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OCR for page 253
12
Genomic Imprinting and the
Evolutionary Psychology of Human
Kinship
DAVID HAIG
Genomic imprinting is predicted to influence behaviors that affect individuals
to whom an actor has different degrees of matrilineal and patrilineal kinship
(asymmetric kin). Effects of imprinted genes are not predicted in interactions
with nonrelatives or with individuals who are equally related to the actor’s
maternally and paternally derived genes (unless a gene also has pleiotropic
effects on fitness of asymmetric kin). Long-term mating bonds are common
in most human populations, but dissolution of marriage has always affected
a significant proportion of mated pairs. Children born in a new union are
asymmetric kin of children born in a previous union. Therefore, the innate
dispositions of children toward parents and sibs are expected to be sensitive
to cues of marital stability, and these dispositions may be subject to effects
of imprinted genes.
“The burden of making and the duty of exacting compensation ran on
the mother’s side as well as the father’s. A father and son, or two half-
brothers, would for the purposes of the blood-feud have some of their
kindred in common, but by no means all.”
Pollock and Maitland (1895)
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge,
MA 02138. E-mail: dhaig@oeb.harvard.edu.
253
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254 / David Haig
T
he opening quotation comes from a discussion of Anglo-Saxon
law. An individual could be liable to pay wergeld for the slay -
ing of his mother’s kinsman by his father’s kinsman and be
entitled to receive wergeld for the same slaying, because each individual
combined two lines of descent. The individual is divisible. Just as his
loyalties can be divided by obligations to the two sides of his family, so
too can his genome be divided between genes he shares with his mother
and genes he shares with his father. Blood is thicker than water, and
blood does not mix (in the sense that genes do not blend).
Genetically determined behaviors that benefit the father’s side of
the family may be favored by natural selection when a gene has been
transmitted by a sperm but not when the same gene has been transmit -
ted by an egg. Conversely, a behavior that benefits the mother’s side of
the family may be favored when a gene has been transmitted by an egg
but not when the same gene has been transmitted by a sperm. In such cir-
cumstances, imprinted alleles, genes that are differently expressed when
inherited via eggs and via sperm, can supplant unimprinted alleles
that are expressed independent of parental origin (Haig, 1997, 2000b).
Imprinted genes have been considered prime candidates for
involvement in disorders of human social interaction, such as autism
and schizophrenia, because of their predicted role in interactions among
kin (Badcock and Crespi, 2006; Isles et al., 2006; Crespi, 2008; Goos and
Ragsdale, 2008; Úbeda and Gardner, 2010, 2011). Not all social interac -
tions promote imprinted gene expression, however. The principal pur -
pose of this paper is to clarify the rather specific conditions that favor
stable maintenance of imprinted gene expression, but this task requires
a broader understanding of how humans innately categorize kin. These
questions will be addressed with a particular focus on effects of partner
change and on internal genetic conflicts during sexual maturation and
adolescence.
ASYMMETRIES OF RELATEDNESS
Consider an imprinted locus at which the established allele is
silent when paternally derived but expressed at level x > 0 when mater-
nally derived. This pattern of expression is an evolutionarily stable
strategy (ESS) when two conditions are met:
dwi
∑p <0
i
dx (1A)
i
d 2 wi
dwi
∑m = 0, ∑ mi (1B)
<0
i
dx 2
dx
i i
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Genomic Imprinting and the Evolutionary Psychology of Human Kinship / 255
where dwi/dx is the effect of a change in x on the fitness of individual i,
and pi and mi are coefficients of patrilineal and matrilineal relatedness of
the category to which individual i belongs. Inequality (1A) specifies that
extra x reduces patrilineal inclusive fitness. This condition maintains
silence of paternally derived alleles. Eq. (1B) specifies that x is a local
maximum of matrilineal inclusive fitness (Haig, 1997). These conditions
are equivalent to
dws dwa
∑m < – ∑ pa (2A)
s
dx dx
s a
dws dwa
∑m = − ∑ ma (2B)
s
dx dx
s a
where s indexes symmetric kin (individuals for whom ms = ps) and a
indexes asymmetric kin (individuals for whom ma ≠ pa). An individual’s
symmetric kin include herself, her offspring, and her grandoffspring,
but most other categories of kin are asymmetric, including “fullsibs,”
because of uncertainty of paternity. Thus, the right-hand sides of 1A
and Eq. (1B) can be considered to represent the marginal effect of x on
the individual’s own survival and reproduction (individual fitness).
Eq. (2B) describes a tradeoff in the maximization of matrilineal
inclusive fitness. At the ESS, the marginal effect of x on individual fit-
ness is balanced by a marginal effect of opposite sign on indirect fitness
obtained via asymmetric kin. If the value of Eq. (2B) i s negative, then
e xtra x i ncreases individual fitness at a cost to matrilineal asymmetric
kin. If the value of Eq. (2B) is zero, then x simultaneously maximizes
both components of inclusive fitness (most plausible if x has no effects
on matrilineal asymmetric kin). If the value of Eq. (2B) is positive, then
extra x increases the fitness of matrilineal asymmetric kin at a cost to
individual fitness.
Substitution of the right-hand side of Eq. (2B) for the left-hand side
of 2A yields
dw dw
∑ ma dxa > ∑ pa dxa , (3A)
a a
which can be rearranged to give
dw j dwk
∑ (m > ∑ ( pk − mk )
− pj ) ,
j
dx dx (3B)
j k
where j indexes matrikin (individuals for whom mj > pj) and k indexes
patrikin (individuals for whom mk < pk). This partition allows kin to be
assigned to three mutually exclusive classes: symmetric kin ( mi = pi),
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256 / David Haig
matrikin (mi > pi), and patrikin (mi < pi). Inequality (3B) states that
inactivation of the silent paternal allele is maintained when the summed
effects of extra x on fitness are worse for patrikin than for matrikin,
where fitness effects are weighted by the asymmetries of relatedness
(terms in parentheses).
The ESS for a locus at which the established allele is silent when
maternally derived but expressed at level z > 0 when paternally derived
is obtained by substitution of z for x and reciprocal substitution of m
for p throughout the above analysis.
If maternal-specific expression of x has effects on two individuals
only, (1A) and Eq. (1B) become
dw1 dw2 (4A)
+ p2 <0
p1
dx dx
dw1 dw2
+ m2 = 0.
m1 (4B)
dx dx
These conditions describe a tradeoff in which the two individuals’
fitnesses are differently weighted for genes of maternal and paternal
origin. Condition (4A) can be expressed in a convenient form using a
substitution from Eq. (4B):
p2 m2 dw2
– <0
p1 m1 dx (4C)
Condition (4C) shows that the maintenance of paternal silence depends
on a difference in the ratios of matrilineal and patrilineal relatedness
for the two individuals affected.
If one of these individuals is the actor within whom x i s
e xpressed ( p 1 = m 1 = 1 ), then (4C) and Eq. (4B) become
{ p2 − m2 } dw2 < 0 (5A)
dx
dw1 dw2
= − m2 . (5B)
dx dx
Maternal-specific expression of x either benefits self at a cost to an
individual who is patrikin (dw1/dx > 0, dw2/dx m2) or benefits
an individual who is matrikin at a cost to self ( dw1/dx 0,
p2 < m2). The ESS at a maternally silent locus, with paternal expression
level z, is obtained by swapping m2 for p2 and z for x:
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Genomic Imprinting and the Evolutionary Psychology of Human Kinship / 257
(6A)
{m2 − p2 } dw2 < 0
dz
dw1 dw2 (6B)
= − p2 .
dz dz
Paternal-specific expression of z either benefits self at a cost to an
individual who is matrikin (dw1/dx > 0, dw2/dx < 0, p2 < m2) or benefits an
individual who is patrikin at a cost to self (dw1/dx 0, p2 > m2).
KINSHIP CATEGORIES
Other individuals evoke different innate dispositions in ego: some
are sexual rivals, and others are potential mates; some are parents,
and others are offspring; some are friends, and others are strangers.
These dispositions constitute an implicit categorization of others that
represents the way natural selection has parsed social interactions in a
particular evolutionary lineage. The dispositions define the categories:
all individuals who evoke a disposition belong to a category defined by
the disposition. If the members of a category are, on average, related
to ego, then the disposition will evolve, in part, shaped by its effects
on the fitness of kin. An individual who evokes the disposition can be
considered to be treated as a kinsman and the disposition can be con -
sidered a kin-directed behavior.
An actor can treat another individual as belonging to an innate
category without recognizing that a category exists or recognizing par-
ticular individuals as members of the category. As a simple example,
h ormones secreted into the maternal circulation by a fetus affect
another individual who necessarily carries copies of the maternally
derived alleles of the fetus (Haig, 1996). However, if a behavior is to
be preferentially directed toward a particular category of kin within a
larger group of similar individuals, then the actor must discriminate
among individuals and the individuals that belong to a category must
be learned by social context. As a classic example, goslings have an innate
disposition to follow “mother,” but the individual that is recognized as
“mother” by a particular gosling is learnt through a process of imprint-
ing (in an earlier sense of the word). Similarly, human children may
possess innate dispositions in their interactions with “mother,” “father,”
“brother,” or “sister,” but the particular individuals who evoke these
dispositions must be learnt from social context.
We probably possess more-or-less discrete instinctive categories for
primary kin, such as “self,” “mother,” “sister,” and “daughter,” and
perhaps for some secondary kin, such as “sister’s daughter” or “daugh -
ter’s daughter.” However, for more distant kin, I suspect we possess a
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258 / David Haig
vague sense of some individuals as closer kin than others, with behav -
ioral dispositions that vary with degree of perceived kinship. Where we
place a particular individual on this continuum will be determined by
things we have been told, and how often, and in what contexts we have
interacted with them, particularly during childhood.
A disposition evolves according to the average relatedness of the
individuals who evoke the disposition, not according to the relatedness
of any particular genealogical category. Thus, instinctive categories
should be distinguished from the categories that would be determined
by an omniscient geneticist. Suppose, for example, that a disposition
is evoked by females, born within a few years of the actor, who live
in close association with the actor’s “mother” during the actor’s own
childhood. Such a disposition will often have been evoked by genealogi -
cal sisters, and the innate category can be labeled, for convenience, as
“sister,” even though it may sometimes have been evoked by individu -
als who were not offspring of the actors’ mothers.
Hamilton’s second principle of the genetical evolution of social
behavior was that “The situations in which a species discriminates in
its social behaviour tend to evolve and multiply in such a way that
the coefficients of relationship involved in each situation become more
nearly determinate” (Hamilton, 1964b). In other words, natural selec -
tion will tend to favor actors who are able to subdivide beneficiaries
into categories with a lower variance of genealogical relatedness. By
this process, innate categories would more nearly come to approximate
g enealogical categories. However, this conclusion should be qualified
by the observation that an individual may benefit from being classi -
fied by an altruistic actor as a member of a category with a coefficient
of relatedness greater than the individual’s “true” relatedness. Thus,
natural selection on actors to make ever finer discriminations of kin -
ship may be opposed by natural selection on a subset of beneficiaries
to confound such discrimination (Haig, 2000a).
Instinctive categories should also be distinguished from the cultural
classification of kin (Feinberg and Ottenheimer, 2001). Cultural evolu -
tion exploits our innate dispositions for various cultural and rational
ends. For example, by defining another individual as a brother, a cul -
tural tradition or a political innovator attempts to evoke dispositions
appropriate to innate brotherhood in interactions with that individual
(Johnson, 1987; Salmon, 1998). To the extent that this evocation is suc -
cessful, culture thereby changes the coefficients of relatedness associated
with an innate category in ongoing natural selection. By this means,
culture can shape the innate taxonomy of kin.
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Genomic Imprinting and the Evolutionary Psychology of Human Kinship / 259
Symmetric Kin
“Self” and “offspring” are symmetric kin. These innate categories are
evolutionarily ancient and undoubtedly have accrued a rich set of innate
dispositions. “Grandoffspring” are also symmetric kin. Genes of mater -
nal and paternal origin favor the same outcomes when fitness tradeoffs
affect symmetric kin alone. Therefore, significant effects of imprinted
genes on symmetric kin are predicted only if a gene’s expression also
affects asymmetric kin. For example, gene expression might mediate a
direct tradeoff between the fitness of symmetric kin (e.g., “self”) and
asymmetric kin (e.g., “mother”).
Perfect symmetry of matrilineal and patrilineal relatedness is
an ideal that is probably rarely realized, although selection favoring
imprinted expression will be weak when asymmetries of relatedness
are small. For example, fullsibs, considered as a genealogical category,
are symmetrically related to ego. However, “fullsibs,” considered as
an innate category, are ego’s matrikin because of the possibility of
undetected cuckoldry. The asymmetry of relatedness associated with
“fullsibs” will be small, however, whenever the probability of shared
paternity is high. As another example, ego’s offspring will be asym -
metrically related to ego when ego’s spouse is asymmetrically related to
ego, as occurs under some forms of inbreeding (Haig, 1999; Wilkins and
Haig, 2003a), but the asymmetries of relatedness will be small, except
under close inbreeding.
Mother
“Mother” is the most important category of matrikin. Strong effects
of imprinted genes are expected in an offspring’s relations with its
mother, both prenatally and postnatally, because mothers have large
effects on the fitness of offspring and are associated with an extreme
asymmetry of relatedness from an outbred offspring’s genetic perspec -
tive (m − p = 1). Paternally expressed genes are predicted to increase the
demands offspring impose on mothers, whereas maternally expressed
genes are predicted to reduce these demands (Wilkins and Haig, 2003b;
Haig, 2004). The strength of these effects will be attenuated when moth -
ers establish stable breeding bonds with a particular male because pater-
nally derived genes of an offspring then have an interest in a mother’s
continued reproduction. Her future offspring are potentially also
the offspring’s father ’s future offspring. However, when a mother
changes partner, her continued reproduction expends limited maternal
i nvestment on maternal halfsibs, who are unrelated rivals from the
perspective of paternally derived genes of existing offspring.
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260 / David Haig
Effects of imprinted genes during fetal development are broadly
consistent with theoretical predictions that paternally expressed genes
should enhance growth and maternally expressed genes should restrain
overgrowth (Eggermann et al., 2008; Haig, 2010). Evolutionary specula -
tion about postnatal effects of imprinted genes on a child’s relations
with his or her mother has focused on the phenotypes of Prader-Willi
syndrome (PWS) and Angelman syndrome (AS), with the former caused
by loss of paternally expressed genes at 15q11–13 and the latter by loss
of maternally expressed genes from the same region (Buiting, 2010).
Therefore, PWS is predicted to exhibit absence, or weak development,
of behaviors that elicit resources from mothers, whereas AS is predicted
to exhibit an overdevelopment of such behaviors (Haig and Wharton,
2 003; Úbeda, 2008).
Infants with PWS exhibit poor suck, weak cry, and excessive sleepi -
ness, suggesting paternally expressed genes from 15q11–13 promote
suckling, strength of cry, and wakefulness (all phenotypes that are
expected to enhance maternal costs). From about the age of natural
weaning, children with PWS develop an insatiable appetite associated
with “foraging” behaviors. These phenotypes have been interpreted as
a pathological expression of “weaning conflicts” that occurred when
our ancestors were transitioning from predominant reliance on the
breast to reliance on supplemental foods (Haig and Wharton, 2003;
Úbeda, 2008).
The happy affect and smiling demeanor of children with AS con -
trast with the less effusive personality of children with PWS. Children
with AS are proposed to express strongly behaviors that normally func -
tion to elicit maternal care, attention, and attachment (Isles et al., 2006;
Brown and Consedine, 2004). However, the overtly social personality of
children with AS is combined with a profound deficit in communication
(Haig, 2008). Speech and gesture are largely absent. Therefore, maternally
expressed genes at 15q11–13 appear necessary for the normal develop -
ment of language. Badcock and Crespi (2006) have suggested that genes
of maternal origin have been selected to act in the language centers
of the child’s brain to promote attentiveness to maternal instruction
and maternal example, coordinating maternal and child needs for the
benefit of the matriline.
Father
Fathers are patrikin of their offspring. Therefore, maternally
expressed genes in offspring are predicted to favor increased demands
on fathers relative to the effects of paternally expressed genes. By
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Genomic Imprinting and the Evolutionary Psychology of Human Kinship / 261
contrast, paternally expressed genes are predicted to show greater
s olicitude to the needs of fathers.
Most mammals probably lack an innate category of “father.” The
evolution of more-or-less stable mating bonds between men and women
has allowed fathers to recognize their offspring and offspring to rec -
ognize their fathers (often with a fair degree of confidence). Human
fathers recognize offspring as babies born to women with whom they
are involved in a more-or-less exclusive sexual relationship. Human
offspring recognize fathers as adult males closely associated with their
mother during infancy and early childhood (Chapais, 2008).
Recognition of fathers means fathers can be avoided as mates.
From the genetic perspective of a daughter, mating with her father is
associated with a direct cost of producing inbred, rather than outbred,
offspring but an indirect benefit of an extra, albeit inbred, paternal half -
sib (with the daughter herself as the mother). The direct cost is experi -
enced equally by the daughter’s maternal and paternal alleles, but the
indirect benefit is experienced solely by the daughter’s paternal alleles.
Therefore, maternally expressed genes are predicted to promote strong
aversions to sexual relations with fathers (Haig, 1999).
Sibs
Uterine sibs sometimes have different fathers and are thereby
matrikin. Paternal-specific expression of imprinted genes is expected
to benefit self at the expense of uterine sibs, whereas maternal-specific
expression is expected to benefit uterine sibs at a cost to self. Two factors
in human evolution have probably had opposing effects on the intensity
of conflict between genes of maternal and paternal origin over relations
with uterine sibs. On the one hand, the evolution of persistent pair -
bonds increased the proportion of uterine sibs that were fullsibs, thus
reducing asymmetries of relatedness and mitigating potential conflicts.
On the other hand, the evolution of shorter interbirth intervals and
prolonged childhoods increased opportunities for competition among
sibs (Kennedy, 2005; Sellen, 2007; Humphrey, 2010).
Sibs are both sharers of common genes and competitors for com -
mon resources; hence, the characteristic admixture of affection and
aggression in many sibling relations. Innate dispositions toward sibs
are expected to be sensitive to relative age, with rivalry more intense
among sibs who are closer in age. An older sib usually has greater power
to help or harm a younger sib than the younger has to help or harm
t he older (although younger sibs will often attempt to recruit the even
greater power of a parent on their behalf). The age-related asymmetry
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in power between a pair of sibs is expected to lessen as they grow older
because they become closer together in relative age.
“Younger uterine sib” is likely to have been an evolutionarily salient
category of matrikin because the arrival of a new baby will often have
been accompanied by a reapportionment of maternal care away from
older sibs. Consider two scenarios. In the first, a child grows up with
h is or her mother and a “father” who disappears and is replaced by
an unfamiliar adult male, after which the mother has a new baby. From
the perspective of the older child, the new baby is associated with a
large asymmetry of relatedness ( m − p = 0.5). In the second scenario,
the “father” and mother remain together for the birth of a new baby.
I n this scenario, the new baby is associated with a much smaller asym -
metry of relatedness because he or she is likely (although not certain)
to be a fullsib of the older child.
New babies evoke a single instinctive category if the innate disposi -
tions of older sibs are the same in the two scenarios. In this case, gene
expression will have evolved according to a gene’s average relatedness
to babies in the different scenarios, weighted by the long-term average
f requencies of each scenario. If the two scenarios evoke different innate
dispositions, then the babies belong to different instinctive categories
a nd gene expression will have evolved according to scenario-specific
coefficients of relatedness.
Innate dispositions of younger children toward “older uterine sibs”
are probably less responsive to a mother’s change of partner than dis -
positions of older children to “younger uterine sibs” because a newborn
child has not herself or himself experienced the change of partner and
has few direct cues about the paternity of older sibs. The latter are
m ore powerful and better informed than younger sibs, and thus may
often set the tone of sibling relations. Infants and toddlers may, at first,
express behaviors designed to ingratiate themselves to older sibs in
an attempt to elicit help and avoid harm, with the overt expression of
rivalry intensifying as disparities of power lessen with age.
Paternal halfsibs are patrikin, but it is unclear whether we have
evolved innate dispositions that are specific for this category of kin.
Relations with paternal halfsibs are usually less intimate than relations
with maternal halfsibs because a father’s contact with his offspring
becomes attenuated once his sexual relations with their mother ends,
especially if he has offspring with another woman. Interactions with
paternal halfsibs are more intense in polygynous households in which the
offspring of two or more women compete for family resources (Jankowiak
and Diderich, 2000), but this situation has probably been less frequent
than living with maternal halfsibs.
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Genomic Imprinting and the Evolutionary Psychology of Human Kinship / 263
Extended Kinship
Asymmetries of matrilineal and patrilineal relatedness are created
whenever individuals of one sex disperse to reproduce, whereas indi -
viduals of the other sex remain in their natal group. If the variance of
reproductive success is similar in the two sexes, then random pairs of
individuals are more likely to share genes of maternal origin than genes
of paternal origin in matrilocal groups with male-biased dispersal, but
the reverse is true in patrilocal groups with female-biased dispersal
(Haig, 2000a, 2010; Brandvain, 2010; Úbeda and Gardner, 2010, 2011; Van
Cleve et al., 2010). Thus, differential dispersal of the sexes can result in
genes having effects that discriminate between matrikin and patrikin
without other individuals being explicitly recognized as belonging to
the mother ’s family or father ’s family.
Whether human reproductive dispersal has been female-biased or
male-biased, on average, is controversial (Ember, 1978; Alvarez, 2004).
What is not controversial is that human groups exhibit a flexibility of
social organization such that ties of matrilineal and patrilineal kinship
predominate in different populations, with strong ties to both sides of
the family maintained in many groups (Rodseth et al., 1991; Marlowe,
2004; Chapais, 2008). Most, if not all, cultures distinguish between matri -
lineal and patrilineal kin. A key unanswered question is whether this
cultural distinction is reinforced by innate dispositions that distinguish
“mother’s kin” from “father’s kin,” or whether the two kinds of kin
are lumped together in a single instinctive category with asymmetries
of relatedness determined by social context.
The recognition of particular individuals as belonging to particu -
lar categories of kin enables discrimination among members of social
groups on the basis of degree of relatedness (nepotism). The evolution -
arily oldest and strongest ties are between mothers and their offspring,
and among uterine sibs. If adults maintain associations with their moth -
ers and uterine sibs, then second-order ties are facilitated between
c hildren and their mother ’s mother and mother’s sibs (Chapais, 2008).
Strong ties of patrilineal kinship are more tenuous because recognition
of fathers is less certain and (evolutionarily) more recent. Perhaps for
these reasons, ties of patrilineal kinship are often reinforced by strong
patriarchal ideologies.
KITH AND KIN
Queller (2011) distinguishes social effects mediated via kin from
those mediated via kith or kind. Kin selection involves fitness effects
on individuals who share genes via genealogical descent. Kind selection
involves fitness effects mediated by identity by state rather than by
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264 / David Haig
descent. Kith selection involves an actor’s effects on other individuals
that feed back to the actor’s own individual or inclusive fitness. I will not
discuss kind selection except to draw attention to Queller ’s perceptive
discussion of the relation between “phenotype matching” and green -
beard effects (Queller, Chaper 1, this volume).
Each individual has two parents who may be genetically unrelated
b ut have a common interest in the survival and reproduction of their
m utual offspring. The parents are each other’s kith, and their relation
engenders a complex intertwining of kith and kin effects because the
a ffines of the father and mother are, respectively, matrikin and patrikin
of the offspring. Put another way, an individual’s matrikin are kith from
the perspective of paternally derived genes, whereas an individual’s
p atrikin are kith from the perspective of maternally derived genes.
Further entanglement of kith and kin occurs when parents are them -
selves kin because of consanguineous matings.
A husband may benefit from investment in the health and well-
being of his wife because this feeds back to increased fitness of his
c hildren. By extension, a husband is kith of his wife’s family, who
are matrikin of his offspring. His investment in relations with his
wife’s parents, and their investment in their son-in-law, may feed back
to increased fitness of his children and their grandchildren. By further
extension, a mother is kith of the paternally derived genes of her own
offspring. These genes have an interest in her well-being to the extent
that the offspring’s individual fitness depends on continued investment
by a healthy mother. Moreover, the offspring’s patrilineal inclusive
fitness may benefit from maternal investment in fullsibs.
Kith relations are contingent in ways that kin relations are not. The
love of a child is more robust to bad behavior by the child than is love
of a spouse to bad behavior by the spouse. The sharing of genes by descent
is a brute fact that is unchanged by changes in the personal relations of
kin, but spousal fitnesses are decoupled when either partner pursues
other reproductive opportunities.
PARTNER CHANGE
In preindustrial societies, it was a lucky child who reached maturity
living in a household with both biological parents because of high rates
of parental death and divorce (Hewlett, 1991; Marlowe, 2005). Some
of our ancestors undoubtedly grew up in families with both parents
present, but others grew up in families in which one or both parents
w ere absent. Behaviors that best promoted inclusive fitness are likely
to have differed between intact and disrupted families because parents
differed in their ability (or willingness) to invest in offspring and divorce
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Genomic Imprinting and the Evolutionary Psychology of Human Kinship / 265
was associated with predictable changes in relatedness for the children
of former marriages.
As long as a couple remains together, their mutual offspring are
f ullsibs and symmetric kin of existing offspring (ignoring, for the
moment, children conceived by extrapair copulations). However, once
p arents change partners, subsequent offspring of the mother and
father are, respectively, maternal halfsibs (matrikin) and paternal half -
sibs (patrikin) of the parents’ mutual offspring. Therefore, a child’s
innate dispositions toward parents and younger sibs should be sensitive
to whether or not his or her parents remain together, and these dispo -
sitions may be particularly sensitive to influences of imprinted genes
after divorce or parental death.
Conflict in a child’s relations with his or her parents is expected
to intensify after parental separation, especially after parents acquire
new partners (Emlen, 1995, 1997b), because genes of maternal origin in
the child have no direct interest in the father ’s continued reproduc -
tion, whereas genes of paternal origin have no direct interest in the
mother’s continued reproduction. Therefore, genes of paternal ori-
gin are expected to promote reduced cooperation with mothers after
divorce, either expressed as increased demands for maternal resources,
increased competition with maternal halfsibs, or reduced expression
of helpful behaviors. Genes of maternal origin are expected to have
opposing effects. As a result, conflicts within the child’s genome are
predicted to intensify after divorce.
When marriages dissolve, children usually remain with their moth -
ers and contact with their fathers declines; social interactions with mater -
nal halfsibs tend to be stronger than with paternal halfsibs; and ties to
the mother’s extended family strengthen, whereas ties to the father’s
family weaken (Furstenberg and Cherlin, 1991). If similar biases were
present in our evolutionary past, then the dissolution of pairbonds would
have been associated with a statistical shift toward greater interaction
with matrikin and a concomitant shift in the selective forces acting on
imprinted genes in children. Paternally derived genes of children would
therefore favor a greater emphasis on self-beneficial behaviors and a
reduced emphasis on kin-beneficial behaviors after parental divorce.
SEXUAL MATURATION
Age at sexual maturity is a pivotal life-history variable (Stearns,
1992). In standard life-history theory, risk of death is the primary factor
favoring earlier reproduction because individuals who delay matura -
tion may not survive to reproduce or may not remain alive long enough
to raise their offspring. Other things being equal, higher mortality of
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young adults favors earlier reproduction. Thus, high risks of subadult
mortality have been proposed to explain early reproduction at small
size in human pygmies (Walker et al., 2006; Migliano et al., 2007). Early
maturation, in this case, is assumed to reflect a genetic change in the
pygmy gene pool. Facultative responses are also possible. Thus, early
reproduction by poor African-American women has been interpreted
as a rational response to low life expectancy (Geronimus, 1997).
Theoretical discussions have focused on effects of pubertal timing
on individual fitness with indirect effects on the fitness of relatives, for
the most part, neglected. In this section, I will focus on indirect effects.
My motivation is that a number of imprinted regions of the human
genome influence pubertal progression and timing. This suggests that
variation in age at maturity has affected the fitness of asymmetric kin,
as well as individual fitness (Haig, 2010). I do not address the relative
importance of direct and indirect effects. The selective forces acting on
pubertal timing are undoubtedly complex, and a comprehensive review
is beyond the scope of this paper.
The timing of ego’s transition to adulthood would have had var-
ied consequences for the fitness of ego’s kin depending on ecological
conditions: whether ego remained in his or her natal group or moved
to another group, how much ego contributed to communal goods, and
the extent to which ego’s offspring competed for limited resources
w ith other group members (Haig, 2010). Rather than attempt a global
analysis that sums fitness effects across all categories of kin, I will
consider a simple model in which the level of x (expressed from one
locus) accelerates ego’s pubertal development, whereas the level of z
(expressed from another locus) decelerates pubertal development, and
consider two ways in which ego’s age at maturity could affect the fitness
of a younger uterine sib.
In the first scenario (another-mouth-to-feed), ego ( m1 = p1 = 1) and
a younger sib (m2 = 0.5 > p2) compete for limited maternal investment
until ego leaves the parental home. Earlier puberty reduces ego’s fit -
ness (∂w1/∂x 0) at a benefit to the younger sib (∂w2/∂x > 0,
∂w2/∂z < 0), who acquires more resources because of reduced competi -
tion with ego. Ego’s genes of paternal origin have less of an interest in
the younger sib’s welfare than ego’s genes of maternal origin. There -
fore, this scenario predicts maternal-specific expression of accelerators
of puberty and paternal-specific expression of decelerators of puberty.
From Eq. (5B) and Eq. (6B), the joint ESS is characterized by
∂ w1 ∂ w2 ∂ w1 ∂w2 (7)
= m2 = – p2
– , .
∂x ∂x ∂z ∂z
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Genomic Imprinting and the Evolutionary Psychology of Human Kinship / 267
Ego is predicted to undergo puberty at a younger age than is optimal
for his or her individual fitness. Production of x is “altruistic” because
i t benefits the younger sib at a cost to self, whereas production of z
i s “selfish” because it benefits self at a cost to the younger sib.
In the second scenario (helper-at-the-nest), ego helps raise the
younger sib by providing child care and contributing food to the
household pot or otherwise reducing maternal workload (Turke, 1988;
Bereczkei and Dunbar, 2002; Kramer, 2002; Hrdy, 2009), but this help is
withdrawn when ego begins to reproduce on his or her own. Earlier
puberty enhances ego’s individual fitness (∂w1/∂x > 0, ∂w1/∂z < 0) at a
cost to the fitness of the younger sib (∂w2/∂x 0). Ego’s genes
of paternal origin have less interest in the fitness of the younger sib
than ego’s genes of maternal origin. Therefore, this scenario predicts
m aternal-specific expression of decelerators of puberty and paternal-
specific expression of accelerators of puberty. The joint ESS is character-
ized by
∂w1 ∂w2 ∂w ∂w2
= – p2 , – 1 = m2 .
∂x ∂x ∂z ∂z (8)
Ego is predicted to undergo puberty at an older age than is optimal
for his or her individual fitness. Production of x is “selfish” because it
benefits self at a cost to the younger sib, whereas production of z is
“altruistic” because it benefits the younger sib at a cost to self.
Human sexual maturation is delayed relative to the other great
apes. The two scenarios make different predictions about the reason
for delayed maturation in the human lineage. In the another-mouth-to-
feed scenario, delayed maturation is favored because it allows ego to
accumulate more embodied capital and become a better parent (Gurven
et al., 2006). In the helper-at-the-nest scenario, delayed maturation is
f avored because ego obtains greater returns from indirect investment
in a younger sib than from direct investment in his or her own offspring
(Reiches et al., 2009; Kramer and Ellison, 2010). The two scenarios are, of
course, not mutually exclusive: A child can both compete with his or her
sibs for limited resources and provide help to his or her parents. More -
over, experience gained in care of younger sibs is a form of embodied
capital when a child has offspring of his or her own.
What would one expect if age at maturity were contingent on
whether ego’s mother and father stayed together for the birth of the
younger sib? Partner change causes a decrease in p2, thus discounting
the cost of competition with the younger sib, or discounting the ben -
efit of helping raise the younger sib, for genes of paternal origin. In the
another-mouth-to-feed scenario, reduced relatedness to younger sibs
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is predicted to favor increased production of z from alleles of paternal
origin to slow the onset of puberty. Partner change, by itself, does not
promote a change in x because m2 is unchanged. However, the accel -
eration of puberty due to increased z may favor enhanced production
of x from alleles of maternal origin as a countermeasure. By contrast,
in the helper-at-the-nest scenario, reduced relatedness to younger sibs
directly favors increased production of x from alleles of paternal origin
t o hasten the onset of puberty.
Blended vs. Unblended Relatedness
What coefficient (or coefficients) of relatedness should be associ-
ated with an innate kinship category in models of inclusive fitness?
Inclusive-fitness theory usually employs a coefficient that averages
relatedness for alleles of maternal and paternal origin, as if maternal
and paternal alleles were blended together in offspring rather than
retaining their separate identities. By contrast, the present paper uses
parent-specific coefficients. There has been surprisingly little discussion
of if, and when, blending is appropriate given that the two approaches
make different kinds of predictions about what should be observed in
nature. I will use the helper-at-the-nest scenario to illustrate the differ-
ence of approach and predictions.
A “conventional” model of pubertal timing would use age at puberty, y,
as the variable for direct optimization. Larger values of y would be associated
with a benefit to the younger sib (dw2/dy) at a cost to self (−dw1/dy). At the
optimal age of puberty,
dw1 dw2
= r2
– , (9)
dy dy
where r2 = (m2 + p2)/2 is a coefficient that blends matrilineal and patrilineal
relatedness. By contrast, an “imprinting” model would treat y as a function
of the level of expression of one or more genes [e.g., y = f(x, z), where x is a
pubertal accelerator and z is a pubertal decelerator] [Eq. (8)]. The model then
makes statements about levels of gene expression at evolutionary equilibrium.
This comparison immediately identifies the attraction of the conventional
approach. The use of blended relatedness allows statements to be made about
phenotype y, whereas the use of parent-specific relatedness views y as an issue
in dispute between opposing parties. The latter models usually do not predict
how the dispute will be resolved at the level of outward phenotype. The dif-
ferences should not be overstated. When considering the effects of husband
replacement on optimal age at puberty, r2 (the blended coefficient) changes
in the same direction as p2 (the patrilineal coefficient), with m2 (the matrilineal
coefficient) unchanged. Therefore, predictions about the direction of change
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Genomic Imprinting and the Evolutionary Psychology of Human Kinship / 269
in phenotype will be similar for the two kinds of model, absent the possibility
that genes of paternal origin have no influence. Nevertheless, I would argue
that parent-specific coefficients are more appropriate than blended coefficients
except in the special case where effects of imprinted alleles can be excluded.
Even in the latter case, my preference is to use parent-specific coefficients and
let the “blending” of relatedness emerge from the mathematics of the model.
Effects of Father Absence
Girls are reported to enter puberty and begin reproduction at younger
ages when raised in households in which biological fathers are absent (Surbey,
1990; Maestripieri et al., 2004). Previous attempts to explain this association
have focused on the role of father absence as a predictor of the daughter’s
expected fitness when “choosing” among alternative reproductive strategies.
Thus, absence of her father during a girl’s early childhood has been proposed
to predict lower paternal investment by the potential fathers of her own off-
spring. Her poor prospects of finding a reliable spouse have been conjectured
to favor an earlier onset of reproduction (Belsky et al., 1991). A somewhat
simpler hypothesis is that daughters themselves expect less parental investment
from delaying maturation in a family with a single parent than in a family in
which both biological parents are present (Ellis, 2004). These hypotheses
interpret the association between father absence and early maturity as the
outcome of a conditional strategy of a common genotype. An alternative
interpretation is that early maturation of daughters and absence of fathers
are genetically correlated (Mendle et al., 2006, 2009).
The helper-at-the-nest scenario predicts earlier menarche in disrupted
families, whereas the another-mouth-to-feed scenario predicts a delay in men-
arche. Therefore, the association of early menarche with father absence is
consistent with older daughters having been selected to delay reproduction
to help mothers raise younger sibs when these are likely to be fullsibs but
not when these are likely to be halfsibs. The assumptions of the model are
simplistic, however. In particular, partner change is assumed to change patri-
lineal relatedness to the younger sib but not to affect the form of the fitness
functions. Thus, the model does not consider direct effects of father absence
on the daughter’s expected fitness or the purported value of father absence
as a cue to the quality of the mating market.
The helper-at-the-nest hypothesis is compatible with the effect of father
absence being either the expression of a conditional strategy or the result of a
genetic correlation. In the first instance, the presence of a girl’s father would
be used as a cue to delay maturation. In the second instance, genes that pre-
dispose men to short-term relationships would become statistically associ-
ated with genes of paternal origin that predispose daughters to mature early,
and thus avoid sacrificing personal reproduction for the benefit of maternal
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halfsibs. Conversely, genes that predispose men to long-term relationships
would become associated with genes that predispose daughters to help
parents raise fullsibs.
Early reproduction by elder daughters maximizes the potential for repro-
ductive overlap between mothers and daughters. Either could help the other
raise offspring at the expense of personal reproduction. What determines
who becomes the helper at whose nest? Cant and Johnstone (2008) have
argued that when a young woman moves into the extended family of her hus-
band, her mother-in-law is predisposed to become the helper at the younger
woman’s nest because the older women is related to the younger’s offspring
(and therefore has a genetic incentive to help), whereas the younger woman
is unrelated to the older’s offspring (and therefore has no genetic incentive to
help). Perhaps a similar dynamic can play out after divorce between a
younger woman and her own mother. In this case, the older woman is sym-
metrically related to the younger woman’s offspring (she is their maternal
grandmother), but genes of paternal origin in the younger woman are unre-
lated to potential offspring of the older woman. This would create a bias in
favor of the older woman helping the younger.
Effects of Birth Order
Elder daughters probably provide most effective help for sibs several
years younger than themselves. Therefore, the helper-at-the-nest hypothesis
predicts earlier menarche for daughters with fewer younger sibs and later
menarche for elder daughters in larger families. A British study found cor-
relations broadly consistent with these predictions: Menarche was delayed in
girls from larger families, but girls born later in a family of a given size had
earlier menarche (Dann and Roberts, 1993). However, in a Spanish study,
first-born daughters had earlier menarche than second-born and third-born
daughters but later menarche than fourth-born or higher-born daughters
(Apraiz, 1999). Effects of birth order on age at menarche may be complex
and highly contingent. The greater competence of elder daughters to provide
help is accompanied by a greater ability to compete for limited resources. Elder
daughters have also spent early childhood in a smaller family than the family
experienced by their younger sibs at the same age.
Expectations about the effects of family size are complicated because
larger families contain more competitors for limited resources but also more
opportunities for help. Analyses that consider effects of birth order commonly
assign lowest birth order to oldest offspring, regardless of family size, and
assign higher birth orders to younger sibs. In this formulation, birth order
is linearly related to ego’s number of older sibs but provides no information
about number of younger sibs (potential beneficiaries of help). From an evo-
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Genomic Imprinting and the Evolutionary Psychology of Human Kinship / 271
lutionary perspective, it might be more informative to perform these analyses
with numbers of older and younger sibs as independent predictors.
Effects of Imprinted Genes
Previous sections have explored the hypothesis that mothers (and mater-
nally derived genes of daughters) benefit from delayed maturation because
of help provided to mothers by older daughters. The effects of father absence
on timing of menarche were construed as supportive of this hypothesis. How-
ever, evidence from the effects of imprinted genes on pubertal progression is
not readily compatible with the helper-at-the-nest hypothesis.
PWS and Silver-Russell syndrome are caused by the absence of paternally
expressed genes or increased dosage of maternally expressed genes. Both
syndromes are associated with reduced linear growth in childhood and a
weak (or absent) pubertal growth spurt (Davies et al., 1988; Wollmann et
al., 1995; Hauffa et al., 2000). These phenotypes suggest matrikin benefited
from slower childhood growth. Moreover, individuals who receive both copies
of chromosome 14 from their mother experience precocious puberty (Kotzot,
2004). This phenotype suggests that earlier puberty benefited matrikin, per-
haps via reduced competition for resources among uterine sibs. Thus, the
effects of imprinted genes are more easily reconciled with the another-
mouth-to-feed scenario than with the helper-at-the nest scenario.
Given the centrality of age of first reproduction to life-history the -
ory, it is perhaps surprising how little we understand about the fitness
tradeoffs that influence variation within and among human popula -
tions in age at puberty in either sex. A detailed study of the effects
of imprinted genes on pubertal timing and progression promises to
provide important clues about the evolution of the distinctive human
life history.
Adolescence
Adolescence has been defined as the period from onset of puberty
to independence from parents (Casey et al., 2010). The duration of
adolescence, by this definition, is highly variable within and among
human populations. Popular opinion views adolescence as a time of
h eightened conflict between parents and offspring and of internal
turmoil within the adolescent psyche. Adolescence is both a period of
reorganization of neural circuits within the brain (Casey et al., 2010) and
a period in which decisions are made about where to live and whom
to marry that may have divergent effects on matrilineal and patrilineal
inclusive fitness of the child and of his or her parents.
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Humans exhibit variation, even within sibships, in the degree to
which adults maintain close ties with parents, siblings, and more dis -
tant kin. Relations with parents during adolescence are often perceived
by young persons as a conflict between their desire for autonomy and
parental attempts to control their choices (Surbey, 1998). Parents often
perceive the adolescent as self-absorbed and as neglecting responsi -
bilities to family. Adolescence is a life-history transition in which the
expression of imprinted genes may have significant effects within the
brain. The maternal and paternal genomes of the adolescent agree about
individual fitness but may disagree over how much individual fitness
should be killed for investment in indirect fitness via kin.
A long tradition in anthropology has emphasized the role of mar-
riage as a form of exchange between patriarchal groups with young
women as the commodity of exchange (Tylor, 1889; Durkheim, 1963;
Lévi-Strauss, 1980). This was sometimes a direct exchange of daughters
between groups, and it sometimes involved a transfer of family wealth,
either a payment for a bride or a payment to place a daughter in a
favorable situation. The freedom of young people to choose their own
partners was curtailed. Conflicts between parents and offspring over
the choice of marriage partners are the stuff of legend and literature.
Parents usually believe they are acting in their child’s best interests
(they believe they have more experience than their child in identifying
a suitable spouse), but evolutionary theory recognizes that the genetic
interests of parent and offspring may diverge.
Material benefits that a spouse brings to a marriage can be trans-
mitted to affinal kin of the spouse, but genetic benefits are transmitted
only to offspring of the marriage. Offspring are therefore expected to
place a greater emphasis than parents on the genetic qualities, rather
t han material resources, provided by mates (Trivers, 1974; Apostolou,
2007a,b; Buunk et al., 2008). Mother and father may disagree over the
relative value of material and genetic benefits provided by potential
spouses of their child if material benefits flow unequally to matrikin and
patrikin. For the same reason, maternal and paternal genomes of the
child may disagree about the optimal attributes of a spouse.
The choice of where and with whom to reside may also have impor-
tant fitness consequences for a young couple. Families can both provide
support for personal reproduction and demand support for kin. The
expression of imprinted genes within the brain raises the possibility
t hat some of these conflicts, over where to live and who to marry, may
be internalized within the adolescent psyche.
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DISCUSSION
Life-history theory is concerned with tradeoffs in fitness: between
the benefits of muscle and fat, between immune function and reproduc-
tive effort, between quantity and quality of offspring, and between
reproduction now and reproduction later. Inclusive-fitness tradeoffs
may involve the personal fitness of different individuals. Social tradeoffs
exist between eating food now or bringing it back to the camp to be
shared, between being a dad or a cad, between sponging on mother’s
kin or father’s kin, and between helping one’s mother raise sibs or
having a child of one’s own. Psychology is concerned with tradeoffs in
mental function: between immediate and delayed gratification, between
empathizing and systemizing, between focused and diffuse attention,
and between impulsiveness and executive control. A key challenge for a
synthesis of these fields will be to understand how psychological trade-
offs mediate life-history tradeoffs.
Our species’ innate taxonomy of kin is defined by evolved disposi -
tions that are directed toward some individuals but not others based
o n environmental cues that are correlated with degree of related -
ness. An innate disposition defines the membership of a category, and
the membership defines the coefficient of relatedness associated with
the category. All individuals who evoke a disposition belong to the
category, and all members of the category determine the relatedness
associated with fitness consequences of the disposition. Thus, innate
k in categories need not correspond exactly to genealogical categories,
a nd, given enough time and genetic variation, the cultural categoriza -
tion of kin can shape our innate dispositions.
An unresolved issue is the richness of our innate categorization of
kin both in terms of the number of different kinds of kin for whom we
have distinct dispositions and in terms of the complexity of disposi -
tions toward each particular category. No one would seriously argue
that innate structure is absent in our interactions with mothers, but
there is no similar consensus over whether we innately distinguish
fullsibs from halfsibs, let alone mother ’s brother ’s daughters from
f ather ’s sister ’s daughters.
When tradeoffs exist between the individual fitnesses of relatives,
inclusive fitness assigns relative values to effects on different categories
of kin based on each category’s degree of relatedness to an actor. For
most categories of kin, relatedness differs for genes of maternal and
paternal origin. The inclusive fitness of maternal and paternal alleles
will be maximized by different allocations of fitness among kin, creating
the potential for conflicting goals within individual organisms and a
deep-seated biological ambivalence in relations among kin.
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Maternal and paternal genes have a common interest in the effec -
tive functioning of the individual actor, but phenotypes that are deter -
mined by agents with different fitness functions are not expected to
show the degree of integration and physiological efficiency one would
expect of a phenotype determined by agents with identical interests.
Perhaps such internal conflicts can partially account for inefficiencies
of mental function and a high frequency of pathology in human social
interactions.
ACKNOWLEDGMENTS
The paper has benefited from the comments of Bernard Crespi, Edgar
Dueñez-Guzman, Sarah Hrdy, Karen Kramer, David Queller, Stephen
Stearns, Robert Trivers, and two anonymous reviewers. The work was
supported by a Collaborative Innovation Award from the Howard
Hughes Medical Institute to Catherine Dulac.
