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Primate mating systems kin associations and cooperative behavior Evidence for kin recognition.

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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
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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).
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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.
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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
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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.
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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).
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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.
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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
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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
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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.
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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.
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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
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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-
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[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
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[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. Also crucial to a n ultimate understanding
of the evolution and extent of nepotism in different primate species, and much more
difficult to acquire, are data on the demography of various classes of paternal and
maternal kin over several generations from a number of wild populations.
ACKNOWLEDGMENTS
I am very grateful to the following people who critically read and commented on
earlier drafts of the manuscript: L.M. Fedigan, H. Gouzoules, W. Holmes, P. Marler,
J. Murie, R. Seyfarth, and P. Sherman.
LITERATURE CITED
Altmann, J (1979)Age cohorts as paternal sibships.
Behav. Ecol. Sociobiol. 6r161-164.
Altmann, J (1980) Baboon Mothers and Infants.
Cambridge: Harvard University Press.
Altmann, J, Altmann, SA, Hausfater, G, and McCuskey, SA (1977)Life history of yellow baboons:
Physical development, reproductive parameters
and infant mortality. Primates 18:315-330.
Altmann, SA, and Altmann, J (1970) Baboon Ecology: African Field Research. Chicago: University
of Chicago Press.
Altmann, SA, and Altmann, J (1980) Demographic
constraints on behavior and social organization.
In IS Bernstein and EO Smith (eds): Primate Ecology and Human Origins. New York: Garland
STPM Press, pp. 47-63.
Angst, W (1975) Basic data and concepts on the
social organization of Macaca fasicularis. In LA
Rosenblum (ed): Primate Behavior. Developments
in Field and Laboratory Research, Vol. 4. New
York: Academic Press, pp. 325-388.
Angst, W, and Thommen, D (1977) New data and a
discussion of infant killing in Old World monkeys
and apes. Folia Primatol. 27r198-229.
Armitage, KB, and Johns, DW (1982) Kinship, reproductive strategies and social dynamics of yellow-bellied marmots. Behav. Ecol. Sociobiol.
11.55-63.
Baldwin, J (1968)The social behavior of adult male
squirrel monkeys (Saimiri sciureus) in a seminatural environment. Folia Primatol. 9:281-314.
Baldwin, J (1971) The social organization of a semifree-ranging troop of squirrel monkeys (Sairniri
sciureus). Folia Primatol. 14:23-50.
Barash, DP (1975) Ecology of paternal behavior in
the hoary marmot (Marmota caligata): An evolutionary interpretation. J. Mammol. 56613-618.
Bearder, SK, and Doyle, G (1974)Field and laboratory studies of social organization in bushbabies
(Galago senegalensis). J. Human Evol. 3t37-50.
Beecher, MD (1982)Signature systems and kin rec-
ognition. Am. Zool. 22,477-490.
Bekoff, M (1981) Mammalian sibling interactions.
In DJ Gubernick and PH Klopfer (eds.): Parental
Care in Mammals. New York: Plenum Press, pp.
307-347.
Berenstain, L, Rodman, PS, and Smith, DG (1981)
Social relations between fathers and offspring in
a captive group of rhesus monkeys (Macaca mulatta). Anim. Behav. 29:1057-1063.
Berman, CM (1980)Early agonistic experience and
rank acquisition among free-ranging infant rhesus monkeys. Int. J. Primat. lt153-170.
Berman, CM (1982)The ontogeny of social relationships with group companions among free-ranging
infant rhesus monkeys. I. Social networks and
differentiation. Anim. Behav. 3Ot149-162.
Bernstein, IS (1966) Analysis of a key role in a
capuchin (Cebus albifrons) group. Tulane Stud.
Zool. 13(2):49-54.
Bernstein, IS (1976)Dominance, aggression and reproduction in primate species. J. Theor. Biol.
60:459-472,
Bertrand, M (1969)The behavioral repertoire of the
stumptail macaque. Bibl. Primatol. 11:l-273.
Blaustein, AR (1983) Kin recognition mechanisms:
Phenotypic matching or recognition alleles? Am.
Nat. 121:749-754.
Blaustein, AR, and O’Hara, RK (1981)Genetic control for sibling recognition? Nature 290r246-248.
Blaustein, AR, and O’Hara, RK (1982) Kin recognition in Rana cascadae tadpoles: Maternal and
paternal effects. Anim. Behav. 30t1151-1157.
Boelkins, RC, and Wilson, AP (1972) Intergroup
social dynamics of the Cay0 Santiago rhesus (Macaca nulatta) with special reference to changes in
group membership by males. Primates 13:125140.
Bourliere, F, Hunkeler, C, and Bertrand, M (1970)
Ecology and behavior of Lowe’s guenon (Cercopithecus campbelli Zowei) in the Ivory Coast. In JR
Napier and PH Napier (eds): Old World monkeys.
128
YEARBOOK OF PHYSICAL ANTHROPOLOGY
New York: Academic Press, pp. 297-350.
Box, H (1977)Quantitative data on the carrying of
young captive monkeys (Callitrinjacchus)by other
members of their family groups. Primates 18:475484.
Bradbury, JR, and Vehrencamp, SL (1977) Social
organization and foraging in emballonurid bats.
111. Mating Systems. Behav. Ecol. Sociobiol. 21117.
Breed, MD (1981)Individual recognition and learning of queen odors by worker honey bees. Proc.
Natl. Acad. Sci. USA 78t2635-2637.
Breed, MD (1983) Nestmate recognition in honey
bees. Anim. Behav. 31t86-91.
Brown, JL (1978) Avian communal breeding systems. Annu. Rev. Ecol. Syst. 9t123-155.
Brown, K, and Mack, D (1978)Food sharing among
captive Leontopithecus rosalia. Folia Primatol.
29:268-290.
Buckle, GR, and Greenberg, L (1981) Nestmate recognition in sweat bees (Lasioglossum zephyrurn):
Does an individual recognize its own odour or only
odours of its nestmates? Anim. Behav. 29t802809.
Bundnitz, N, and Dainis, K (1975) Lemur catta.
Ecology and behaviour. In I Tattersall and R Sussman (eds): Lemur Biology. New York: Plenum
Press, pp. 219-235.
Burton, F (1972) The integration of biology and
behavior in the socialization of Macaca syluana of
Gilbraltor. In FE Poirier (ed): Primate Socialization. New York: Random House, pp. 29-62.
Busse, C, and Hamilton, WJ (1981)Infant carrying
by male chacma baboons. Science 212t1281-1283.
Butynski, TM (1981)Harem-male replacement and
infanticide in the Kibale Forest, Uganda. Am. J.
Primatol. 3t1-22.
Chalmers, N (1968)Group composition, ecology and
daily activities of free living mangabeys in
Uganda. Folia Primatol. 8:247-262.
Chapais, B (1983)Reproductive activity in relation
to male dominance and the likelihood of ovulation
in rhesus monkeys. Behav. Ecol. Sociobiol. 12t215228.
Chapman, M, and Hausfater, G (1979) The reprodutive consequences of infanticide in langurs. Behav. Ecol. Sociobiol.5t227-240.
Charles-Dominique,P (1975)Vie sociale de Peredic
ticus potto (Primate, Lorisides) Etude de terrain
en foret equatoriale de I’Ouest Africain au Gabon.
Mammalia 38t355-379.
Charles-Dominique, P (1977) Ecology and Behaviour of Nocturnal Primates: Prosimians of Equatorial West Africa. New York: Columbia
University Press.
Charles-Dominique, P, and Hladik, CM (1971) Le
lepilemur du Sud de Madagascar: Ecologie, alimentation et vie sociale. Terre Vie 25t3-66.
Cheney, DL (1977) The acquisiton of rank and the
development of reciprocal alliances among freeranging immature baboons. Behav. Ecol. Sociobiol. 2r303-318.
Cheney, DL (1978)Interactions of male and female
baboons with adult females. Anim. Behav. 26389408.
Cheney, DL, Lee, PC, and Seyfarth, RM (1981) Behavioral correlates of non-random mortality
among free-ranging female vervet monkeys. Behav. Ecol. Sociobiol. 9t153-161.
Cheney, DL, and Seyfarth, RM (1980) Vocal recognition in free-ranging vervet monkeys. Anim. Be-
rvoi. 27,1984
hav. 28:363-367.
Cheney, DL, and Seyfarth, RM (1982) Recognition
of individuals within and between groups of freeranging vervet monkeys. Am. Zool.22t519-529.
Cheney, DL, and Seyfarth, RM (1983) Non-random
dispersal in free-ranging vervet monkeys: Social
and genetic consequences. Am. Nat. 122t392-412.
Chepko-Sade, D, and Olivier, TJ (1979) Coefficient
of genetic relationship and the probability of intragenealogical fission in Macaca mulatta. Behav.
Ecol. Sociobiol. 5~263-378.
Chepko-Sade, BD, and Sade, DS (1979) Patterns of
group splitting within matrilineal kinship groups:
A study of social group structure in Macaca mulattu (Cercopithecidae: Primates). Behav. Ecol. Sociobiol. 5:67-87.
Cheverud, JM, Buettner-Janusch, J, and Sade, DS
(1978)Social group fission and the origin of intergroup genetic differentiation among the rhesus
monkeys of Cay0 Santiago. Am. J. Phys. Anthropol. 49:449-456.
Chivers, D (1974) The Siamang in Malaya, a field
study of a primate in a tropical rainforest. Contrib. Primatol. 4:l-335.
Chivers, D (1976) Communication within and between family groups of siamang (Symphalangus
syndactylus). Behaviour 57:116-135.
Chivers, DJ, and Raemakers, J (1980) Long-term
changes in behaviour. In DJ Chivers (ed): Malayan Forest Primates: 10 Years of Study in
Tropical Rainforest. New York: Plenum Press,
pp. 209-260.
Clark, AB (1978) Sex ratio and local resource
competition in a prosimian primate. Science. 201:
163-165.
Clutton-Brock, TH (1974) Primate social organization and ecology. Nature 232539-542.
Clutton-Brock,TH (1975)Ranging behaviour of red
colobus (Cobbus badiurn tephrosceles) in the
Gombe National Park. Anim. Behav. 23t706-722.
Clutton-Brock, TH, and Harvey, P (1976) Evolutionary rules and primate societies. In PPG Bateson and RA Hinde (eds): Growing Points in
Ethology. Cambridge: Cambridge Univ. Press, pp.
195-237.
Clutton-Brock, TH, and Harvey P (1977) Primate
ecology and social organization. J. 2001. 183:l-39.
Clutton-Brock, TH, and Harvey, PH (19781 Mammals, resources and reproductive strategies. Nature 273: 191- 195.
Coe, CL, and Rosenblum, LA (1974) Sexual segregation and its ontogeny in squirrel monkey social
structure. J. Human Evol. 3t551-561.
Crook, JH (1970) The socio-ecology of primates. In
JH Crook (ed): Social Behaviour in Birds and
Mammals. New York: Academic Press, pp. 103-166.
Crook, JH,and Gartlan, S (1966) Evolution of primate societies. Nature 21Ot1200-1203.
Curtin, R, and Dolhinow, P (1978) Primate social
behavior in achanging world. Am. Sci. 66468-475.
Davis, LA (1982) Sibling recognition in Richardson’s ground squirrels (Spermophilus richardsonii). Behav. Ecol. Sociobiol. 11:65-70.
Dawson, GA (1977) Composition and stability of
social groups of the tamarin, Saguinus oedipus
geoffreyi, in Panama: ecological and behavioral
implications. In DG Kleiman (ed): The Biology
and Conservation of the Callitrichidae. Washington, DC: Smithsonian Institution Press, pp. 23-37.
V g , J, and Crook, J (1971) Social behavior and
agonistic buffering’ in the wild Barbary macaque
Gouzoules]
PRIMATE KIN RECOGNITION
Macaca sylvana L Folia Primatol. 15:183-200.
Dittus, WPJ (1977) The social regulation of population density and age-sex distribution in the
toque monkey. Behaviour 63:281-322.
Dittus, WPJ (1980) The social regulation of primate
populations: A synthesis. In DG Lindburg (ed):
The Macaques: Studies in Ecology, Behavior and
Evolution. New York: Reinhold Co., pp. 263-286.
Drickamer, LC, and Vessey, SH (1973) Groupchanging in free-ranging rhesus monkeys. Primates 14:359-368.
Duggleby, CR (1977) Blood group antigens and the
population genetics of Macaca mulatta on Cay0
Santiago. 11. Effects of social group division. Yrbk.
Phys. Anthropol. 20:263-271.
Dunbar, R (1979a) Population demography, social
organization, and mating strategies. In IS Bernstein and EO Smith (eds): Primate Ecology and
Human Origins. New York: Garland STMP Press,
pp. 65-88.
Dunbar, R (197913) Structure of gelada baboon reproductive units. I. Stability of social relationships. Behaviour 69:72-87.
Dunbar, RIM (1980) Demographic and life-history
variables of a population of gelada baboons. J.
Anim. Ecol. 49:485-506.
Dunbar, R (1983) Structure of gelada baboon reproductive units. 11. Social relationships between reproductive females. Anim. Behav. 31.556464.
Dunbar, R, and Dunbar, P (1975) Social dynamics
of gelada baboons. Contrib. Primatol. 6, Basel:
Karger.
Eisenberg, JF (1976) Communication mechanisms
and social integration in the black spider monkey,
Ateles fusciceps and related species. Smithsonian
Contrib. Zool. 133:.
Eisenberg, JF,and Kuehn, RE (1966)The behavior
of Ateles geoffroyi and related species. Smithsonian Misc. Collections 151:l-63.
Eisenberg, JF, Muckenhirn, N, and Rudran, R
(1972) The relation between ecology and social
structure in primates. Science 176:863-874.
Ellefson, JO (1968) Territorial behaviour in the
common white-handed gibbon, Hylobates lar Linn.
In PC Jay (ed): Primates: Studies in Adaptation
and Variability. New York Holt, Rinehart and
Winston, pp. 180-199.
Ellefson, JO (1974) A natural history of whitehanded gibbons in the Malayan peninsula. In DM
Rumbaugh (ed): Gibbon and Siamang, Vol. 3.
Base1 S. Karger, pp. 2-136.
Emlen, ST, and Oring, LW (1977) Ecology, sexual
selection, and the evolution of mating systems.
Science 197:215-223.
Enomoto, T (1974) The sexual behavior of Japanese
monkeys. J. Human Evol. 3:351-372.
Enomoto, T (1978) On social preference in sexual
behavior of Japanese monkeys (Macaca fuscata).
J. Human Evol. 7.283-293.
Epple, G (1975) The behavior of marmoset monkeys. In LA Rosenblum (ed): Primate Behavior.
Developments in Field and Laboratory Research,
Vol. 4. New York Academic Press. pp. 195-240.
Estrada, A, and Sandoval, J M (1977) Social relations in a free-ranging troop of a stumptail macaques (Macaca arctoides): Malecare behavior I.
Primates 18:793-813.
Fairbanks, LA (1980) Relationships among adult
females in captive vervet monkeys: testing a model
of rank-related attractiveness. Anim. Behav.
28:853-359.
129
Fedigan, LM (1982) Primate Paradigms, Sex Roles
and Social Bonds. Montreal: Eden Press.
Fedigan, LM and Baxter, MJ (in press) Sex differences and social organization in free-ranging spider monkeys (Ateles geofioyi). Primates.
Fox, R (1967) Kinship and Marriage. Harmondsworth, Middlesex: Penguin Books.
Frederickson, WT and Sackett, GP (1984)Kin preference in primates (Macaca nemestrina): Relatedness or familiarity? J. Comp. Psychol. 98:29-34.
Furuya, Y (1962)The social life of the silvered leafmonkeys, Trachypithecus cristatus. Primates 3:
41-60.
Furuya, Y (1965) Social organization of the crabeating monkey. Primates 6285-336.
Galdikas, B (1979) Orangutan adaptation in Tanjung Putin Reserve: Mating and ecology. In DA
Hamburg and ER McCown (eds): The Great Apes.
Menlo Park, CA: The BenjamidCummings Publ.
Co., pp. 195-234.
Gautier-Hion, A (1971) L'ecologie du talapoin du
Gabon. Terre Vie 25427-490.
Gautier-Hion, A, and Gautier, JP (1978) Le singe
de Brazza: une strategie originale. Z. Tierpsychol.
46:84-104.
Getz, WM,and Smith, KB (1983) Genetic kin recognition: Honey bees discriminate between full
and half sisters. Nature 320:147-148.
Glander, K (1980) Reproduction and population
growth in free-ranging mantled howling monkeys. Am. J. Phys. Anthropol. 53:25-36.
Glick, BB (1980) Ontogenetic and psychobiological
aspects of the mating activities of male Macaca
radiata. In DG Lindburg (ed): The Macaques:
Studies in Ecology Behavior and Evolution. New
York Van Nostrand Reinhold Co., pp. 345-370.
Goodall, J (1968) The behaviour of free-living chimpanzees of the Gombe Stream Reserve. Anim. Behav. Monogr. 1:161-311.
Goodall, J (1977) Infant killing and cannibalism in
free-living chimpanzees. Folia Primatol. 28:259282.
Goodall, J (1983) Population dynamics during a 15
year period in one community of free-living chimpanzees in the Gombe National Park, Tanzania.
Z. Tierpsychol. 61:1-60.
Guuzoules, H (1975)Maternal rank and early social
interactions of infant stumptail macaques, Macaca arctoides. Primates 16r405-418.
Gouzoules, H (1980a) A description of genealogical
rank changes in a troop of Japanese monkeys
(Macaca fuscata). Primates 21:262-267.
Gouzoules, H (1980b)Biosocial Determinants of Behavioral Variability in Infant Japanese Monkeys.
Ph.D. dissertation, University of Wisconsin,
Madison.
Gouzoules, H (1984) Social relations of males and
infants in a troop of Japanese monkeys: An examination of determinants. In DM Taub (ed): Primate Paternalism: An Evolutionary and
Comparative View of Male Investment. New York
Van Nostrand, pp. 127-145.
Gouzoules, H, Gouzoules, S, and Fedigan, L (1982)
Behavioural dominance and reproductive success
in female Japanese monkeys (Macaca fuscata).
Anim. Behav. 30:1138-1150.
Gouzoules, H, Gouzoules, S, and Marler, P (In press)
External reference in mammalian vocal communication. In G Zivin (ed): The Development of Expressive Behavior: Biology-Environment Interactions. New York: Academic Press.
130
YEARBOOK OF PHYSICAL ANTHROPOLOGY
Gouzoules, S (1981) Social Relationships of Adult
Female Japanese Monkeys (Macaca fuscata). Ph.D.
dissertation, University of Chicago.
Gouzoules, S, Gouzoules, H, and Marler, P (1984)
Rhesus monkey (Macaca mulatta) scream vocalizations: Representational signaling in the recruitment of agonistic aid. Anim. Behav. 32r182-193.
Grau, H J (1982) Kin recognition in white-footed
deermice (Peromyscus leucopus). Anim. Behav.
30~497-505.
Greenberg, L (1979)Genetic component of bee odor
in kin recognition. Science 206:1095-1097.
Greenwood, P J (1980) Mating systems, philopatry,
and dispersal in birds and mammals. Anim. Behav .28:1140-1162.
Hadidian, J, and Bernstein, IS (1979)Female reproductive cycles and birth data from an Old World
monkey colony. Primates 20:429-442.
Hall, KRL (1965)Behaviour and ecology of the wild
patas monkey Erythrocebus patas, in Uganda. In
PC Jay (ed): Primates: Studies in Adaptation and
Variability. New York: Holt, Rinehart and Winston, pp. 32-119.
Hamilton, WD (1964) The genetical evolution of
social behaviour, I and 11. J. Theor. Biol. 7:l-51.
Hamilton, WJ, Busse, C, and Smith, KS (1982)
Adoption of infant orphan chacma baboons. Anim.
Behav. 30:29-34.
Harcourt, AH (1978) Strategies of emigration and
transfer by primates, with particular reference to
gorillas. Z. Tierpsychol. 48t401-420.
Harcourt, AH (1979) Social relationships among
adult female mountain gorillas. Anim. Behav.
27:251-264.
Harcourt, AH, and Stewart, K (1981) Gorilla male
relationships: Can differences during immaturity
lead to contrasting reproductive tactics in adulthood? Anim. Behav. 29:206-210.
Harcourt, A, Stewart, K, and Fossey, D (1976)Male
emigration and female transfer in wild mountain
gorilla. Nature 263t226-227.
Harrington, J (1978) Diurnal behavior of Lemur
mongoz at Ampijoroa, Madagascar. Folia Primatol. 29:291-302.
Hasegawa, T, and Hiraiwa, M (1980) Social interactions of orphans observed in a free-ranging troop
of Japanese monkeys. Folia Primatol. 33t129-158.
Hausfater, G, Altmann, J, and Altmann, SA (1982)
Long-term consistency of dominance relations
among female baboons (Papio cynocephdus). Science 2175'52-755.
Hinde, RA (1976a) Interactions, relationships and
social structure. Man. 11:l-17.
Hinde, RA (1976b) On describing relationships. J.
Child Psychol. Psychiatry. 17:l-19.
Holmes, WG, and Sherman, PW (1982) The ontogeny of kin recognition in two species of grounh
squirrels. Am. 2001. 2:491-517.
Holmes, WG, and Sherman, PW (1983) Kin recognition in animals. Am. Sci. 71t46-55.
Hoogland, JL (1982) Prairie dogs avoid extreme
inbreeding. Science 215: 1639-1641.
Hoogland, JL (1983)Nepotism and alarm calling in
the black-tailed prairie dog (Cynomys ludouicianus). Anim. Behav. 31:472-480.
Horr, D (1977)Orang-utan maturation: growing up
in a female world. In S. Chevalier-Skolnikoff and
FE Poirier (eds): Primate Bio-Social Development.
New York: Garland Publishing Co., pp. 289-322.
Horrocks, J, and Hunte, W (1983) Maternal rank
and offspring rank in vervet monkeys: An ap-
[Vol. 27, 1984
praisal of the mechanisms of rank acquisition.
Anim. Behav. 31t772-782.
Hrdy, S (1974) Male-male competition and infanticide among the langurs (Presbytis entellus) of Abu,
Rajasrhan. Folia Primatol. 22t19-58.
Hrdy, SB (1976) Care and exploitation of nonhuman primate infants by conspecifics other than
the mother. Adv. Stud. Behav. 6t101-158.
Hrdy, SB (1977) The Langurs of Abu: Female and
Male Strategies of Reproduction. Cambridge: Harvard University Press.
Hrdy, SB (1979) Infanticide among animals: A review, classification, and examination of the implications for the reproductive strategies of females.
Ethol. Sociobiol. 1:13-40.
Hrdy, SB, and Hrdy, DB (1976) Hierarchical relations among female Hanuman langurs (Primates:
Colobinae, Presbytis entellus). Science 193:913915.
Imanishi, K (1961) The origin of the human familya primatological approach. Jpn. J. Ethnol. 24;119130.
Itani, J (1959) Paternal care in the wild Japanese
monkey (Macaca fuscata). Primates 2t61-93.
Itani, J (1965) On the acquisition and propagation
of a new food habit in the troop of Japanese monkeys at Takasakijama. In K Imanishi and SA
Altmann (eds): Japanese Monkeys. Atlanta:
Emory University Press, pp. 52-65.
Itani, J, and Nishimura, A (1973) The study of
infra-human culture in Japan. In EW Menzel (ed):
Precultural Primate Behavior. Vol. 1. Basel: Karger, pp. 26-50.
Izawa, K (1976) Group sizes and compositions of
monkeys in the upper Amazon basin. Primates
17t367-399.
Izawa, K, Kamura, K, and Nieto, AS (1979) Grouping of the wild spider monkey. Primates. 20:
503-512.
Jay, P (1965) The common langur in northern India. In I DeVore (ed): Primate Behavior: Field
Studies of Monkeys and Apes. New York: Holt,
Rinehart and Winston, pp. 197-249.
Jolly, A (1966) Lemur Behavior. Chicago: University of Chicago Press.
Jolly, A (1967)Breeding synchrony in Lemur catta.
In SA Altmann (ed): Social Communication
Among Primates. Chicago: University of Chicago
Press, pp. 3-14.
Judge, P (1983) Reconciliation based on kinship in
a captive group of pigtail macaques. Am. J. Primatol. 4:346(Abstract).
Kaplan, J (1977) Patterns of tight interference in
free-ranging rhesus monkeys. Am. J. Phys. Anthropol. 47t279-287.
Kaplan, J (1978)Fight interference and altruism in
rhesus monkeys. Am. J. Phys. Anthropol. 49:
241-249.
Kawai, M (1965) On the system of social ranks in a
natural troop of Japanese monkeys. I. Basic rank
and dependent rank. In K Imanishi and SA Altmann (eds): Japanese Monkeys. Atlanta: Emory
University Press, pp. 66-86.
Kawai, M, Asuma, S, and Yoshiba, K (1967)Ecological studies of reproduction in Japanese monkeys
(Macaca fuscata). I. Problems of the birth season.
Primates 8t36-73.
Kawai, M, Dunbar, R, Ohsawa, H, and Mori, U
(1983) Social organization of gelada baboons: Social units and definitions, Primates 24t13-24.
Kawamura, S (1959) The process of sub-culture
Gouzoules]
PRIMATE K I N RECOGNITION
propagation among Japanese monkeys. Primates
2r43-54.
Kawamura, S (1965) Matriarchial social ranks in
the Minoo-B troop: A study of the rank system of
Japanese monkeys. In K Imanshi and SA Altmann (eds): Japanese Monkeys. Atlanta: Emory
University Press, pp. 105-112.
Kinzey, W (1977) Diet and feeding behaviour of
Callicebus torquatus. In TH Clutton-Brock (ed):
Primate Ecology: Studies of Feeding and Ranging
Behaviour in Lemurs, Monkeys and Apes. New
York Academic Press, pp, 127-152.
Kinzey, W, Rosenberger, A, Heisler, P, Prowse, D,
and Trilling, J (1977) A preliminary field investigation of the yellow handed Titi monkey, Callice
bus torquatus torquatus, in northern Peru.
Primates 18:159-182.
Kleiman, D (1977) Monogamy in mammals. Rev.
Biol. 52:39-69.
Kleiman, D (1979) Parent-offspring and sibling
competition in a monogamous primate. Am. Nat.
114:753-760.
Kleiman, D, and Malcolm, JR (1981) The evolution
of male parental investment in mammals. In DJ
Gubernick and PH Klopfer (eds): Parental Care in
Mammals. New York: Plenum Press, pp. 347-388.
Klein, L (1974) Agonistic behavior in neotropical
primates. In RL Holloway (ed): Primate Aggression, Territoriality and Xenophobia. New York:
Academic Press, pp. 77-122.
Klein, L and Klein, D (1975) Social and ecological
contrast between four taxa of neotropical primates. In RH Tuttle (ed): Socioecology and Psychology of Primates. The Hague: Mouton Press,
pp. 59-85.
Koyama, N (1967) On dominance rank and kinship
of a wild Japanese monkey troop in Arashiyama.
Primates 8:189-216.
Koyama, N (1970)Changes in dominance rank and
division of a wild Japanese monkey troop in Arashiyama. Primates 11:335-390.
Kukuk, PF, Breed, MD, Sobti, A, and Bell, WJ
(1977)The contributions of kinship and conditioning to nest recognition and colony member recognition in a primitively eusocial bee, Lasioglossum
zephyrurn (Hymenophera: Halicitidae). Behav.
Ecol. Sociobiol. 2:319-327.
Kummer, H (1968) Social Organization of Hamadryas Baboons. Chicago: University of Chicago
Press.
Kummer, H (1975)Rules of dyad and group formation among captive gelada baboons. Proc. Symp.
5th Congr. Int. Primat. Sac. 1974, pp. 129-159.
Kurland, JA (1977) Kin selection in the Japanese
monkey. Contributions to Primatology, Vol. 12.
Basel: S. Karger.
Labov, JB (1982) Factors influencing infanticidal
behavior in wild male house mice ( M u s musculus).
Behav. Ecol. Sociobiol. 6r297-304.
Lacy, RC, and Sherman, PW (1983)Kin recognition
by phenotype matching. Am. Nat. 121:489-512.
Lee, PC, and Oliver, JI (1979) Competition, dominance and the acquisition of rank in juvenile yellow baboons (Papio cynocephalus). Anim. Behav.
27:576-585.
Levi-Strauss, C (1970) The Elementary Structures
of .Kinship. London: Social Science Paperbacks.
Lindburg, D (1971) The rhesus monkey in North
India: an ecological and behavioral study. In LA
Rosenblum (ed): Primate Behavior. Vol. 2. New
York: Academic Press, pp. 2-106.
131
Lay, J (1981) The reproductive and hetero-sexual
behaviours of adult patas monkeys in captivity.
Anim. Behav. 29:714-726.
MacKinnon, J (1974) The behaviour and ecology of
wild orang-utans, Pongo pygmaeus. Anim. Behav.
223-74.
MacKinnon, J (1979)Reproductive behavior in wild
orangutan populations. In DA Hamburg and ER
McCown (eds): The Great Apes. Menlo Park, CA:
The BenjamidCummings Publ. Co., pp. 257-274.
Marsh, C (1979) Female transfer and mate choice
among Tana River red colobus. Nature 281:
568-569.
Martin, RD (1972) A preliminary field study of the
lesser mouse lemur (Microcebus murinus, JF
Miller 1777).Z. Tierpsychol. [Suppl.]9:43-89.
Martin, RD (1973) A review of the behaviour and
ecology of the lesser mouse lemur (Microcebus murinus, JF Miller 1777). In RP Michael and JH
Crook (eds): Comparative Ecology and Behaviour
of Primates. New York Academic Press. pp. 2-68.
Massey, A (1977) Agonistic aids and kinship in a
group of pigtail macaques. Behav. Ecol. Sociobiol.
2:31-40.
Massey, A (1979) Reply t o Kurland and Gaulin,
1979. Behav. Ecol. Sociobiol. 6%-83.
McArthur, PD (1982) Mechanisms and development of parent-young vocal recognition in the pinon jay (Gymnorhinus cyanocephalus). Anim.
Behav. 30:62-74.
McKenna, JJ (1979)The evolution of allomothering
behavior among Colobine monkeys: Function and
opportunism in evolution. Am. Anthropol. 81;
818-840.
McLean, IG (1982)The association of female kin in
the arctic ground squirrel Spermophilus purr@.
Behav. Ecol. Sociobiol. 10:91-100.
McLean, IG (1983) Paternal behaviour and killing
of young in arctic ground squirrels. Anim. Behav.
31:32-44.
McMillan, CA (1979) Genetic differentiation of female lineages in rhesus macaques on Cay0 Santiago. Am. J. Phys. Anthropol. 5Ot461-462.
McMillan, CA (1980)The possibility of selection as
a factor in the patterning of genetic distances
between matrilineages of rhesus monkeys on Cay0
Santiago. Am. J. Phys. Anthropol. 52:251-252.
McMillan, C, and Duggleby, C (1981) Interlineage
genetic differentiation among rhesus macaques
on Cay0 Santiago. Am. J. Phys. Anthropol.
52:305-312.
Meikle, DB, and Vessey, SH (1981) Nepotism among
rhesus monkey brothers. Nature 294:160-161.
Melnick, D, and Kidd, KK (1983) The genetic consequences of social group fission in a wild population of rhesus monkeys (Macaca mulatta). Behav.
Ecol. Sociobiol. 12:229-236.
Michener, G (1983) Kin identification, matriarchies, and the evolution of sociality in grounddwelling sciurids. In JF Eisenberg and DG Kleiman: Advances in the Study of Mammalian Behaviour. Special Publication of the American
Society of Mammalogists, pp. 528-572.
Miller, GA, and Johnson-Laird, PN (1976) Language and Perception. Cambridge: Harvard University Press.
Missakian, EA (1972) Genealogical and cross-genealogical dominance relations in a group of freeranging rhesus monkeys (Macaca mulatta) on
Cay0 Santiago. Primates 13t169-180.
Missakian, EA (1973a) Genealogical mating activ-
132
YEARBOOK OF PHYSICAL ANTHROPOLOGY
ity in free-ranging groups of rhesus monkeys (Macaca mulatta) on Cay0 Santiago. Behaviour
45:224-240.
Missakian. EA (1973b) The timing of fission among
free-ranging rhesus monkeys. Am. J. Phys. Anthropol. 38:621-624.
Moore, JJ (1978) Dominance relations among freeranging female baboons at Gombe National Park,
Tanzania. In D Chivers and J Herbert (eds): Recent Advances in Primatology, Vol. I. Behaviour.
London: Academic Press, pp. 67-70.
Mori, U (1979) Development of sociability and social status. In M Kawai (ed): Ecological and Sociological Studies of Gelada Baboons. Contrib.
Primatol. 16:125-155.
Moynihan, M (1976) The New World Primates.
Princeton, New Jersey: Princeton University
Press.
Nash, LT (1976) Troop fission in free-ranging baboons in the Gombe Stream National Park, Tanzania. Am. J. Phys. Anthropol. 4:63-78.
Neville, MK (1972) Social relations within troops of
red howler monkeys (Abuatta seniculus). Folia
Primatol. 18t47-77.
Neyman, P (1977) Aspects of the ecology and social
organization of free-ranging cotton-top tamarins
(Saguinus oedipus) and the conservation status cf
the species. In D Kleiman (ed): The Biology and
Conservation of the Callitrichidae. Washington,
DC: Smithsonian Institution Press, pp. 39-71.
Nishida, T (1979) The social stucture of chimpanzees on the Mahali Mountains. In D Hamburg and
ER McCown (eds): The Great Apes. Perspectives
on Human Evolution, Vol. 5. Menlo Park: BenjamidCummings Publ. Co., pp. 73-121.
Nishida, T (1983) Alloparental behavior in wild
chimpanzees of the Mahale mountains, Tanzania.
Folia Primatol. 41:l-33.
Norikoski, K, and Koyama, N (1974) Group shifting
and social organization among Japanese monkeys. In S Kondo, M Kawai, A Ehara, and S.
Kawamura (eds): Proceedings of the Symposium
of the Fifth International Primatology Society.
Tokyo: Japan Science Press, pp. 43-61.
Oates, JF (1977)The social life of a black-and-white
colobus monkey, Colobus quereza. Z. Tierpsychol.
45:l-60.
Ober, CL, Buettner-Janusch, J, and Olivier, TJ
(1979) Genetic differentiation between matrilines
in the Cay0 Santiago macaque groups Am J
Phys Anthropol 50 468
O’Hara, RK, and Blaustein, AR (1981) Kin preference behavior in Bufo boreas tadpoles. Behav.
Ecol. Sociobiol. I1:43-50.
Ohsawa, H (1979) The local gelada population and
environment of the Gich area. In M Kawai (ed):
Ecological and Sociological Studies of Gelada Baboons. Contributions to Primatology, Vol. 16.
Basel: S. Karger, pp. 4-46.
Olivier, TJ, Ober, CL, Buettner-Janusch, J, and
Sade, DS (1981) Genetic differentiation among
rnatrilines in social groups of rhesus monkeys.
Behav. Ecol. Sociobiol. 8t279-285.
Orians, G (1969) On the evolution of mating systems in birds and mammals. Am. Nat. 103t589603.
Packer, C (1979a) Intertroop transfer and inbreeding avoidance in Papio anubis. Anim. Behav. 27:
1-36.
Packer, C (1979b) Male dominance and reproductive activity in Papio anubis. Anim. Behav.
[Vol. 27, 1984
27(1):37-45.
Packer, C (1980) Male care and exploitation of infants in Pabio anubis. Anim. Behav. 29:512-520.
Packer, C, and Pusey, A (1979) Female aggression
and male membership in troops of Japanese macaques and olive baboons. Folia Primatol. 31:
212-218.
Petter, JJ (1975) The lemurs of Madagascar. In I
DeVore (ed): Primate Behavior. New York Holt,
Rinehart and Winston, pp. 292-319.
Pfennig, DW, Reeve, HK, and Shellman, JS (1983)
Learned component of nestmate discrimination in
workers of a social wasp, Polistes fuscatus (Hymenoptera: Vespidae). Anim. Behav. 31:412-416.
Poirier, F (1968) The Nilgiri langur (Presbytisjohnii)
mother-infant dyad. Primates 9:45-68.
Poirier, F (1970a) The Nilgiri langur (Presbytis
johnii) of South India. In LA Rosenblum (ed): Primate Behavior, Vol. 1. New York: Academic Press,
pp. 254-283.
Poirier, F (1970b) Dominance structure of the Nilgiri langur (Presbytisjohnii) of South India. Folia
Primatol. 12161-186.
Pollack, JI (1979) Female dominance in Indiri indri. Folia Primatol. 31t143-164.
Porter, RH, and Wyrick, M (1979) Sibling recognition in spiny mice (Acomys cahirinus): Influence
of age and isolation. Anim. Behav. 27:761-766.
Porter, RH, Wyrick, M, and Pankey, J (1978) Sibling recognition in spiny mice (Acomys cahirinus).
Behav. Ecol. Sociobiol. 3t61-68.
Porter, RH, Matochik, JA, and Makin, JW (1983)
Evidence for phenotypic matching in spiny mice
(Acomys cahirinus). Anim. Behav. 31:978-984.
Pusey, A (1979) Intercommunity transfer of chimpanzees in Gombe National Park. In DA Kamburg and ER McCown (eds): The Great Apes.
Perspectives on Human Evolution, Vol. 5. Menlo
P a r k BenjamidCummings Publ. Co., pp. 465-479.
Pusey, A (1980) Inbreeding avoidance in chimpanzees. Anim. Behav. 28543-582.
Pusey, A (1983) Mother-offspring relationships in
chimpanzees after weaning. Anim. Behav. 31:
363-377.
Ralls, K (1977) Sexual dimorphism in mammals:
Avian models and unanswered questions. Am.
Nat. 111:917-938.
Ransom, TW, and Ransom, BS (1971) Adult maleinfant relations among baboons (Papio anubis).
Folia Primatol. 16179-195,
Ransom, TW, and Rowell, TE (1972) Early social
development of feral baboons. In FE Poirier (ed):
Primate Socialization. New York: Random House,
pp. 105-144.
Redican, WK (1976) Adult male-infant interactions
in nonhuman primates. In ME Lamb (ed): The
Role of the Father in Child Development. New
York John Wiley and Sons, pp. 345-385.
Richard, A (1974) Intra-specific variation in the
social organization and ecology of Propithecus uerreauxi. Folia Primatol. 22178-207.
Richard, A, and Schulman, S (1982) Sociobiology:
Primate field studies. Annu. Rev. Anthropol.
llt231-255.
Rijksen, HD (1981) Infant killing: A possible consequence of a disputed leader role. Behaviour
78: 138-168.
Rodman, P (1973) Population composition and
adaptive organization among orangutans of the
Kutai Reserve. In RP Michael and JH Crook (eds):
Comparative Ecology and Behavior of Primates.
Gouzoules]
PRIMATE KIN RECOGNITION
New York: Academic Press, pp. 171-209.
Rodman, P (1979) Individual activity patterns and
the solitary nature of orangutans. In DA Hamburg and ER McCown (eds): The Great Apes.
Menlo Park: BenjamidCummings Publ. Co., pp.
235-256.
Rondinelli, R, and Klein, LL (1976) An analysis of
adult social spacing tendencies and related social
interactions in a colonv of suider monkevs (Ateles
geoffroyi) at the San Francisco Zoo. Folia Primatol. 25122-142.
Roonwal, ML, and Mohnot, SM (1977) Primates of
South Asia. Cambridge: Harvard University
Press.
Rosenblum, L (1971) Kinship interaction patterns
in pigtail and bonnet macaques. In: Proc. Third
Int. Congr. Primatol., Zurich, 1970, Vol. 3. New
York: S. Karger, pp. 79-84.
Ross, NM, and Gamboa, GJ (1981) Nestmate discrimination in social wasps (Polistes metricus, Hymenoptera: Vespidae). Behav. Ecol. Sociobiol.
9: 163-165.
Rowell, TE (1973) Social organization of wild talapoinmonkeys. Am. J. Phys. Anthropol. 38:593-598.
Rowell, TE, and Olson, DK (1983) Alternative
mechanisms of organization in monkeys. Behaviour 86:3 1-54.
Rudran, R (1973) Adult male replacement in onemale troops of purple-faced langurs (Presbytis sener senex) and its effect on population structure.
Folia Primatol. 29:166-192.
Rudran, R (1979) The demography and social mobility of a red howler (Alouatta seniculus) population in Venezuela. In JF Eisenberg (ed):Vertebrate
Ecology in the Northern Neotropics. Washington,
DC: Smithsonian Institution Press, pp. 107-126.
Sade, DS (1965) Some aspects of parent-offspring
and sibling relations in a group of rhesus monkeys, with a discussion of grooming. Am. J. Phys.
Anthropol. 23:l-18.
Sade, DS (1967) Determinants of dominance in a
group of free-ranging rhesus monkeys. In SA Altmann (ed): Social Communication Among Primates. Chicago: University of Chicago Press, pp.
99-114.
Sade, DS (1968) Inhibition of mother-son mating
among free-ranging rhesus monkeys. Sci. Psychoanal. 12:18-38.
Sade, DS (1972) A longitudinal study of social behavior of rhesus monkeys. In RH Tuttle (ed): The
Functional and Evolutionary Biology of Primates.
Chicago: Aldine, pp. 378-398.
Sekulic, R (1982) Behavior and ranging patterns of
a solitary female red howler (Alouatta seniculus).
Folia Primatol. 38:217-232.
Seyfarth, RM (1976) Social relationships among
adult female baboons. Anim. Behav. 24:917-938.
Seyfarth, RM (1977) A model of social grooming
among adult female monkeys. J. Theor. Biol.
65t671-698.
Seyfarth, RM (1980) The distribution of grooming
and related behaviours among adult female vervet
monkeys. Anim. Behav. 28.798-813.
Seyfarth, RM, Cheney, DL, and Hinde, RA (1978)
Some principles relating individual behavior and
social structure in primates. In D Chivers and J
Herbert (eds): Recent Advances in Primatology.
New York: Academic Press, pp. 39-51.
Sherman, P (1978) A comparative review of the
Langurs of Abu (SB Hrdy) and Kin Selection in
the Japanese Monkey (JA Kurland). Q. Rev. Biol.
133
53t491-492.
Sherman, P (1980) The limits of ground squirrel
nepotism. In GW Barlow and J Silverberg (eds):
Sociobiology: Beyond Nature Nurture? Boulder:
Westview Press, pp. 505-544.
Sherman, PW (1981) Kinship, demography, and
Belding's ground squirrel nepotism. Behav. Ecol.
Sociobiol. 8t251-260.
Sigg, H, Stolba, A, Abegglen, J-J, and Dasser, V
(1982) Life history of hamadryas baboons: physical development, infant mortality, reproductive
parameters and family relationships. Primates
23:473-487.
Silk, JB (1982) Altruism among female Macaca rudiata: Explanations and analysis of patterns of
grooming and coalition formation. Behaviour
79:162-188.
Silk, J, Samuels, A, and Rodman, P (1981) The
influence of kinship, rank, and sex on affiliation
and aggression between adult female and immature bonnet macaques (Macaca radiata). Behaviour 78:lll-177.
Silk, JB,and Boyd, R (1983) Cooperation, competition, and mate choice in matrilineal macaque
groups. In SK Wasser (ed): Social Behavior of Female Vertebrates. New York: Academic Press, pp.
315-347.
Small, MF, and Smith, DG (1981)Interactions with
infants by full siblings, paternal half-siblings, and
nonrelatives in a captive group of rhesus macaques(Macaca mulatta). Am. J. Primatol. 1t91-94.
Smith, DG (1982a) A test of the randomness of
paternity of members of maternal sibships in six
captive groups of rhesus monkeys (Macaca mulatta). Int. J. Primatol. 3:461-468.
Smith, DG (198213) Inbreeding in three captive
groups of rhesus monkeys. Am. J. Phys. Anthropol. 58t447-451.
Stacey, P (1982) Female promiscuity and male reproductive success in social birds and mammals.
Am. Nat. 1205-64.
Stammbach, E (1978) On social differentiation in
groups of captive female hamadryas baboons. Behaviour 67:322-338.
Strum, S (1983) Use of females by male olive baboons (Papio anubis). Am. J. Primatol. 5t93-110.
Struhsaker, 'IT (1967) Social structure among
vervet monkeys (Cercopithecus aethiops). Behaviour 29:6-12 1.
Struhsaker, 'IT (1975) The Red Colobus Monkey.
Chicago: University of Chicago Press.
Struhsaker, 1T (1977) Infanticide and social organization in the redtail monkey (Cercopithecus QScanius schmidti) in the Kibale Forest, Uganda. Z.
Tierpsychol. 45:75-84.
Struhsaker, 'IT (1983) Infanticide in a patrilineal
society of red colobus monkeys. Paper presented
at the 18th Int. Ethol. Conf., Brisbane, Australia.
Struhsaker, TT,and Gartlan, SS (1970) Observations on the behavior and ecology of the patas
monkey. J. 2001. 161r49-63.
Struhsaker, 'IT, and Leland, L (1979) Socioecology
of five sympatric monkey species in the Kibale
Forest, Uganda. Adv. Stud. Behav. 9t159-228.
Sugiyama, Y (1967) Social organization of Hanuman langurs. In SA Altmann (ed): Social Communication Among Primates. Chicago: University
of Chicago Press, pp. 207-219.
Sugiyama, Y (1971)Characteristics of the social life
of bonnet macaques (Macaca radiata). Primates
12:247-266.
134
YEARBOOK OF PHYSZCAL ANTHROPOLOGY
Sugiyama, Y (1976) Life history of male Japanese
monkeys. In JS Rosenblatt, RA Hinde, E Shaw,
and C Beer (eds): Advances in the study of Behavior, Vol. 7. New York: Academic Press, pp. 25-284.
Takahata, Y (1982) The socio-sexual behavior of
Japanese monkeys. Z. Tierpsychol. 59239-108.
Tattersall, I (1976) Group structure and activity
rhythm in Lemur mongoz (Primates, Lemuriformed on Anjouan and Moheli Islands, Comoro
Archipelago. Anthropol. Papers Am. Mus. Nat.
History 53t367-380.
Taub, D (1980) Female choice and mating strategies among wild Barbary macaques (Mucaca syluanus LJ. In D Lindburg (ed): The Macaques:
Studies in Ecology, Behavior and Evolution. New
York: Van Nostrand Reinhold, pp. 287-344.
Tenaza, R (1975) Territoriality and monogamy
among Kloss’ gibbons (Hylobates klossii) in Siberut Island, Indonesia. Folia Primatol. 24t68-80.
Tenaza, R (1976) Songs, choruses and countersigning of Kloss’ gibbons (Hylobates Klossii) in Siberut
Island. Z. Tierpsychol. 4Ot37-52.
Tilson, RL (1981) Family formation of Kloss’ gibbons. Folia Primatol. 35:237-312.
Tokuda, K (1961-1962) A study on the sexual behavior in the Japanese monkey troop. Primates
3:l-40.
Tokuda, K, Simons, RC, and Jensen, GD (1968)
Sexual behavior in a captive group of pigtailed
monkeys (Macaca nemstrina). Primates 9t283-294.
Tutin, C (1979) Mating patterns and reproductive
strategies in a community of wild chimpanzees
(Pan troglodytes schweinfurthii). Behav. Ecol. Sociobiol. 6t29-38.
Tutin, CEG, McGrew, WC, and Baldwin, PJ (1983)
Social organization of savanna-dwelling chimpanzees, Pan troglodytes uerus, a t Mt. Assirik, Senegal. Primates 24t154-173.
Vehrencamp, SL (1979) The roles of individual, kin,
and group selection in the evolution of sociality.
In P Marler and JG Vandenbergh (eds): Handbook
of Behavioral Neurobiology, Vol. 3, Social Behavior and Communication. New York: Plenum Press,
pp. 351-394.
Waal, F de (1977) The organization of agonistic
relations within two captive groups of Java-monkeys (Macaca fascicularis). 2. Tierpsychol.
[Vol. 27, 1984
441:225-282.
Waldman, B (1981) Sibling recognition in toad tadpoles: the role of experience. Z. Tierpsychol.
56:341-358.
Walters, J (1980) Interventions and the development of dominance relationships in female baboons. Folia Primatol. 34:61-89.
Walters, J (1981) Inferring kinship from behaviour:
Maternity determinations in yellow baboons.
Anim. Behav. 29r126-136.
Waser, PM, and Jones, WT (1983) Natal philopatry
among solitary mammals. Q. Rev. Biol. 58:
355-390.
Watanabe, K (1979) Alliance formation in a freeranging troop of Japanese macaques. Primates
20:459-474.
Whitten, PL (1983) Diet and dominance among female vervet monkeys (Cercopithecus aethiops).
Am. J. Primatol. 5139-160.
Wittenberger, J (1979) The evolution of mating systems in birds and mammals. In P Marler and JG
Vandenbergh (eds): Handbook of Behavioral Neurobiology, Vol. 3, Social Behavior and Communication. New York: Plenum, pp. 271-350.
Wittenberger, J (1980) Group size and polygamy in
social mammals. Am. Nat. I15t197-222.
Wittenberger, JF,and Tilson, R (1980) The evolution of monogamy: A theoretical overview. Annu.
Rev. Ecol. Syst. 11t197-232.
Wolf, K, and Fleagle, J (1977) Adult male replacement in a group of silvered leaf monkeys (Presbytis cristata) at Kuala Selangor, Malaysia. Primates
18:949-955.
Wrangham, R (1979) Sex differences in chimpanzee
dispersion. In DA Hamburg and ER McCown (eds):
The Great Apes. Menlo Park: BenjamidCummings Publ. Co., pp. 481-490.
Wrangham, R (1980) An ecological model of femalebonded primate groups. Behaviour 75269-299.
Wu, H, Holmes, WG, Medina, SR, and Sackett, GP
(1980) Kin preference in infant Macaca nemestrina. Nature 285t225-227.
Yamada, M (1963) A study of blood-relationship in
the natural society of the Japanese macaque: an
analysis of co-feeding, grooming, and playmate
relationships in Minoo-B troop. Primates 4:43-65.
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