Biol. Rev. (2007), 82, pp. 319–334.

319
doi:10.1111/j.1469-185X.2007.00011.x

Paternal kin discrimination: the evidence

and likely mechanisms
Anja Widdig1,2,3,*
1
Max Planck Institute for Evolutionary Anthropology, Department of Primatology, Deutscher Platz 6,
D-04103 Leipzig, Germany
2
Department of Biology, Duke University, P.O. Box 90338, Durham NC 27708, USA
3
Caribbean Primate Research Center, P.O. Box 906, Punta Santiago, PR 00741, USA

(Received 17 July 2006; revised 17 January 2007; accepted 30 January 2007)

ABSTRACT

One of the most important assumptions of kin selection theory is that individuals behave differently towards kin
than non-kin. In mammals, there is strong evidence that maternal kin are distinguished from non-kin via
familiarity. However, little is known about whether or not mammals can also recognize paternal kin as many
female mammals, including primates, mate with multiple males near the time of conception, potentially
concealing paternal kinship. Genetic data in several mammalian species with a promiscuous mating system and
male-biased dispersal reveal a high skew in male reproduction which leads to co-residing paternal half-siblings. In
most primates, individuals also form stable bisexual groups creating opportunities for males to interact with their
offspring. Here I consider close paternal kin co-resident in the same social group, such as father-offspring and
paternal half-siblings (i.e. animals sharing the same father but who were born to different mothers) and review
mammalian studies of paternal kin discrimination. Furthermore, I summarize the most likely mechanisms of
paternal kin discrimination (familiarity and phenotype matching). When familiarity is the underlying mechanism,
mothers and/or the sire could mediate familiarity among paternal half-siblings as well as between fathers and
offspring assuming mothers and/or fathers can assess paternity. When animals use phenotype matching, they
might use their fathers’ template (when the father is present) or self (when the father is absent) to assess paternal
kinship in others. Available evidence suggests that familiarity and phenotype matching might be used for paternal
kin discrimination and that both mechanisms might apply to a wide range of social mammals characterized by
a high skew in male reproduction and co-residence of paternal kin. Among primates, suggested evidence for
phenotype matching can often have an alternative explanation, which emphasizes the crucial importance of
controlling for familiarity as a potential confounding variable. However, the mechanism/s used to identify
paternal kin might differ within a species (as a function of each individual’s specific circumstances) as well as
among species (depending upon the key sensory modalities of the species considered). Finally, I discuss the
possible cues used in paternal kin discrimination and offer suggestions for future studies.

Key words: paternal kin discrimination, mammals, primates, familiarity, phenoytype matching, recognition
cues.

CONTENTS
I. Introduction ...................................................................................................................................... 320
II. Conditions influencing the availability and interactions of paternal kin ........................................ 321
III. The impact of paternal kinship on social behaviour ....................................................................... 322
(1) Paternal kin bias in mammals .................................................................................................... 322
( a ) Inbreeding avoidance ............................................................................................................ 322

*Address for correspondence: Tel: ]49 (0) 341 3550 233; Fax: ]49 (0) 341 3550 299. E-mail: anja.widdig@eva.mpg.de

Biological Reviews 82 (2007) 319–334 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society
320 Anja Widdig

( b ) Affiliation and aggression ...................................................................................................... 322

( c ) Paternal care ......................................................................................................................... 322
( d ) Offspring protection against infanticide ............................................................................... 322
(2) Paternal kin bias in primates ...................................................................................................... 322
( a ) Inbreeding avoidance ............................................................................................................ 323
( b ) Affiliation ............................................................................................................................... 323
( c ) Dyadic aggression ................................................................................................................. 324
( d ) Coalition formation ............................................................................................................... 324
( e ) Offspring protection against infanticide ............................................................................... 324
IV. Mechanisms of kin discrimination ................................................................................................... 324
(1) Familiarity ................................................................................................................................... 324
( a ) Familiarity among paternal half-siblings via age proximity ................................................ 324
( b ) Familiarity among paternal half-siblings mediated by mothers .......................................... 325
( c ) Familiarity among paternal half-siblings mediated by a common father ........................... 325
(2) Phenotype matching ................................................................................................................... 327
( a ) Using the father as a template to match potential paternal half-siblings ........................... 327
( b ) Using self as a template to match potential paternal half-siblings ........................... 327
(3) Familiarity and/or phenotype matching? .................................................................................. 327
V. Cues potentially used in kin discrimination ..................................................................................... 328
(1) Odour .......................................................................................................................................... 328
(2) Appearance ................................................................................................................................. 328
(3) Vocalization ................................................................................................................................. 329
(4) Personality ................................................................................................................................... 329
VI. Conclusions ....................................................................................................................................... 329
VII. Acknowledgements ............................................................................................................................ 329
VIII. References ......................................................................................................................................... 330

I. INTRODUCTION
Across the mammalian order there is evidence that animals
form differentiated relationships with one another which
may be achieved by direct recognition of kin or shared
spatial proximity. Kin selection theory predicts that animals
can increase their fitness by allocating more cooperation to
kin than to non-kin (Hamilton, 1964). There is widespread
evidence of nepotism (i.e. favouring kin: Sherman, 1980) in
behaviour across a broad range of mammalian taxa [e.g.
greater horsehoe bat, Rhinolophus ferrumequinum (Rossiter
et al., 2002), Belding’s ground squirrels, Spermophilus beldingi
(Sherman, 1981), African elephants, Loxodonta africana
(Archie, Moss & Alberts, 2006); reviewed in Dugatkin,
(1997)]. Furthermore, in some taxa, females increase their
fitness via associations with maternal kin [e.g. house mice, Mus
domesticus (Koenig, 1994; Dobson, Jacquot & Baudoin,
2000), wood mice, Apodemus sylvaticus (Gerlach & Bartmann,
2002), field vole, Microtus agrestis (Pusenius et al., 1998), grey
seals, Halichoerus gryphus (Pomeroy et al., 2001); reviewed for
primates in Chapais (2001) and Silk (2002)].
Less is known about paternal kinship (relatedness
through the father). In many mammalian species, including
primates, females mate with more than one male near the
time of conception (e.g. Anderson, 1994; Hare, Todd &
Untereiner, 2004; Engelhardt et al., 2006; reviewed in
Jennions & Petrie, 2000). In species with such a mating
system, paternity can only be revealed to human observers
via genetic techniques (e.g. Inoue et al., 1993). To date we do
not understand whether and how mammals assess paternity
and we only have limited information about the distribution
of paternal kinship within and across social groups (but see
e.g. Bradley et al., 2005, Widdig et al., 2006a). Furthermore,
little is known about the impact of paternal relatedness on
the evolution of mammalian social behaviour.
The inability to recognize paternal kin would greatly
limit the potential for kin selection and exposes individuals
to fitness costs (Hamilton, 1964). Selection should favour
paternal kin recognition for several reasons. First, the ability
to recognize paternal kin would minimize the risks of
paternal inbreeding (Pusey, 1987; Crnokrak & Roff, 1999;
Meagher, Penn & Potts, 2000; reviewed in Keller & Waller,
2002). Second, individuals that direct more cooperation
and less aggression to paternal kin compared to non-kin
would potentially increase their fitness (Hamilton, 1964;
West, Pen & Griffin, 2002). Third, paternal kin recognition
may enable males to protect their infants from infanticide
and prevent potentially infanticidal males from harming
their own infants (Borries et al., 1999a).
Chapais (2001) argues that the spatial proximity of
maternal kin that arises in matrilineal societies biases kin
towards cooperating with each other, so that maternal kin
biases in mutually beneficial interactions may reflect
natural selection, not kin selection. However, frequently
shared spatial proximity can not necessarily be expected
among paternal half-siblings, e.g. when they are born to
mothers which are maternally unrelated (and therefore less
affiliative) even when living in the same social group.
Therefore, evidence of paternal kin bias and the mecha-
nisms responsible for paternal kin discrimination are
important for our understanding of the evolution of social
behaviour (Silk 2002).

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Paternal kin discrimination 321

In this review, I focus on mammalian social systems
where we can expect paternal kin to interact. I then review
studies in mammals and primates that have looked at the
ability of animals to discriminate paternal kin from non-kin.
After summarizing the most likely mechanisms of paternal
kin discrimination (familiarity and phenotype matching), I
focus on the detailed primate literature to postulate how
these mechanisms could operate among some primate
species, and propose that some of the mechanisms may
generalize to other social mammals with similar mating and
dispersal patterns. Finally, I discuss cues likely to be used in
paternal kin discrimination by suggesting directions for
future research. I will only consider here close paternal kin
co-resident in the same social group, such as father-offspring
(degree of relatedness, r ¼ 0.5) and paternal half-siblings
(i.e. animals who share the same father but were born to
different mothers, r ¼ 0.25).
II. CONDITIONS INFLUENCING THE
AVAILABILITY AND INTERACTIONS OF
PATERNAL KIN
Only when social groups consist of both paternal kin and
non-kin is it relevant to ask whether animals preferentially
interact with paternal kin in comparison to non-kin. A
mammalian species favouring interactions with both
paternal kin and non-kin would have to live, even only
temporarily, in stable multi-male multi-female groups where
females mate with multiple males and male reproduction is
highly skewed towards a few sires (reviewed in Strier, 2004;
compare Holmes & Sherman, 1982; Sherman & Holmes,
1985). Skew in male reproduction is characteristic of a wide
range of mammalian species [e.g. Damaralad mole-rats,
Cryptomys damarensis (Cooney & Bennett, 2000), banded
mongooses, Mungo mungo (Cant, 2000), fallow deer, Dama
dama (Say, Naulty & Hayden, 2003), black rhinoceros,
Diceros bicornis (Garnier, Bruford & Goossens, 2001), spotted
hyenas, Crocuta crocuta (Engh et al., 2002), African lions,
Panthera leo (Packer et al., 1991), bottlenose dolphins, Tursiops
truncatus (Krützen et al., 2004), humpback whales, Megaptera
novaeangliae (Nielsen et al., 2001). Detailed genetic studies on
several primate species have also demonstrated considerable
skew in male reproduction, with a high proportion of
paternity assigned to high-ranking males (Table 1).
Patterns of dispersal will regulate the co-residence of kin
and duration of their association. In most mammals, the
males usually leave their natal group while females are
philopatric (Greenwood, 1980) and therefore females are
more likely to interact continuously with kin (both maternal
and paternal) and non-kin. By contrast, in species with male
philopatry, males should be more likely to live with paternal
kin. Unlike other mammals, most primates form stable
bisexual groups; therefore, a father’s presence creates the
opportunity to interact with his offspring (reviewed in van
Schaik & Paul, 1996). In species with high reproductive skew,
sex-biased dispersal limits the potential for reproduction

Table 1. Evidence for male reproductive skew in primates. Male skew measures the percentage of paternity assigned to group
males: the alpha male1, high-ranking males2 or the most successful sire regardless of rank3. Male breeding tenure represents either
mean years or the range of years males have been reported to stay in a non-natal group for breeding before they subsequently
disperse again. Note that male group tenure was assigned as permanent for species in which males are philopatric. Tenure for
rhesus macaques was taken from Manson (1995)4. If available, I cite more than one study per species.

Offspring of a
Paternal female mainly N offspring
Male Male breeding sibs close with different Seasonal with solved
Species skew (%) tenure (yrs) in age sires breeders paternity Reference
1
Long-tailed macaques 50–90 1–5 Yes 45 De Ruiter et al. (1994);
Macaca fascicularis Yes Yes J.R. de Ruiter (pers. comm.)
1
Savanna Baboons 81 1–7 Yes No 27 Altmann et al. (1996);
1
Papio cynocephalus 32 0.7 Yes Yes 208 Alberts et al. (2006)
1
Hanuman langurs 57 Yes Yes 29 Launhardt et al. (2001);
Semnopithecus entellus 0.5–1.7 Borries (2000)
Rhesus macaques 24 Yes Yes Yes 241 Widdig et al. (2002);
2
Macaca mulatta 80 247 Widdig et al. (2004)
2
Mandrills 76 3 Yes 193 Charpentier et al. (2005);
Mandrillus sphinx Yes Yes M.J.E. Charpentier (pers. comm.)
1
Capuchin monkeys 49 7–13 Yes Yes 41 Muniz et al. (2006);
Cebus apella No L. Muniz (pers. comm.)
2
Bonobos 50–70 Permanent Yes No 10 Gerloff et al. (1999)
Pan paniscus
1
Chimpanzees 35 Permanent No 14 Constable et al. (2001);
3
Pan troglodytes 33 Yes Yes 34 Vigilant et al. (2001)
1
Mountain Gorilla 85 Yes Yes No 48 Bradley et al. (2005);
Gorilla beringei Robbins & Robbins (2005)
2 or perman.

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322
between opposite-sex co-resident paternal half-siblings.
Likewise, male secondary transfer reduces the potential
for inbreeding between fathers and daughters (e.g. Starin,
2001).
Finally, demographic patterns such as interbirth interval
length relative to the duration of alpha male tenure affect
the probability that successive offspring of a given female
will be full- or half-siblings (Strier, 2004). Male breeding
tenure is relatively short in primate species with female
philopatry (Table 1). One consequence of short tenure and
high skew in male reproduction is that age cohorts tend to
be composed of paternal half-siblings (Altmann, 1979) (see
Table 1), and social groups are genetically substructured by
age (Altmann et al., 1996). However, longer tenure implies
that paternal half-siblings might greatly differ in age.
Notable in the majority of primates studied, offspring born
to the same mother rarely share the same father, which
results in a preponderance of half-siblings over full-siblings
(Table 1).
III. THE IMPACT OF PATERNAL KINSHIP ON
SOCIAL BEHAVIOUR
Previous studies investigating the effect of kinship on social
behaviour in wild or wild-captured mammals often used
molecular genetic markers to estimate pairwise relatedness
among group members (e.g. Blumstein, Ardon & Evans,
2002; Matocq & Lacey, 2003), which fails to account for
pedigree information. When using these estimates of
relatedness alone, distinguishing between maternal and
paternal kin is difficult. Although kin (specifically sibling)
recognition has been studied in detail in many mammals
(reviewed in Blaustein, Bekoff & Daniels, 1987; Porter,
1988), these studies have not always distinguished maternal
and paternal kin (e.g. Grau, 1982; Blumstein et al., 2002).
However, there is good evidence in amphibians (e.g.
Blaustein & O’Hara, 1982), birds (e.g. Petrie, Krupa &
Burke, 1999) and mammals, especially rodents, suggesting
that individuals can discriminate paternal half-siblings from
unrelated individuals.
(1) Paternal kin bias in mammals
(a ) Inbreeding avoidance
A mechanism for inbreeding avoidance between fathers and
daughters appears to exist in montane voles (Microtus
montanus) as male presence causes sexual maturation (seen
from increased uterine weight) in unfamiliar females but not
in daughters (Berger, Negus & Day, 1997). Likewise, female
striped mice (Rhabdomys pumilio) are more likely to reproduce
with an unfamiliar male than their father (Pillay, 2002).
(b ) Affiliation and aggression
Captive Belding’s ground squirrels (Spermophilus beldingi)
direct less agonistic behaviour to paternal half-sisters than
to unrelated females (Holmes, 1986a). Golden-mantled
Biological Reviews 82 (2007) 319–334 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society
Anja Widdig
ground squirrels (S. lateralis), although not behaving nepo-
tistically, investigate the odour of paternal half-siblings
longer than those of other kin (Mateo, 2002). Adult
male house mice groom and investigate unfamiliar paternal
half-siblings less than unfamiliar non-kin, which is partic-
ularly interesting given that both behaviours are known
preludes to fights (Kareem & Barnard, 1982). In addition,
adult male and female house mice spend more time in
passive body contact with paternal half-siblings than with
unrelated individuals (Kareem & Barnard, 1982). Golden
hamsters (Mesocricetus auratus) discriminate between paternal
half-siblings and non-siblings in odour habituation tests
(Todrank, Heth & Johnston, 1998).
The most detailed mammalian study of interest comes
from wild spotted hyenas (Wahaj et al., 2004). Paternal half-
siblings in this species feed more often together than
unrelated individuals and form more coalitions with each
other than non-kin. Likewise, paternal half-siblings direct
less aggression towards each other compared to non-kin,
but no paternal kin bias was found in patterns of spatial
association in this species (Wahaj et al., 2004).
(c ) Paternal care
The higher social status of females and their cubs in
comparison to male hyenas suggests some constraints on
nepotism by sires. Male hyenas indeed exhibit no overt
nepotism, but associate more with daughters (not sons) than
with unrelated animals (van Horn, Wahaj & Holekamp,
2004). Although sires evidently recognize their own offspring,
nepotism by sires towards cubs was weaker than nepotism by
cubs towards their sires (van Horn et al., 2004). Paternal care
(i.e. playing and grooming) has been reported in mammalian
species with a high certainty of paternity. For example,
paternal care has been demonstrated in wild guinea pigs
(Cavia aperea) who exhibit a polygynous mating system
compared to the yellow-toothed guinea pig (Galea musteloides)
which mates promiscuously (low paternity certainty) and
therefore shows no paternal care (Adrian et al., 2005).
(d ) Offspring protection against infanticide
Infanticide among mammals has been reported in several
mammalian species, e.g. Columbian ground squirrels, S.
columbianus (Dobson, 1990); brown bears, Ursus arctos (Olson,
1993); bottlenose dolphins (Patterson et al., 1998; Dunn et al.,
2002); reviewed for mammals by Agrell, Wolff, Yloenen
(1998), Ebensperger (1998) and Blumstein (2000). However,
there is evidence that resident males do not kill their own
offspring or protect them against infanticide by others [e.g.
white footed mice, Peromyscus leucopus (Wolff & Cicirello,
1989); alpine marmots, Marmota marmota (Coulon et al.,
1995) and African lions (Packer & Pusey, 1983)].
(2) Paternal kin bias in primates
One of first pieces of evidence in favour of paternal kin
discrimination came from a captive study of pigtail
macaques, Macaca nemestrina (Wu et al., 1980). In this
experiment, unfamiliar juvenile peers sat closer to their
Paternal kin discrimination
paternal half-siblings than to non-kin (Wu et al., 1980).
Because the subjects were separated from their mothers and
other relatives immediately after birth, these authors
concluded that kin recognition may occur in the absence
of prior association with any relatives. Subsequent captive
studies in multiple species were not able to replicate these
results under varying rearing conditions, but showed a con-
sistent preference for familiar over unfamiliar animals re-
gardless of their relatedness: pigtail macaques (Fredrickson &
Sackett, 1984; Sackett & Fredrickson, 1987); long-tailed
macaques, Macaca fascicularis (Welker et al., 1987); savanna
baboons, Papio cynocephalus (Erhart, Coehlo & Bramblett,
1997). Among maternally deprived stump-tailed macaques,
M. arctoides, social preferences correlated most strongly with
companionship, followed by (paternal) kinship and rearing
conditions (MacKenzie, McGrew & Chamove, 1985).
The results of these studies convinced most primatologists
that nepotism is a consequence of familiarity, and that
primates cannot recognize paternal kin (e.g. Gouzoules &
Gouzoules, 1987; Bernstein, 1991; Chapais, 2001; Rendall,
2004). However, few primatologists questioned whether the
fact that experimental animals were isolated from their
mothers soon after birth, reared in peer groups, and tested
with unfamiliar individuals created an appropriate context
for evaluating kin recognition abilities (but see Walters,
1987). Therefore, it seems possible that these studies failed
because animals might need to be exposed to any kin (either
maternal or paternal) to learn their templates and then use
these templates to match phenotypes of unfamiliar kin.
Behavioural studies have also suggested that male
savanna baboons care for infants that they are unlikely to
have sired (e.g. Stein, 1984; Strum, 1984; Smuts, 1985;
Smuts & Gubernick, 1992). Genetic data supported the
hypothesis that male care is not a function of paternity in
Barbary macaques (M. sylvanus) a species which exhibits
pronounced male care (e.g. Paul, Kuester & Arnemann,
1992, 1996; Menard et al., 2001). These results do not
suggest that male primates can recognize their offspring
(Bernstein, 1988). Some studies have suggested that male
care is a byproduct of mating effort (e.g. Smuts &
Gubernick, 1992; Menard et al., 2001, reviewed in van
Schaik & Paul, 1996), a hypothesis strengthened by
experimental data showing that male vervet monkeys
(Cercopithecus aethiops) alter their behaviour towards infants
depending upon the presence or absence of the mother
(Keddy Hector, Seyfarth & Raleigh, 1989).
Recent studies of wild and free-ranging primates that
combined paternity analyses and behavioural observations
have demonstrated that some primate species discriminate
paternal kin from non-kin in various social contexts (see
below). These findings have resurrected interest in paternal
kin discrimination in primates.
(a ) Inbreeding avoidance
In wild savanna baboons opposite-sex paternal half-siblings
were as likely to be in sexual consorts as non-kin, but ex-
hibited lower levels of affiliative and sexual behaviour with
each other than unrelated opposite-sex pairs (Alberts, 1999).
In species with sex-biased dispersal, such as baboons, opposite-
Biological Reviews 82 (2007) 319–334 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society
323
sex paternal half-siblings born into the same social group
are less likely to spend their reproductive career in the same
group. In Alberts’ (1999) study, the fact that male emigration
was naturally reduced may account for these findings.
The probability of paternity by alpha male mandrills
(Mandrillus sphinx) decreased when alpha males were closely
related to the prospective female partner (Charpentier et al.,
2005). In a study of wild capuchin monkeys (Cebus apella)
alpha males monopolize breeding opportunities and retain
high-ranking positions over an extended period, a situation
that results in opportunities for males to mate with their
daughters. However, alpha males are much less likely to sire
the offspring of their daughters than they are to sire the
offspring of unrelated females (Muniz et al., 2006). A study
on free-ranging Barbary macaques contradicts this finding.
Kuester, Paul & Arnemann (1994) found that many
paternal dyads mated incestuously after more than two
years of co-residence (mainly fathers and daughters), but
interestingly this resulted in only two out of 62 potential
inbred offspring via the paternal line (Kuester et al., 1994).
Male reproduction in Barbary macaques (even in the wild)
does not appear to be skewed (Kuester & Paul, 1999,
Menard et al., 2001); this may reduce the probability of
paternal inbreeding.
(b ) Affiliation
Several studies indicate that levels of affiliation are higher
among paternal half-siblings than non-kin. In free-ranging
rhesus macaques (M. mulatta) adult females were signifi-
cantly more affiliative with their paternal half-sisters than
with unrelated females (Widdig et al., 2001, 2002; Widdig,
2002). The discrimination of paternal half-sisters was even
more pronounced among females of the same age (Widdig
et al., 2001). Very similar patterns have been detected
among wild savanna baboons where adult females affiliated
more with their paternal half-sisters than with unrelated
females (Smith, Alberts & Altmann, 2003; Silk, Altmann &
Alberts, 2006). Furthermore, Charpentier et al. (2007) found
that free-ranging juvenile mandrills affiliate more with
paternal half-siblings than with unrelated individuals sug-
gesting that the ability to recognize paternal kin is present at
a young age (two years) in this species. This bias was directed
towards adults, not juvenile half-siblings. However, the
absence of nepotism among juvenile paternal half-siblings
indicates that nepotism and kin recognition can evolve
independently and that, under some circumstances, the
benefits derived from preferential treatment might be
negligible (cf. Mateo, 2002). There is strong evidence in
primates that females exhibit stronger affiliation biases to
maternal half-sisters compared to paternal half-sisters
(Widdig et al., 2001, 2002; Silk et al., 2006). Interestingly,
female baboons form stronger bonds with paternal half-sisters
when no close maternal kin is available (Smith et al., 2003;
Silk et al., 2006). The availability of kin partners may change
systematically during an individual’s lifetime (Silk et al., 2006).
Preferential interactions among fathers and offspring are
also reported in some primate species. For example, af-
filiation between juvenile and adult male mandrills is higher
among father-offspring than non-kin dyads (Charpentier et al.,
324
2007). Goldberg & Wrangham (1997) have argued that the
lack of investment by male chimpanzees (Pan troglodytes) in
infants makes the possibility of offspring recognition by
males unlikely. However, a recent analysis, using genetic
data to determine paternity, suggests that male chimpanzees
spend more time playing with and grooming their own
infants (Lehmann, Fickenscher & Boesch, 2007).
(c ) Dyadic aggression
No primate study has found that paternal half-siblings direct
less dyadic aggression towards each other than towards
unrelated individuals as predicted by kin selection theory
(Hamilton, 1964). Among rhesus macaques paternal half-
sisters exchange non-physical and physical aggression at
similar rates as unrelated females (Widdig et al., 2002).
Similarly, mandrills direct dyadic aggression equally often to
paternal half-siblings and non-kin (M.J.E. Charpentier,
personal communication). However, male rhesus macaques
direct less aggression towards their own offspring than to
unrelated juveniles, even though they do not bias affiliative
interactions towards their offspring (A. Widdig, M. Chiavetta,
P. Nürnberg, W.J. Streich & M. Krawzcak, in preparation).
(d ) Coalition formation
Kin selection theory predicts that when intervening in an
ongoing conflict between two opponents, individuals
intervene more often on behalf of kin than non-kin, but
less often against kin than non-kin given that the cost/
benefit ratio is equal (Hamilton, 1964). In contrast to this
prediction, female rhesus macaques supported unrelated
females more often than paternal half-sisters (Widdig et al.,
2006b). However, in accordance with kin selection theory,
females intervened significantly less often against their
paternal half-sisters in comparison to unrelated females,
suggesting some constraints inhibiting females from pro-
viding support for paternal kin (Widdig et al., 2006b).
Among wild red howler monkeys (Alouatta seniculus)
father-son coalitions are more stable than coalitions among
unrelated males (Pope, 1990). A recent study on wild
savanna baboons revealed evidence that males supported
their own offspring more in agonistic disputes over
unrelated juveniles (Buchan et al., 2003). Male rhesus
macaques rarely intervene in dyadic conflicts and there is
no evidence that they support their offspring more often
than non-offspring (A. Widdig, M. Chiavetta, P. Nürnberg,
W.J. Streich & M. Krawzcak, in preparation).
(e ) Offspring protection against infanticide
Infanticide occurs in several primate species, but there is
evidence that male primates do not kill their own offspring;
instead, they protect them against infanticide by other males
[e.g. Hanuman langurs, Presbytis (now Semnopithecus) entellus
(Borries et al., 1999b); red howlers (Crockett & Janson, 2000);
long-tailed macaques (de Ruiter, van Hooff & Scheffrahn,
1994); Japanese macaques, Macaca fuscata (Soltis et al., 2000);
chacma baboons, P. ursinus (Palombit et al., 2000; Weingrill,
2000); mountain gorillas, Gorilla beringei (Watts, 1989)].
Biological Reviews 82 (2007) 319–334 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society
Anja Widdig
IV. MECHANISMS OF KIN DISCRIMINATION
The close relationship in mammals between mothers and their
offspring produces social systems in which maternal kinship
and familiarity are closely associated [e.g. house mice (Koenig,
1994); African elephants (Archie et al., 2006); Barbary
macaques (Kuester et al., 1994); reviewed for primates in
Gouzoules & Gouzoules, 1987)]. In many mammals, females
predominantly remain in their natal groups whereas males
disperse (Pusey, 1987) leading to the formation of female kin
groups (Greenwood, 1980). Consequently, a female’s offspring
are familiar with other maternal kin such as aunts, cousins,
and grandmother, with familiarity being mediated among
maternal siblings through their common mother. Given these
close links between mothers and their offspring, familiarity is
thought to be the most important mechanism of maternal kin
discrimination in mammals (Kareem & Barnard, 1982;
Walters, 1987; Bernstein, 1991; Chapais, 2001). However,
when testing the mechanisms of kin recognition, there is
a need to separate the effects of relatedness from those
resulting from familiarity (cf. Kareem & Barnard, 1982;
Koenig, 1994; Mateo & Holmes, 2004).
The most likely mechanisms of paternal kin discrimination
among mammals are familiarity and/or phenotype matching
(Mateo & Holmes, 2004, see Table 2). There is extensive
evidence supporting both familiarity and phenotype match-
ing among rodents [e.g. Belding’s ground squirrels (Holmes,
1986b); North American beaver, Castor canadensis (Sun &
Müller-Schwarze, 1997); golden hamsters (Heth, Todrank &
Johnston, 1998; Mateo & Johnston, 2000); white-footed
deermice, Peromysus leucopus (Grau, 1982); spiny mouse, Acomys
cahirinus (Porter, Matochik & Makin, 1983); reviewed for
rodents by Mateo (2003)]. Recent primate studies have also
suggested familiarity and/or phenotype matching as under-
lying mechanisms of paternal sibling discrimination, while
fathers might use mating information as a proxy to recognize
offspring (summarized in Table 3).
(1) Familiarity
(a ) Familiarity among paternal half-siblings via age proximity
Paternal half-siblings are also likely to share familiarity,
because they tend to be peers, i.e. born in the same age-
cohort (references in Table 1). These peers preferentially play
and interact more with each other than with non-peers (e.g.
Pereira, 1988; Janus, 1992). The fact that peers are more
likely to be kin is the facilitating condition that allows kin
selection to act. In species with a perfect skew (all offspring
sired by one male) and short male tenure (one breeding
season), peerage could therefore be used as a marker of
paternal kinship and kin selection should be expected to
favour affiliation among peers. However, in species with high,
but not perfect, skew (few males monopolizing all reproduc-
tions) and where male tenure extends beyond one breeding
season, age proximity could only be used as a first
approximation for paternal kin discrimination. Indeed, for
most mammals, perfect male skew does not occur (see
references in Introduction); therefore, age proximity alone is
Paternal kin discrimination 325

Table 2. Mechanisms of kin recognition in primates

Familiarity
Kin discrimination by familiarity predicts that individuals will treat those conspecifics as kin with whom they either interacted
during a critical period in their development (Tang-Halpin, 1991) or with whom they had persistent long-term exposure
(Walters, 1987). This hypothesis requires a high correlation between relatedness and social association (Walters, 1987).
Phenotype matching
The phenotype matching hypothesis assumes that phenotypic similarities correlate with genotypic similarities (Sherman et al., 1997).
An individual learns its own phenotypic attributes (e.g. odour or appearance) or those of known relatives and matches this learned
template against a potential kin in order to assess kinship (Holmes & Sherman, 1983; Lacy & Sherman, 1983; Tang-Martinez, 2001).
Is familiarity different from phenotype matching?
Tang-Martinez (2001) emphasized that in both mechanisms an individual learns a phenotype and then matches that phenotype to a
given individual. In the case of recognition by association (i.e. familiarity) the phenotype that is learned is an individually
distinctive cue in which the learned template and the cues of the encountered individual must match exactly. In the case of
phenotype matching, an individual learns the most likely or salient aspects of a cue or a combination of components of a cue
(i.e. family-specific cues) that are then matched to the cue of the encountered individual. This family-specific cue could be
learned from known relatives (but only by the father when considering paternal kin discrimination) or if the father is not present,
from self. However, familiarity might be the more reliable mechanism in paternal kin discrimination, as this is likely to lead to
fewer mistakes in assessing kinship compared to phenotype matching.

not sufficient to discriminate with complete accuracy
between paternally related and unrelated individuals.
Studies in species exhibiting high skew in male reproduc-
tion, however, found a strong effect of age proximity on the
ability to discriminate paternal half-siblings from non-kin. For
example, consortship cohesiveness was lower for opposite-sex
paternal half-siblings of the same age than of different age
(Alberts, 1999). Same-age paternal half-sisters were more
affiliative than different-age paternal half-sisters in rhesus
macaques and savanna baboons (Widdig et al., 2001, 2002;
Silk et al., 2006).
(b ) Familiarity among paternal half-siblings mediated by mothers
Mothers could mediate familiarity either directly among
paternal half-siblings or via the common father. This
prediction assumes that females have reliable information
on offspring paternity. Females might derive this informa-
tion by comparing mate preferences of other females with
their own (e.g. rhesus macaques, McMillan, 1986) or by
comparing phenotypic cues such as odour of other females’
newborns with those of their own. Mothers could mani-
pulate the extent of familiarity among paternal half-siblings
by influencing their offspring’s association patterns during
a critical developmental phase (the maternal-control
hypothesis: Widdig et al., 2001). For example, if mothers
(even when they are unrelated) who have conceived infants
from the same male in a given mating season were closely
associated after parturition, their offspring could preferen-
tially develop affiliations with same-age paternal relatives
(see a in Fig. 1). Mothers in many primate species exert
control over the interactions of their offspring with other
group members and tend to be more tolerant of maternal
kin than to maternally unrelated individuals (e.g. Fairbanks,
1990; Berman & Kapsalis, 1999; reviewed in Paul, 1999). In
addition, affiliation among peers was related to affiliation
between the peers’ mothers in captive rhesus macaques (de
Waal, 1996), but shared paternity among peers was not
investigated in that study. However, this mechanism would
assume that the ability to discriminate paternal kin precedes
the birth of her next newborn. Depending upon shared
paternity, patterns of association among mothers are
expected to change every year unless females consistently
converge in their mate-choice decisions.
Mothers might also mediate familiarity among paternal
half-siblings by maintaining close relationships with the
common sire after their infants are born (the mother’s-
common-male-friend hypothesis, see b in Fig. 1). While
‘sharing a common friend’ has not yet been reported in multi-
male groups, ‘friendship’ in opposite-sex pairs has been
described in several primate species [e.g. savanna baboons
(Smuts, 1985); chacma baboons (Palombit et al., 1997);
chimpanzees (Goodall, 1986); mountain gorillas (Watts,
1994); Japanese macaques (Takahata, 1982); rhesus mac-
aques (Manson, 1994)]. Sometimes, females and males who
have previously mated form affiliative relationships during
the following birth season (Manson, 1994) suggesting that
some males are still close to their mates after the offspring is
born. Post-birth association between mother and father
might provide offspring protection against infanticide (e.g.
Palombit et al., 1997; Soltis et al., 2000; reviewed in van Schaik
& Kappeler, 1997), but could also promote familiarity
between offspring and fathers. There is nevertheless evidence
that maternal proximity to fathers is not always necessary.
Adult male rhesus macaques associated at higher rates with
offspring than with unrelated infants, regardless of whether
the mothers were in spatial proximity, but long-term social
relationships between parents might have promoted father-
offspring associations (Berenstain, Rodman & Smith, 1981).
If females ‘share’ male friends, then recognition of paternal
half-siblings via familiarity might be a byproduct of friend-
ships between mothers and the common sire.
(c ) Familiarity among paternal half-siblings mediated by
a common father
If the father remains present in the group after the infants’
birth as is the case in baboons (Buchan et al., 2003),

Biological Reviews 82 (2007) 319–334 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society
326 Anja Widdig

Table 3. Suggested mechanisms of paternal kin discrimination in primates. PS ¼ Paternal half-siblings

Study
Species Finding Suggested mechanism/s conditions References
Savanna baboons Inbreeding avoidance among Familiarity (age proximity) Wild Alberts (1999)
Papio cynocephalus adult PS of the opposite-sex and phenotype matching
Capuchin monkeys Inbreeding avoidance Familiarity (long-term Wild Muniz et al. (2006)
Cebus apella among father-daughters co-residence)
Rhesus macaques Kin bias in affiliation and Familiarity (age proximity) Free- Widdig et al. (2001,
Macaca mulatta coalitions among adult female PS and phenotype matching ranging 2002, 2006b)
Savanna baboons Kin bias in affiliation Familiarity (age proximity) Wild Smith et al. (2003);
Papio cynocephalus among adult female PS and phenotype matching Silk et al. (2006)
Mandrills Kin bias in affiliation of juveniles Familiarity * Free- Charpentier et al. (2007)
Mandrillus sphinx towards adult female PS, and ranging
fathers, but not to juvenile PS
Chimpanzees Kin bias in playing by fathers Behavioural cues Wild Lehmann et al. (2007)
Pan troglodytes with offspring (mating information)
Savanna baboons Bias in offspring support by Phenotype matching or Wild Buchan et al. (2003)
Papio cynocephalus males when intervening in behavioural cues
juvenile conflicts (mating information)
Hanuman langurs Offspring protection by males Behavioural cues Wild Borries et al. (1999b)
Semnopithecus entellus against infanticide (mating information)
Japanese macaques Offspring protection by males Behavioural cues Wild Soltis et al. (2000)
Macaca fuscata against infanticide (mating information)

*This study concluded that age proximity is not responsible for paternal kin discrimination in mandrills, as juveniles initiated more
affiliation with adult, but not with juvenile, paternal half-siblings. They further hypothesized that individuals with the same degree of
relatedness (regardless of the origin of relatedness) should have an equivalent amount of genes in common, and hence equivalent
phenotypic cues should be matched. Based on their finding that paternal half-siblings showed higher affiliation than other dyads of the
same degree of relatedness, they rejected phenotype matching as a potential mechanism.

capuchins (Muniz et al., 2006), and rhesus macaques (A.
Widdig, unpublished data), fathers could develop relation-
ships with their own offspring (the paternal-care hypothesis,
see c in Fig. 1). Male baboons provide paternal care in
supporting their own offspring in agonistic disputes against
other juveniles (Buchan et al., 2003). This suggests that
males assess paternity either through mating information or
by direct offspring recognition after birth. Paternal half-
siblings could also become familiar with one another
through their joint associations with the common father.
Father-offspring familiarity (which should be high when the
father is in the group centre or low when the father is at the
periphery) might then determine the degree of familiarity
among paternal half-siblings.
Fathers might also mediate familiarity among paternal
half-siblings by maintaining close relationships with the

Associations among paternal half-siblings

via familiarity via phenotype matching

mother mediated father mediated father present father absent

a. maternal b. mothers affiliate c. paternal d. father affiliates e. father used f. self-

control with the father care with mothers as a template reference

Fig. 1. Associations among paternal half-siblings explained by familiarity mediated either by their mothers, the common father, or
by phenotype matching when the father is either present or absent (see text for details).

Biological Reviews 82 (2007) 319–334 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society
Paternal kin discrimination
mothers of his offspring following parturition [the father-
mothers-friendship hypothesis, cf. Stein (1984), Smuts
(1985), Busse (1985), see d in Fig. 1]. Under this hypothesis
the friendship is initiated or maintained by the male in
contrast to the mother (see b in Fig. 1). As a byproduct,
infants grow up in close proximity to both their father and
paternal half-siblings for a certain period. However, only
one study that did not include genetic data has suggested
that males were more responsible than females in main-
taining spatial proximity during the birth season (Manson,
1994), while others found that females are responsible for
maintaining associations with their mates (Chapais, 1983,
1986; Hill, 1990; Palombit et al., 1997).
(2) Phenotype matching
The phenotype matching hypothesis assumes that individ-
uals use themselves or known kin, such as the father, as
a template to assess kinship to other individuals (Holmes &
Sherman, 1983; Lacy & Sherman, 1983; see Table 2). The
fact that, regardless of age, females preferred paternal half-
sisters might suggest that phenotype matching is involved in
paternal kin discrimination, too (Widdig et al., 2001; Smith
et al., 2003; but see Silk et al., 2006, for no such effect).
Evidence for some types of phenotype matching has been
suggested for male baboons, where males were more likely
to support their own offspring than unrelated juveniles
(Buchan et al., 2003). Buchan et al. (2003) tested whether
such preferences could arise through behavioural patterns
by comparing three classes of juveniles per male: (i) genetic
offspring, (ii) behavioural offspring (juveniles for which
a male consorted with the mother during the days of most
likely conception, but the male was excluded as a genetic
father) and (iii) unconnected juveniles (neither genetic nor
behavioural offspring). If males rely on phenotype match-
ing, one would predict that males give more support to their
genetic than behavioural offspring, but one would expect no
difference between behavioural offspring and unconnected
juveniles. The data on male baboons are consistent with this
prediction (Buchan et al., 2003). Alternatively, Buchan et al.
(2003) suggested that males might rely on fine-grained
assessments of their mating behaviour with their offspring’s
mother (Table 3). This hypothesis was supported by the fact
that whether or not the male mated with the mother was
not a good predictor of paternal care, while how often he
mated with her during her fertile period was a good
predictor. While these studies suggest that animals use
phenotype matching as a cue for paternity, we cannot rule
out the possibility that long-term associations between
mother and father could account for these results (see
below).
(a ) Using the father as a template to match potential paternal
half-siblings
If the father is present in the group after his offspring is
born, this increases the chance that he will be familiar with
his offspring in comparison to non-group males. In any
case, when the father is present the offspring might use him
Biological Reviews 82 (2007) 319–334 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society
327
as the relevant template of a known kin to assess other
infants for shared paternity (see e in Fig. 1). Note that two
mechanisms might be involved: the mechanism for father-
offspring recognition might be familiarity; but, as a conse-
quence, offspring can use the father as a template to match
phenotypes of potential paternal half-siblings.
(b ) Using self as a template to match potential paternal
half-siblings
In some circumstances fathers might be absent before their
offspring is born. For example, in rhesus macaques, 30% of
infants are born without their fathers present (A. Widdig,
unpublished data). In these cases it is not possible for offspring
to use the father as a template to assess paternal kinship in
other individuals. Therefore, the most reliable reference for
paternal kin discrimination, assuming that the impact of
mothers is absent, is probably one’s self (’self-referent’
phenotype matching: Sherman, 1991; Hauber & Sherman,
2001a, ‘armpit effect’: Dawkins, 1982, see f in Fig. 1).
Self-referent phenotype matching has been suggested for
different species and cues from various communication
modes are likely to be used across species. For example,
lekking male peacocks (Pavo cristatus) preferentially display
next to paternal half-brothers even when males have been
reared apart and cannot rely on learned social cues (Petrie
et al., 1999). Female sticklebacks (Gasterosteus aculeatus) derive
information about their own and their potential mates’
Major histocompatibility complex (MHC) polymorphism
for optimal complementarity of their own set of alleles
(Aeschlimann et al., 2003). Self-referent phenotype match-
ing has also been suggested among mammals. Golden
hamsters discriminate between the odour of unfamiliar kin
and non-kin, even when reared only with non-kin (Heth
et al., 1998; Mateo & Johnston, 2000). In humans (Homo
sapiens) women prefer the odour from men with human
leukocyte antigen (HLA, human MHC) genes similar to
their own, but not identical or totally dissimilar (Jacob et al.,
2002). Interestingly, the choice was based upon HLA genes
inherited from the woman’s father, but not her mother
(Jacob et al., 2002).
There is considerable controversy about the experimental
procedures for demonstrating self-referent phenotype
matching (e.g. Heth & Todrank, 2001; Mateo & Johnston
2001, 2003; Hauber & Sherman 2001b, 2003; Hare et al.,
2003) as self-referent phenotype matching seems to be the
remaining explanation when all others are excluded (Hauber &
Sherman, 2001a). The only way to show self-referent pheno-
type matching among paternal half-siblings is to look at
offspring who have never seen their father (either naturally
or via experimental manipulation), and demonstrate (i) that
they discriminate between paternal half-siblings and non-
kin, and (ii) that mothers do not mediate such kin bias.
(3) Familiarity and/or phenotype matching?
Familiarity and phenotype matching are not necessarily
mutually exclusive mechanisms and it is often impossible to
disentangle them (Porter, 1988; Tang-Martinez, 2001). It is
328
important to point out that none of the primate studies have
yet been able to provide direct evidence for phenotype
matching (Table 3) as alternative mechanisms can also ex-
plain the results. For example, mothers mediating familiar-
ity and/or mother-father postbirth associations might have
triggered the social preference of paternal half-siblings over
non-kin (cf. Widdig et al., 2001, 2002; Smith et al., 2003; Silk
et al., 2006). Likewise, it is not clear whether males rec-
ognize offspring by matching phenotypes or whether they
use behavioural cues such as mating information to assess
paternity (cf. Borries et al., 1999b; Soltis et al., 2000; Buchan
et al., 2003; Lehmann et al., 2007). A study providing direct
evidence for phenotype matching would have to demon-
strate paternal kin bias while controlling for familiarity, e.g.
by systematic behavioural observations starting from birth
to adulthood when considering sibling recognition and
taking into account the potential impact of familiarity.
Alternatively, when considering father-offspring recogni-
tion, observation should begin before the conception of the
offspring to control for paternity certainty.
V. CUES POTENTIALLY USED IN KIN
DISCRIMINATION
Future research should focus on targeting cues used in
paternal kin discrimination which may vary across species
depending upon their key sensory modalities. The most
likely cues used in primates are odour (Hübener & Laska,
1998), appearance (Dasser, 1988; Vokey et al., 2004),
acoustic characteristics of vocalizations (Rendall, Rodman
& Edmond, 1996), and/or personality (Gosling, 2001;
Weiss, King & Perkins, 2006). The general assumption when
testing these cues is that a particular cue, such as the odour
of individual A, elicits differential behavioural responses by
the discriminator (individual B) depending upon the social
context in which kinship is assessed. For example, individuals
who do not mate with close kin avoid costs of inbreeding, so
individuals should prefer mates which differ to some extent
from their own odour. Mating preferences for MHC-
dissimilar or heterozygous mates have been demonstrated in
house mice (Potts, Manning & Wakeland, 1991). By
contrast, individuals would benefit most from cooperation
with close kin, so individuals should preferentially cooperate
with partners which are similar to their own odour. House
mice prefer communal nesting partners that share alleles of
the MHC (Manning, Wakeland & Potts, 1992).
(1) Odour
If animals use odour in paternal kin discrimination, then one
would predict that paternal half-siblings recognize each
other based upon odour similarities. The use of odour for kin
discrimination is well documented among rodents (Schwag-
meyer, 1988). For example, golden hamsters perceive odour
from genetically similar individuals such as paternal half-
siblings as similar even when unfamiliar (Todrank et al.,
1998). Belding ground squirrels produce odours that are
Biological Reviews 82 (2007) 319–334 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society
Anja Widdig
correlated with relatedness, allowing precise estimates of
kinship even among distant relatives (Mateo 2002).
Paternal half-siblings should be more similar in odour
than non-kin, and individuals should be most attracted to
those of their paternal half-siblings which are most similar
to their own odour. One way of testing this could be
a comparison of genotype similarities of odour-associated
genes, such as the MHC, with rates of affiliative behaviour
among paternal half-siblings (see Potts, 2002). Those pairs
of paternal half-siblings who have high affiliation indices are
expected to share more MHC alleles than pairs of paternal
half-siblings with low affiliation indices. However, evolu-
tionary strategies for a functional MHC region differ
between species and even within primate species (Doxiadis
et al., 2000). For example, extremely high rates of
polymorphism of the primate MHC-DRB region suggest
an alternative strategy to cope with pathogens in rhesus
macaques (Doxiadis et al., 2000). Therefore, comparing
genotype similarities in certain olfactory receptor genes
(ORG) might also be appropriate because they are encoded
by more than 1000 genes (Gilad et al., 2003). Interestingly,
54% of human ORG carry at least one coding region
disruption and are therefore considered pseudogenes
(Rouquier et al., 1998), with the fraction of pseudogenes
equal to approximately 32% in chimpanzees and 36% in
rhesus macaques (Gilad et al., 2003). There seems to be
agreement that the decreasing reliance on smell during
primate evolution reflects the increasing importance of
trichromatic vision (e.g. Dominy & Lucas, 2001; Gilad et al.,
2004). However, it is likely that the evolution of paternal kin
discrimination preceded the reduction in olfactory sensitiv-
ity, and may have been retained.
(2) Appearance
It is possible that primates have added visual cues to assess
kinship, given the importance of vision among modern
Cercopithecines (Dominy & Lucas, 2001). To match
phenotypes of others with self, it is presupposed that
animals must recognize themselves. Monkeys do not seem
to recognize themselves in mirrors (Gallup, 1997), but the
methodological approach used to examine self-recognition
has been questioned (De Veer & van den Bos, 1999). Using
self as a template, however, would be essential for offspring
whose fathers left before their birth. Evidence in favour of
visual kin recognition was suggested in chimpanzees based
on their ability to recognize facial similarities of unfamiliar
conspecifics (Parr & de Waal, 1999). Subjects correctly
matched mother-son dyads, but not mother-daughters.
However, a reanalysis of the original data revealed that the
bias of asymmetry between sons and daughters was due to
the framing of the images presented, as eliminating the
frame bias eliminated the asymmetry but not the ability of
humans to recognize chimpanzee kin (Vokey et al., 2004; see
Rendall, 2004 for discussion). Still, it seems plausible to
propose that some primate species rely mainly on odour
cues but might additionally use visual cues for paternal kin
discrimination. Future studies should use images to assess
facial resemblance between kin and non-kin pairs by
Paternal kin discrimination 329

computer programs, human subjects, or touch-screen- will choose social partners on the basis of personality traits.
trained primates. Second, personality traits will be partly determined by
paternal genes. Third, preferred social partners will share
paternity more often than expected by chance alone.
(3) Vocalization
It is also possible that animals use vocal cues to match and
identify kin, especially over long distances when odour or VI. CONCLUSIONS
visual cues are unavailable. This would require that
vocalizations are individually distinct and consistent over
(1) Based on the studies available I conclude that mam-
time as has been shown for spotted hyenas (East & Hofer,
mals, including primates, can discriminate between paternal
1991). Most studies on vocal recognition in mammals
kin and non-kin in various social contexts. Available data
have focused on recognition between mothers and offspring
suggest that paternal kin discrimination works among
(e.g. Kaplan, Winship-Ball, Sim, 1978; Pereira, 1986;
paternal half-siblings, but also among fathers and their off-
Gouzoules & Gouzoules, 1990; Hammerschmidt & Fischer,
spring. A high skew in male reproduction is common among
1998; Holekamp et al., 1999; Rendall, Cheney & Seyfarth,
many mammalian and primate species providing a high
2000). Other studies have looked at vocal recognition of
probability of paternal kin to interact with each other.
maternal kin. For example, spotted hyenas respond more
Depending upon the length of male group tenure, offspring who
vigorously to long-distance vocalizations of maternal kin
share the same sire (i.e. paternal half-siblings) are either close in
than non-kin, and the intensity of response was correlated
age (short male tenure) or different in age (long male tenure).
with the degree of maternal relatedness (Holekamp et al.,
(2) Both familiarity and phenotype matching have been
1999). Female rhesus macaques have been reported to
suggested as mechanisms underlying paternal kin discrim-
respond faster and longer to calls of maternal kin than non-
ination in different mammalian species. However, no direct
kin, also suggesting kin recognition (Rendall et al., 1996). In
evidence of phenotype matching has yet been provided in
addition, individual recognition has been suggested based
primates, as studies have not fully controlled for familiarity
on the evidence that females showed a pronounced re-
as a confounding factor. To reject the familiarity hypothesis
sponse to calls from individual B after being habituated to
one would need to demonstrate that neither mothers nor
different calls of individual A (Rendall et al., 1996). Playback
the father mediate familiarity among paternal half-siblings.
experiments on chacma baboons indicate that females
To support the self-referent phenotype matching hypothesis,
recognize the calls of maternal kin of other individuals
one would need to show that infants, whose father left
(Cheney & Seyfarth, 1999).
before their birth, also develop the ability to discriminate
If animals use acoustic characteristics as a cue to assess
their paternal half-siblings from unrelated individuals
paternal kinship, one would first need to demonstrate that
without the mediation by their mothers. Finally, when both
paternal half-siblings share more acoustic characteristics
mechanisms are involved it is difficult to empirically
than unrelated individuals. If such patterns can be
disentangle them.
observed, one would then need to show that individuals
(3) Mechanisms of kin discrimination are not necessarily
indeed use vocal cues to recognize paternal kin, e.g. by
identical across mammalian species. Differences are to be
demonstrating that test subjects respond differently to
expected because recognition mechanisms must function
playback calls of paternal kin than to calls of non-kin.
within the confines set by a species’ phylogenetic history
and will reflect key sensory modalities used in communi-
cation, mating and demographic structure.
(4) Personality
(4) Mammalian social systems are complex and flexible.
Non-human primates develop and display distinct person- Therefore it is likely that mammals use multiple cues for
ality traits (Capitanio, 1999; King & Figueredo, 1997; Weiss paternal kin discrimination such as odour, appearance,
et al., 2006; Clarke & Boinski, 1995; Bolig et al., 1992). In vocalization or personality. Depending upon the specific
rhesus macaques, some personality traits, such as increased conditions (e.g. social and ecological), individuals even of the
impulsivity and aggressiveness, are closely associated with same species may use different mechanisms and/or cues.
diminished concentrations of cerebrospinal fluid mono-
amine metabolites, which have a significant paternal genetic
component (Higley et al., 1993; Clarke et al., 1995) and are
fairly stable throughout life (Stevenson-Hinde, Stillwell- VII. ACKNOWLEDGEMENTS
Barnes & Zunz, 1980; Capitanio, 1999). Among humans,
approximately 30–50% of personality variance is heritable, I am grateful to Susan Alberts, Bernard Chapais, Marie
i.e. the result of genetic differences among individuals Charpentier, Constance Dubuc, Melissa Gerald, Michael
(Bouchard & Loehlin, 2001) and there is some evidence that Krawczak and Joan Silk for fruitful discussions and
the same is true in chimpanzees (Weiss, King & Figueredo, comments on earlier drafts of the manuscript. Alexander
2000). Hence, shared paternally inherited personality Weiss and Kevin Potts kindly improved the English. I thank
attributes could modulate social relationships and provide two anonymous referees for their constructive comments.
a mechanism for behavioural phenotype matching. Several Funding was provided by the German Science Foundation
predictions follow from this hypothesis. First, individuals with an Emmy Noether Fellowship (WI 1808/1-2).

Biological Reviews 82 (2007) 319–334 Ó 2007 The Author Journal compilation Ó 2007 Cambridge Philosophical Society
330
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