they have not. The ages a t which infants apparently no longer attract aggression vary between species (or a t least between reports). However, the clear pattern of persistent infant- Gouzoules] PRIMATE KIN RECOGNITION 117 directed aggression appears to be restricted to species with polygynous mating system^.^ Male infanticide has also been reported in chimpanzees (see Goodall, 1977, 19831, but apparently as a consequence of severe aggression directed toward females. Similarly, infants in promiscuous baboon species have also been reported killed as a result of male aggression (Packer, 1980), but there is as yet no compelling evidence for infanticide as a reproductive strategy, such as has been suggested for polygynous species. Infanticide in polygynous species typically follows a male’s “takeover” of a group, usually a s a result of ousting the previous male. The new male may then attempt to kill young infants, purportedly to hasten their mothers’ return to reproductive receptivity, at which time the new male will mate with the females (Hrdy, 1976). Thus, infanticide is most often explained as a n evolutionary strategy to increase male reproductive success. Note that it is often under these extreme circumstances that females form coalitions against new males (Hrdy, 1977; Struhsaker, 1977). Though a complete review and discussion of infanticide is beyond the scope of this paper (see Angst and Thommen, 1977; Chapman and Hausfater, 1979; Curtin and Dolhinow, 1978; Fedigan, 1982; Hrdy, 1976,1979), one aspect of this behavior pattern is particularly relevant to a discussion of kin recognition. In all reports of male infanticide, it has been hypothesized that male recognition of offspring was contingent upon either length of tenure in the group and/or copulation with the mother. For instance, Struhsaker (1977) reports that a n infanticidal red-tail male did not kill two infants born 4 months after the male’s takeover. He suggests that, based upon the length of gestation, the male refrained from killing infants who might have been his offspring, but probably were not. It was not known whether the male had actually copulated with the infants’ mothers. Postconception copulation with a new male has, in fact, been suggested as a female counterstrategy to male infanticide in polygynous groups (Hrdy, 1977, 1979). Again, this suggestion implies that associational cues are likely to be the primary (and even the only) mechanisms of male recognition of offspring. A similar finding has been reported from experimental studies of mice (Labov, 1982). Promiscuous species Promiscuity is likely to produce the most varied kin structure of all mating systems. Within promiscuous groups a n individual may be related by descent to some individuals through maternal lines and/or through paternal lines, and to others not a t all. The importance, in terms of representation in the group, of any one of these systems of kinship probably depends chiefly upon several other reproductive parameters and may vary among promiscuous species. Interactions among females in most multimale groups in comparison with those in polygynous groups can be described as highly competitive. For example, female dominance hierarchies are well documented in most macaque and baboon species (Angst, 1975; Bernstein, 1966; Dittus, 1980; Gouzoules, 1980a; Gouzoules et al., 1982; Hausfater et al., 1982; Kawai, 1965; Koyama, 1967; Missakian, 1972; Moore, 1978; Sade, 1967; Seyfarth, 1976; Silk et al., 1981), as well as in vervet monkeys (Seyfarth, 1980; Horrocks and Hunte, 1983) and sooty mangabeys (Cercocebus atys, Bernstein, 1976). In these species, females frequently direct aggressive behavior and form coalitions against one another. It is generally the case that behavior is directed more “asymmetrically” among females in multimale groups than among those in one-male groups. The reason for this asymmetry could lie in the extent to which female relatedness is “skewed” in the direction of matrilines in promiscuously mating species. Wrangham (1980) has suggested that female behavior is generally similar in polygynous and promiscuous species where females do not emigrate (so-called “fe- 4Struhsaker (1983)has recently reported a case in which a male red colobus monkey killed several infants in its own group. 118 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 27, 1984 male-bonded’’ species) as opposed to those where females leave their natal groups (“non-female-bonded”). Although Wrangham’s ecological model (based on resourse defense by females) for the evolution of particular primate mating systems may be generally valid, the consequences of polygyny and promiscuity for patterns of female relatedness, and hence for the probability of female cooperative behavior, are likely to be fundamentally different. Several of the behavioral characteristics which Wrangham suggests are generally applicable to female-bonded species, e.g., frequent grooming, coalition formation, importance of dominance relationships, in fact apply predominantly only to females in multimale groups (see Wrangham, 1980). “Neither give heed to fables and endless genealogies -1 Timothy . . . ’’ Recognition of matrilineal kin.-The most significant finding from long-term studies (over 30 years in some cases) of Japanese and rhesus macaques has been the importance of matrilineal relatedness to the structuring of many aspects of, especially female, behavior (proximity: Yamada, 1963; grooming: Koyama, 1967; Sade, 1965,1972; dominance rank: Kawai, 1965; Kawamura, 1965; Koyama, 1967; Missakian, 1972; Sade, 1965; agonistic alliances: Kaplan, 1977, 1978; Watanabe, 1979; group fissions: Chepko-Sade and Olivier, 1979; Chepko-Sade and Sade, 1979; Koyama, 1970; Missakian, 1973b; sexual behavior: Enomoto, 1974; Missakian, 197313; Sade, 1968; Takahata, 1982; infant interactions: Berman, 1982; Gouzoules, 1980b; transmission of novel behaviors: Itani, 1965; Itani and Nishimura, 1973; Kawamura, 1959; vocalizations: Gouzoules et al., 1984, in press). It is a n interesting coincidence that these two species, which have been studied for the longest period of time of any primate species, are two that, because of several reproductive variables would be predicted to have a particularly strong development of relatedness through matrilineal lines. However, as noted above, relatedness predominantly through matrilineal lines is unlikely to be of comparable importance in polygynous and promiscuous species, nor even in all promiscuous species. In fact, the extent of matrilineal kin discrimination, even in Japanese and rhesus monkeys, has itself rarely been directly examined. First, it is necessary to distinguish between “maternal” behavior (kin-correlated behavior within a maternal family: mother, offspring, siblings) and “matrilineal” behavior (kin-correlated behavior that distinguishes much more distant categories of relatives, e.g., great-aunts, cousins, great-grand-offspring from nonrelatives). Data on matrilineal kin recognition is especially meager. The implicit assumption that individuals of multimale Old World monkey groups, particularly rhesus and Japanese macaques, “recognize” matrilineal kin to the same extent that researchers can calculate degrees of relatedness has often been accepted (e.g., Olivier et al., 1981). The critical question with respect to the recognition of kin and the mechanisms whereby recognition occurs is: What categories of kin are consistently distinguished from one another, and from the class of unrelated individuals, by behavioral interaction? This question is especially interesting in light of the extensive genealogical information now available on several provisioned groups of Japanese and rhesus monkeys. Altmann and Altmann (1980) have suggested that the very large matrilines characteristic of provisioned groups would probably be relatively unusual under more natural, i.e., more ecologically harsh, conditions (see also Melnick and Kidd, 1983).According to Sherman’s (1980,1981)hypothesis, related individuals that have rarely coexisted historically should not distinguish one another from unrelated individuals. Thus we might predict that, beyond a certain category of relatedness, even “matrilineally related’ individuals would not behaviorally discriminate one another from nonrelatives. Sherman calls this the “limits of nepotism” hypothesis. Early studies of rhesus monkey behavior established that mother-offspring and sibling relations could be distinguished from those of other group members, primarily by grooming behavior (Missakian, 1972; Sade, 1965). Yamada (1963) reported Gouzoules] PRIMATE KIN RECOGNITION 119 that even more distant categories of kin, e.g., auntdnieces, could be spatially distinguished in Japanese monkeys. Massey’s (1977, 1979) study of agonistic aiding in pigtail macaques (M. nemestrina) demonstrated that individuals distinguished mother-offspring and sibling-grandparent relations from those of all other categories of relatives (in that study, extending to r = .16): but more distant categories of kin were not distinguished. Massey did not report whether more distant classes of kin were discriminated from nonkin in the frequency of alliances. Kurland (1977) analyzed a number of affinitive (proximity and grooming) and agonistic (threats, aiding) behaviors with respect to putative (behaviorally assigned) degrees of relatedness in a troop of Japanese monkeys (see also Sherman, 1978; Walters, 1981, for discussions of Kurland’s study). In general, Kurland’s data show a marked lack of linearity between behavioral interaction and the degree of matrilineal relatedness. The exact pattern of discrimination (i.e., siblings from aunts or cousins from nonmatriline members) varied depending upon the behavior under consideration. The distribution of several behaviors (e.g., grooming, threats) did not significantly vary between more distant relatives (cousins) and matrilineally “unrelated” individuals. However, overall conclusions from the study must be viewed cautiously since the necessary data on matrilineal kinship were not available. Gouzoules (1981) studied the distribution of behavior with respect to known matrilineal kinship in a group of free-ranging Japanese monkeys in Texas. The study group (Arashiyama West) was one in which matrilineal kinship was documented from 1954 forward, on the basis of birth records, and extended to the r = 1/64 coefficient of “minimal” matrilineal relatedness. Multiple categories of affinitive and agonistic behavior of adult females were measured, and behavioral relationships with different classes of kin were delineated using multivariate techniques. The results of this study suggested that, in general, adult female Japanese monkeys did not consistently discriminate behaviorally among related conspecifics beyond quite close categories of maternal kin (e.g., r = 1/41. The results also suggested, however, that females did behaviorally distinguish some individuals, primarily adult females, from among those matrilineally unrelated. This latter finding coincides with reports by Kaplan (1978) and Kurland (19771, on rhesus and Japanese monkeys, respectively, that females aided unrelated individuals more than would have been expected by chance and more than they aided certain categories of matrilineal kin (more discussion of female relationships and matrilineal relatedness in these macaque species is provided in Gouzoules, 1981). Although avoidance of consanguineous matings in most primate species is accomplished primarily by the emigration of males at sexual maturity, in some cases males may remain in the natal group for at least some portion of their adult lives. Several researchers have reported that when males had the opportunity to mate with very close matrilineal kin (particularly mothers and sisters), they rarely did SO (Enomoto, 1974, 1978; Imanishi, 1961; Sade, 1968; Tokuda, 1961-1962). Missakian (1973a) found mother-son matings in rhesus monkeys under some circumstances (e.g., very young males) to be more frequent than had Sade (1968),but Missakian’s data generally support the conclusion that close matrilineal kin avoid mating with one another. Missakian also analyzed how frequently “familial” kin (defined as aunts-nephews, uncles-nieces, and cousins) mated. Although such matings were clearly infrequent, it was not certain whether they were less frequent than would have been predicted if mating occurred randomly. More recently, Takahata (1982) reported that, although closely related (r = 1/2 to r = 1/81 Japanese monkeys mated significantly less often than predicted by chance, more distant categories of matrilineal kin (r < 1/8) mated a t rates that would be predicted through random choice. The results of these macaque studies tentatively suggest the following. (1) In groups of rhesus and Japanese monkeys, close matrilineal relatives (particularly mothers and offspring and siblings, and less often grandmothers and grand~ ~~ 51n macaque studies, all categories of relatedness are calculated “minimally”; i e , by assuming maternal siblings are always half-siblings. 120 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 27, 1984 offspring or aunts and nieces-nephews) are usually distinguished behaviorally from all other individuals in the group. However, it also seems likely that the recognition of matrilineal kin, in terms of consistent behavioral discrimination, even in rhesus and Japanese macaques, may be more restricted than previously suspected, and certainly more limited than the degree to which genealogies have been documented under artificial provisioning. Some additional evidence for this conclusion is provided by studies of group fissions in rhesus monkeys on Cay0 Santiago. Earlier studies of group fission in Japanese and rhesus monkeys (Koyama, 1970; Missakian, 1973b) had established that, when groups divide, female matrilines tend to join as intact units one or the other of the resulting sister groups, though exceptions did occur. More recent studies of group fissions on Cay0 Santiago (Chepko-Sade and Olivier, 1979; Chepko-Sade and Sade, 1979) have reported that when genealogies become very large or when “connector females” (i.e., a female more closely related to two individuals than they are to each other) are lost, genealogies themselves may divide during group fissions. In both cases, the data suggest that the behavioral discrimination of matrilineal kin is limited either by an “upper bound” on the number of individuals that are usually developmentally classified as kin andor by the necessity of a common, more closely related, “connector” individual for the recognition of more distant relatives. The observation that genealogies tend to join groups as units, or even the welldocumented tendency of female matriline members to share similar dominance ranks (deWaal, 1977; Hausfater et al., 1982; Koyama, 1967; Missakian, 1972; though see Gouzoules et al., 1982; Koyama, 1970)is not sufficient evidence that individuals actually recognize as kin all members of very large matrilines. Note, however, a lack of recognition among related individuals does not alter the genetic consequences of particular behavioral processes that involve kin. For example, group fissions in which matrilines tend to remain together may produce new groups with higher average degrees of relatedness (Chepko-Sade and Olivier, 1979; Olivier et al., 1981; but see Melnick and Kidd, 1983). (2) Regardless of matrilineage size, female Japanese and rhesus monkeys tend also to form special relationships with nonmatrilineal (“unrelated”) kin. These relationships frequently center around alliance formation and also include other affinitive behavior (Gouzoules, 1981; Kaplan, 1978). It is not yet known to what extent matrilineally unrelated individuals in these groups are in fact patrilineal kin (see Fedigan, 1982, for further discussion of this point). Data on genetic relatedness in the Cay0 Santiago population of rhesus macaques suggests the existence of a fairly weak network of patrilineal relatedness (Cheverud et al., 1978; Duggleby, 1977; Ober et al., 1979; Olivier et al., 1981). In contrast, recent data from a wild population of Himalayan rhesus suggest a fairly strong network (Melnick and Kidd, 1983).Melnick and Kidd (1983) have hypothesized that in stable or declining rhesus monkey populations more individuals may actually be patrilineally than matrilineally related (see also Altmann, 1979).These authors further speculate that “shifts” in the predominant pattern of relatedness from “patrilines” to “matrilines” might occur regularly in rhesus population demography. These kin structures, in effect, represent two endpoints of a spectrum. Melnick and Kidd do not consider what effect such changing patterns of relatedness would be expected to have on the behavior of individuals in groups, other than to note that, in small groups, matriline size will be reduced, often to primarily mother-offspring units. This model is intriguing in light of the data presented above which suggest that discrimination of kin, even in expanding groups with large matrilines, may be restricted to fairly close categories of kin (perhaps restricted to those categories of kin that have been “evolutionarily stable”). A number of studies of other promiscuous species of Old World monkeys have suggested that at least some categories of female behavior are matrilineally structured: pigtail macaques-Massey, 1977, 1979; Rosenblum, 1971; bonnet macaques (M. radiataksilk, 1982; Silk et al., 1981;yellow baboons-Altmann, 1980; Hausfater et al., 1982; Lee and Oliver, 1979; Walters, 1980; Chacma baboons (I? ursinusl- Gouzoules] PRIMATE KIN RECOGNITION 121 Cheney, 1977, 1978; Seyfarth, 1978; and vervet monkeys-Cheney et al., 1981; Cheney and Seyfarth, 1980).In several of these studies, however, relatedness among females has been inferred from behavioral data, including dominance interactions (see Walters, 1981, for a review), and in others degree of relatedness has been classified simply as either “matrilineal” or “nonmatrilineal” (e.g., Silk, 1982; Silk et al., 1981).The combining of all categories of relatedness through female lines into a single class makes it difficult to separate “maternal” behavior from more distant “matrilineal” relationships. Since the group of bonnet macaques studied by Silk and colleagues contained up to 80 individuals and yet was composed of 18 “matrilines,” much of the matrilineal effect may have been a result of maternal behavior. Matrilineal kinship has not been advanced as the major factor underlying the distribution of behavior in many promiscuous species of New World monkeys. However, since kinship has usually been unknown, its importance could be underestimated. Social groups in these species are reported to be less cohesive than those of Old World species (Moynihan, 1976). Most reports of spatial deployment, subgroup membership, and coalition formation in New World species have emphasized the importance of sex, age, and parity, or reproductive state on behavior patterns (Baldwin, 1968,1971; Coe and Rosenblum, 1974; Eisenberg, 1976; Klein, 1974; Klein and Klein, 1975). However, both Klein (1974) and Rondinelli and Klein (1976) reported that female spider monkeys formed coalitions against other females, and also speculated that genealogical afiliation might influence choice of sexual partner in this species (see also Eisenberg, 1976; Izawa et al., 1979). Klein and Klein (1975) noted that social behavior in groups of black-capped capuchins (Cebus apella) was organized around dominancelsubordinance interactions, and in this respect resembled that of Old World genera such as macaques and baboons. The omnivorous diet of Cebus was advanced as one possible explanation for this convergence in patterns of social behavior. Clearly, the kin structure of a group will not be the sole determinant of patterns of social interaction. A number of authors have reported or suggested that, in addition to matrilineal kinship, dominance rank, sex, parity, and reproductive state were also important in determining the patterning of female behavior in several multimale species of Old World monkeys (Fairbanks, 1980; Seyfarth, 1976, 1977, 1980; Silk, 1982; Walters, 1980).It is also conceivable, though as yet undocumented, that patrilineal kinship might be important in structuring behavioral interaction among matrilineally unrelated individuals in some of these species. Additional studies of New World monkeys, in which female genealogical relations are known, would contribute considerably to the understanding of the complex, multivariate, nature of kin structure, ecology, and social interaction. In those promiscuous species in which females emigrate, e.g., red colobus monkeys, female group members apparently interact infrequently, either affinitively or agonistically (Struhsaker and Leland, 1979). In contrast, male red colobus (who are likely to be related) behave much as females in other promiscuous species; i.e., they are spatially cohesive, form a dominance hierarchy, and direct both aggressive and affinitive behaviors toward one another (Struhsaker and Leland, 1979). In addition to the extensive documentation of genealogical relationships of some Japanese and rhesus macaque troops, lengthy records also exist for the chimpanzee population a t the Gombe Stream National Park. Because of the long life-span and relatively delayed age of sexual maturation in chimpanzees, categories of relatedness have not been extended to the same degree as in the macaques, though data on chimpanzee matrilineal relatedness a t Gombe now extend through three generations in some cases (Goodall, 1983). As indicated in the preceding section, motherdependent offspring units and all-male groups are the most typical forms of social units among chimpanzees. Pusey (1983) noted that mothers may continue to associate with male offspring even after weaning and occasionally even with adolescent daughters. However, primarily because of demographic patterns, there appears to be no evidence of a “matrilineal” network of relationships in chimpanzees. The existence of strong mother-offspring and sibling relationships, including those of 122 YEARBOOK OF PHYSICAL ANTHROPOLOGY IVol. 27, 1984 brothers who remain in their natal community, undoubtedly is based on a recognition mechanism involving developmental association. As Bekoff (1981) has pointed out, such relationships can be highly significant in terms of their consequences, and in the case of chimpanzees may involve food-sharing, defense, and even adoption. “Zt is a wise father that knows his own child. ’’ -Shakespeare, The Merchant o f Venice Male recognition of offspring. -In general, males of promiscuous species interact with infants and juveniles to a greater extent than do polygynous males, though a considerable amount of variation in patterns of male behavior toward immatures exists across different promiscuous species (Redican, 1976). For example, although male “paternal” behavior has been reported from several field studies of Japanese monkeys (Gouzoules, 1984; Hasegawa and Hiraiwa, 1980; Itani, 19591, males apparently rarely interact with infants in the closely related rhesus macaque (see Berenstain et al., 1981).Male stumptail (M. arctozdes) and Barbary (M. syluanus) macaques direct various affnitive behaviors toward infants (Bertrand, 1969; Deag and Crook, 1971; Estrada and Sandoval, 1977; Gouzoules, 1975; Taub, 19801, but male pigtail macaques have rarely been reported to do so (see Keiman and Malcolm, 1981; Redican, 1976, for reviews). On the whole, male-infant interactions appear to be more widespread and less variable in the baboons than in the macaques (Altmann, 1980; Busse and Hamilton, 1981; Hamilton et al., 1982; Packer, 1979a, 1980; Ransom and Ransom, 1971; Ransom and Rowell, 1972; Strum, 1983).Chimpanzee males have also been reported to provide alloparental care to infants, particularly in the form of playful behavior (Nishida, 1983). In Japanese macaques, adult male care of infants has been depicted as completely protective, or “care-giving,” in nature (grooming, carrying, defending). In this species, unweaned infants have even been adopted by high-ranking group males after the deaths of mothers (Hasegawa and Hiraiwa, 1980; see also Itani, 1959; Koyama, 1970). There is no evidence that male Japanese monkeys use infants in “agonistic buffering” (Gouzoules, 19841, nor that male selection of infants for special attention in this species is based upon a recognition of paternity; in most reported cases of “paternal” care, a father-offspring relation seemed unlikely (see Gouzoules, 1984). Male-infant interactions in Barbary macaques and in olive (I? anubis), yellow, and chacma baboons are more complex, and apparently involve both protective and exploitative behavior that may even increase an infant’s chance of being injured (Deag and Crook, 1971; Taub, 1980; also above references). Functional explanations of male behavior toward infants in these species have been widely debated (see Packer, 1980; Strum, 1983, for discussion). In general, the data from baboon studies suggest a n asymmetry in male-infant interaction that is based upon the timing of male immigration into a group. Males who are present in groups a t the time of infants’ conceptions (“potential” fathers) frequently interact with infants, while more recent immigrants do not (Busse and Hamilton, 1981; Packer, 1979a). On the contrary, recent immigrants may evoke both fear from infants and care-taking behavior from “possible” fathers. Thus, infants themselves apparently distinguish the class of males present in the group a t the time of their birth from the class of males which join it subsequently. Packer (1979a, 1980)has reported that, within the class of “possible-offspring,” males did not further distinguish probable offspring from other infants. This is not to suggest that males interact with all infants equally. Most studies (Altmann, 1980; Busse and Hamilton, 1981; Ransom and Ransom, 1971; Taub, 1980)have reported that males interact preferentially with one or a few infants. In some cases, infants might be the offspring of the males, but in others they are probably not. Occasionally males choose the infants of females with whom they have had prior “special” relations or even consort relations for interaction (Altmann, 1980; Busse and Hamilton, 1981; Ransom and Rowell, 19721, but this is not always the case (Altmann, 1980; Packer, 1980). Gouzoules] PRIMATE KIN RECOGNITION 123 Busse and Hamilton (1981)have recently suggested that male chacma baboons are in fact able to recognize offspring, and that male “care,” which consists of carrying infants in confrontations with higher-ranking recently immigrant males, has evolved to protect offspring from possible infanticide (See Strum, 1983, for a n alternative hypothesis). In the Busse and Hamilton study, one infant was killed by a n unknown male, and another infant was killed by a male during the capturing of the group. However, infanticide has not been reported from other baboon study sites, despite many years of continuous monitoring of these populations. Rather, Packer (1980) has noted that infants are sometimes hurt, and may even be killed, apparently as a n epiphenomenon of being carried into male-male interactions. Hamilton et al. (1982) have also reported that when several infants in the chacma baboon study group were orphaned, adult males, including possible fathers, did not attempt to adopt them. These authors conclude that fathers should adopt offspring only if the infants’ improved chances of survival exceed the cost to fathers of diminished future mating activities, although why nonnutritive male care of infants should be particularly costly in terms of mating activities is not clear. Gouzoules (1984) in fact argues that adult males will probably incur the least potential cost from infant adoption (see also Packer, 1980). The latter hypothesis suggests that if males could recognize offspring they, rather than female relatives, would be the most likely class of individuals to adopt them in cases of maternal death. Although Nishida (1983) points out that male chimpanzees are potential fathers of the infants in their communities, he provides no evidence that males distinguish for interaction those infants most likely to be their offspring. He suggests that maternal permissiveness is probably the most important factor in the selection of a n infant. The data on male-infant interactions in promiscuous primate species suggest that males distinguish possible or potential offspring based primarily upon the temporal pattern of group membership and possibly upon association with the mother (but see below). This mechanism of offspring recognition resembles that proposed for polygynous males. There is, as yet, no compelling evidence that males make “finer” distinctions among infants, i.e., actually recognize offspring. Taub (1980) has speculated that the mating behavior of female Barbary macaques (M. syluana) is unique in that females attempt to copulate with all group males in order to confuse the issue of paternity and so insure a certain level of male investment in infants. However, careful examination of the data from baboon studies may suggest that such a strategy would not be necessary since, in these species, membership in a group at the time a n infant is conceived may be a sufficient (and indeed the only) stimulus for male care. Laboratory studies of kin recognition Maleoffspring recognition-It should be noted that none of the discussions of maleoffspring recognition in wild groups had available biochemical data on paternity. Recently several papers have dealt with the possible recognition of paternity by males in captive rhesus monkeys a t the Davis Primate Center (Berenstain et al., 1981; Smith, 1982a,b). In the most detailed study, Berenstain et al. (1981) analyzed the behavioral relationships of male rhesus monkeys with their electrophoretically determined offspring. While infants were found to spend significantly more time in proximity to their fathers than to other males, the effect of paternity accounted for only 5% of the variance in the data and was correlated with maternal proximity relationships to males. If maternal behavior was controlled for, the effect of paternity on infant proximity disappeared. Thus Berenstain et al. (1981: 1061-1062) concluded: “The absence of active preference for offspring by adult males, coupled with the small variable effect of paternity on male-immature spatial relations, strongly suggests that selective paternal behaviour that discriminates among immatures born during a male’s residence in a group is not part of the rhesus male’s repertoire . . . thus, there is no evidence here for either direct recog- 124 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 27, 1984 nition of offspring by fathers or reliable indirect identification of offspring through fine discrimination of the relative success of past matings.” In light of the documented ability of male baboons to recognize the class of infants born into a group during their residency, the lack of such a n effect in the Berenstain et al. study suggests that male-infant interaction has not been selected for in rhesus monkeys. In the absence of any selective pressure, even gross levels of recognition have probably not evolved in this species. Further evidence for this suggestion was provided by Smith (1982b), who observed that males in captive rhesus groups, if not removed by the time their daughters matured, did not avoid consanguineous matings. Smith concluded that it is probably male dispersal at sexual maturity, as well as changes in male rank relations, rather than recognition of patrilineal kin, that prevent a greater degree of inbreeding in rhesus groups. In contrast, Packer (1979a) reported that juvenile female baboons, upon reaching sexual maturity, continued to distinguish between familiar males (“possible” fathers) and novel males (more recent immigrants). Matings of male baboons with possible daughters were significantly less frequent than with other females. These data again suggest that different selective pressures for the recognition of offspring and other kin may exist, even among species with similar mating systems. Recognition of other patrilineal kin-While the selective pressures on males to recognize offspring in some promiscuous species may be fairly limited, in certain cases one might expect greater selection for females to distinguish conspecifics related through paternal lines. The importance of female matrilineal or maternal relatedness to female behavior in these species is well documented. But, does the importance of matrilineal kinship necessarily mean that patrilineal kinship is unrecognized? For instance, while association, e.g., sharing a natal burrow, is the most important determinant of female behavioral discrimination in ground squirrels, it is not the only one. Females of some species also distinguish maternal halfsiblings from unrelated individuals in the absence of association subsequent to birth. Clearly, such recognition would be advantageous to female paternal half-siblings, which may inhabit the same natal group throughout their lives in promiscuous primate species and where competition among matrilineally unrelated females, usually expressed via dominance interactions, can be intense. Field observations of rhesus and Japanese macaques (Gouzoules, 1981; Kaplan, 1978; Kurland, 1977)have suggested that females do behaviorally discriminate among matrilineally unrelated females. Is there any evidence for the ability of individuals in promiscuous species to distinguish paternally related kin? A widely cited study in the general literature on kin recognition is that of Wu et al. (1980). In this study, immature pigtail macaques (ranging in age from about 1.5 to 11 months), presented with a choice between unfamiliar, paternal half-siblings and unfamiliar, unrelated individuals, approached their siblings for longer periods of time. Experimental “choice” immatures were sex- and age-matched and ranged from 6 days to 206 days of age. This study is frequently offered as evidence that in the laboratory pigtail macaques are capable of paternal kin recognition in the absence of associational cues. Recently, Fredrickson and Sackett (1984) conducted a study in which they attempted to replicate the results of Wu et al. (1980). Fredrickson and Sackett employed a much larger sample of young pigtail monkeys (N = 90) and they tested for the effects of both kinship and familiarity on the choice between two stimulus animals. Their results strongly implicated familiarity and not paternal kinship as the most important factor governing choice of a partner for spatial association. In none of the test conditions were unfamiliar-related individuals preferred over unfamiliar-unrelated or familiar-unrelated individuals. In contrast, however, unrelatedfamiliar individuals were significantly preferred over unrelated-unfamiliar and related-unfamiliar animals. There was no difference in preference between related and unrelated familiar individuals. The strong and consistent results of these experiments led Fredrickson and Sackett to conclude that familiarity was the only basis Gouzoules] PRIMATE KIN RECOGNITION 125 for choice among stimulus animals and that the discrepancy between their study and the earlier one of Wu et al. (19801, which employed only 16 subjects, was due to type I statistical error. Wu et al. (1980) had speculated that a form of phenotypic matching, possibly using visual cues, might be the mechanism of recognition of paternal kin. Although phenotypic matching has been invoked in a number of studies of kin recognition, its genetic and ontogenetic basis has rarely been critically examined. Lacy and Sherman (1983) have recently considered two models of kin categorization based on a process of matching individuals on the basis of genetically controlled traits against a learned template. The two models assumed either discrete or continuously varying traits. (The reader is referred to Lacy and Sherman 119831 for a complete explication of these models.) The implications of the models led Lacy and Sherman (1983: 507) to cautiously conclude that although phenotypic matching is possible, usually “many traits must be assessed for moderately reliable recognition of relatives,” and that “the large amount of genetic information required may be one reason why phenotype matching has not been commonly observed as a mechanism of nepotism or avoidance of close inbreeding.” A considerable degree of selective pressure would probably have to be assumed before phenotypic matching would become a reliable mechanism of kin recognition. In another laboratory study of kin recognition, Small and Smith (1981) attempted to assess differences in behavior that correlated with paternal relatedness under less closely confined conditions in a breeding group of rhesus monkeys a t the Davis Primate Center. While this study has been cited as demonstrating “that recognition of paternal relatedness . . . exerts a n important influence on social behavior” (Richard and Schulman, 1982), some reservations about this conclusion remain. The data consisted of interactions between infants and their full siblings, paternal halfsiblings, and unrelated immatures, combined into a single category called “grabbing.” All maternal behavior was similarly combined into a category labelled “resist grabs.” Thus, both affnitive and agonistic interactions were apparently considered jointly so that it is not possible to evaluate what the variation in the behavior of differently related “grabbers,” or variation in degree of maternal “resistance,” actually represents. Moreover, while the results suggested that mothers resisted nonrelatives more than paternal half-siblings, there was no difference in the frequency of resistance to nonrelatives and full siblings. Data on the nature of dominance rank relations of the individuals in various categories of relatedness are not presented, although dominance rank has been shown to be important in structuring the interactions of mothers and infants with other group members (Altmann, 1980; Berman, 1980; Gouzoules, 1975). Thus, although the questions raised by this study are intriguing, and deserve further examination, there are as yet no compelling data to suggest a n ability, by rhesus macaques, to recognize paternally related kin. Recognition of the kin-relations of others Human kinship structure and behavior is a n enormously complicated and welldocumented topic (see, for example, Fox, 1967; Levi-Strauss, 1970) and cannot be incorporated in a complete fashion in this review. However, one aspect of kin recognition, relevant to all primate species and generally not arising in discussions of other taxa, is whether or not individuals might recognize the kin relations of others, as we11 as their own. Humans, of course, both recognize and communicate about the relationships of others. Human kinship terminology is linguistically and perceptually distinct from the way in which other objects are named (e.g., Miller and Johnson-Laird, 1976).Evidence that individuals are aware of the social relationships, including kin relations, of others a t least in some nonhuman primate species, has come primarily from recent studies of vocal communication (Cheney and Seyfarth, 1980, 1982; Gouzoules et al., 1984, in press). By playing tape-recorded vocalizations of infants to vervet monkeys, Cheney and Seyfarth (1980)demonstrated that females recognize calls of another female’s infant: upon hearing a n infant’s cry a female looked toward the caller’s mother who was 126 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 27, 1984 sitting nearby. Thus, vervet monkeys might, to some extent, categorize group members on the basis of kin relationships (see Cheney and Seyfarth, 1982, for more discussion). Gouzoules et al. (1984) found that rhesus monkeys in similar social situations gave acoustically different types of vocalizations to matrilineal kin and nonkin. When different call types tape-recorded from relatives were played for females, they reacted differently to calls normally given to kin than to those given to nonkin. This study suggested that, not only do individuals themselves distinguish certain classes of kin, but other animals are capable of perceiving the network of relationships of fellow group members using vocal cues alone. This vocal system of rhesus monkeys is in some ways analogous to kinship terminology in human language (Gouzoules et al., in press). In a study of nonvocal social behavior, Judge (1983)reported that pigtail macaques involved in aggression often “reconciled” subsequently with the relatives of their opponents. These individuals had not been participants in the original agonistic incident. Judge’s work and the above vocalization studies suggest that in a t least some, and probably many, species of primates individuals are aware of the social relationships, including kin relations, of other group members. As in other research on primate kin-correlated behavior, data on the extent of primates’ perception of others’ kin relations and the mechanisms of this recognition are needed. CONCLUSIONS Although factors such as dominance rank, sex, age, and reproductive state are variably important, patterns of cooperative behavior in many primate species can be accounted for largely by kinship. As in Belding’s ground squirrels, there appear to be limits to primate nepotism and the recognition of kin. These limits are most likely a result of complex ecological factors (e.g., diet, predation, resource distribution, competition), phylogenetic constraints (e.g., body size, locomotory mode), as well as mating system and dispersal patterns. For group-living polygamous species the latter two factors are hypothesized as being particularly important in accounting for the extent and distribution of kin-directed cooperative behavior within primate social groups. In general, groups in species characterized by female philopatry and polygyny should be comprised of networks of closely related females. In these species, competitive behavior is notably reduced relative to cooperative behavior. In contrast, female philopatry and promiscuity tend to produce a n asymmetrical system of female kinship that apparently correlates with increased competition among matrilineally unrelated females and the concentration of cooperative behavior particularly among “evolutionarily stable” classes of maternal kin. Discrimination of close paternal kin in these groups might also be hypothesized as important under certain conditions; however, the historical “stable distribution” of paternal kin in promiscuous species is likely to have been more variable, and thus the selective pressure for such recognition may have been less intense. The most important mechanism for the avoidance of inbreeding in primates is the dispersal of members of one sex. Where maternal kin co-occur,close consanguineous matings are rare. Males in polygamous primate species may not recognize individual offspring. Recognition of possible or probable offspring in polygynous species, and in some promiscuous species, is likely to be a consequence of the timing of male residency in the group, and confidence in paternity probably varies with the number of adult breeding males. Thus, in polygynous species, where only one male is present in the group, a relatively high degree of paternity assurance may have led to the evolution of male reproductive strategies, such as infanticide. The evolution of infanticide has probably been countered in promiscuous groups by the presence and reproductive behavior of multiple adult males, which results in males “sharing” recognition of possible paternity for a cohort of infants. The most important mechanism for the discrimination of related conspecifics in primates is probably association during development. In promiscuous groups behavioral discrimination of kin appears to be most consistent only among close maternal Gouzoules] PRIMATE KIN RECOGNITION 127 relatives, which are also those individuals most familiar with one another during rearing. In these species, the coefficient of relatedness among close maternal kin covaries with the “coefficient of familiarity” (Bekoff, 1981). If the distribution of cooperative behavior is contingent only upon familiarity, it cannot be assumed that individuals are actually discriminating on the basis of the degree of genetic relatedness. There is as yet no evidence that strong selective pressures for the recognition of paternal kin have been present in primate species. In the absence of such evidence, especially in natural social groups, the tentative suggestion that paternal kin are probably not recognized as such in promiscuous primate groups is offered. Clearly, definitive answers to many of the questions raised in this review await data on social interactions amongst individuals in natural social groups where kinship is known. Logistically, such data could be most easily obtained from laboratory groups of natural social composition. 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