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Evolutionary context of human development: The cooperative breeding modelS. B. Hrdy
Introduction: moving beyond Bowlby
John Bowlby was the first evolutionary psychologist to explore how selection pressures
encountered by our Pleistocene ancestors, what he termed ‘’the environment of evolutionary
adaptedness’’ (EEA), shaped the development of human infants. Bowlby assumed that the
mother was the primary, typically exclusive, caretaker in the EEA. Later on, he mentioned
the possibility of multiple caretakers, but he nevertheless continued to center his model on a
Victorian division of labor within a pair bond where a sexually monandrous mother nurtured
offspring provisioned by their father. The last quarter century has, however, produced new
evidence from primate sociobiology and from the behavioral ecology of foraging peoples that
challenges this exclusive ‘’sex contract’’ between mother and father as the fundamental
economic unit for childrearing among our ancestors. Attention began to focus on assistance
from group members other than the genetic parents. The long-standing of an EEA
characterized by mother-father childrearing units is being replaced with a model based on
cooperative breeding.
What is meant by ‘’cooperative breeding?
The study of cooperative breeding
The literature on cooperative breeding in vertebrates is divided between studies of birds, of
mammals other than primates, and primates except for humans. Although sometimes
appropriate, this taxonomic compartmentalization has hindered synthetic analyses and led to
a confusing array of taxonomically specific definitions for cooperative breeding. The simple
definition is: a breeding system in which group members, other than the genetic parents
(alloparents), help one or both parents rear their offspring.
Theoretical explanations
At a general level, the altruism of alloparents is explained by Hamilton’s rule: the cost of
helping should be less than benefits to offspring calibrated in line with the alloparent’s
relatedness to his or her charge. Hence alloparents enhance their inclusive fitness by
helping kin. However, there is continuing debate about how important kinship is in
maintaining dispositions to help once they have evolved. In particular, complex patterns of
migration often mean that male and female helpers are not that closely related, yet with
varying levels of commitment, they continue to help.
Cooperative breeding was first studied in social insects and birds, animals without lactation
where nonmothers are just as equipped to feed young as mothers are. Struck by how much
allomothers were helping in hymenopteran social insects, Hamilton (1964) emphasized the
unusually high degree of relatedness between mothers and helpers. His ideas about kin
selection have received strong support. Today, most theorists acknowledge that kinship
facilitates the evolution of cooperative breeding, even if it is not necessarily essential to
maintain helping behaviors in all contexts. Emlen (1997) has played a major role,
emphasizing ecological constraints that discourage relatives from dispersing. Cooperative
breeding is especially likely to evolve where inherited resources are critical for reproduction
since maturing animals must queue up.
Even unrelated allomothers may sometimes benefit from caring for infants. For example,
consider the case of help from prereproductives whose own current breeding opportunities
are limited. Furthermore, as animals age, and especially as female mammals approach the
,end of their reproductive careers at menopause, their threshold for helping may decline,
while their ‘’donative intent’’ increases. In contrast, when physical reserves are at a low
point, or when risks rise high, alloparents with prospects of breeding in the future may
become less altruistic. Still, even helpers with energy to spare or post-reproductives with
little to lose should prioritize their service depending on the degree of relatedness and
especially level of need. The ‘’ideal’’ allomother’s internalized version of Hamilton’s rule
reads: find infants appealing and help them if you can, so long as cost is not prohibitive and
so long as it does not interfere with your own future reproductive career or caring for your
own offspring when you have them.
Ecological and life-history outcomes
Cooperative breeding systems tend to be flexible and dynamic. There are often one or more
mated pairs, but depending on the circumstances, a breeding female may mate
monogamously, polyandrously, or polygynously. Important features of such systems include
delayed dispersal by maturing family members or migration into the group by non-
reproducing adults who are nevertheless responsive to maternal and offspring needs. At the
physiological level there has to be sufficient phenotypic flexibility so individuals can shift
between nonreproductive and reproductive roles. At a cognitive and emotional level, there
has to be some prior predisposition among alloparents to respond to signs or infant need.
That is, the underlying neural circuitry has to be there in both sexes and in virgin and parous
females. As a result of such help, usual quantity versus quality life-history tradeoffs
constraining maternal decision making no longer pertain. This ecological release permits
mothers to produce more, larger, or more closely spaced offspring since the total cost of
rearing each offspring to independence can go up without jeopardizing either her own
survival or that of her offspring.
As early as 1966, Hamilton hypothesized that cooperative breeding would permit slower
maturation. A strong correlation between cooperative breeding and prolonged dependence
has since been documented in birds. Average duration of post-fledging nutritional
dependence was significantly longer in cooperative species, and up to twice as long in the
obligately cooperative. Langen (2000) attributed these extended periods of nutritional
dependence to (a) the reduced cost of parenting produced by a division of labor between
helpers who continued to feed youngsters and mothers who were able to resume breeding,
and (b) the fact that provisioned offspring had less incentive to become independent.
Logically, these same factors should also pertain in cooperatively breeding mammals.
Primate adaptations for cooperative breeding and the case of male primability
The order primates is composed of intensely social species. Many primate attributes
predispose them to evolve some degree of shared caretaking. Relevant preadaptations for
cooperative breeding range from a primate-wide tendency to be attracted to infants, and to
protect infants in the group, to strong urges to hold or carry babies.
Benefits of remaining in their natal group can be documented in all primates. The rule of
thumb among primates is that those who can remain in their natal troop, do so, thereby
enjoying the benefits of social support. For many primates, especially mothers, remaining
among matrilineal kin in multigenerational groups offers special benefits. Enhanced social
support brings with it improved vigilance, stress reduction, health, and fitness benefits, which
probably increase maternal survival rates. Not only does the proximity of matrilineal kin
enhance social support, but a mother’s greater willingness to allow nulliparous daughters
,access to their younger siblings provides inexperienced daughters who remain nearby
greater opportunities to practice and prepare for motherhood.
Over half of all 175 or so species of primates exhibit some form of either biparental care or
shared protection involving allomothers. Such shared care varies from nonexclusive,
occasional care to care so costly that those providing it temporarily forego opportunities to
forage or breed. Among infant-sharing species,, shared care frees mothers to forage with the
result that they breed at a faster pace. Even though the level of shared care varies, the
underlying neural circuitry for responding to infants seems to be universally present.
Many male primates tend to remain aloof from infants and, even in infant-sharing species,
exhibit little interest in holding babies. Surprisingly, though, even in species of primates
which do not normally caretake, males can be primed by experiences to do so, although the
threshold for responding to infants is set higher. The most interesting findings involve
prolactin-mediated systems. Researchers learned that the rise in prolactin levels was more
pronounced among males who had prior caretaking experience. These were impressive
findings, yet it took two decades along with a paradigm shift in the conceptualization of sex
roles before researchers asked the same questions about humans. Only then did we learn
that men cohabiting with pregnant women and new mothers experience hormonal changes
similar to those in cooperatively breeding marmosets. Over the course of a woman’s
pregnancy, the man’s prolactin levels gradually rise. In addition, men exposed to pregnant
women and new babies experience a drop in testosterone after birth. No one is suggesting
that fathers are equivalent to mothers, male caretakers the same as female ones. The point
is: even in animals with low levels of joint caretaking, both sexes can be primed to care.
Why humans must have evolved as cooperative breeders
Humans are costly to produce, mature slowly, and rarely reach nutritional independence
before age 18 or older. Assuming roughly 13 million calories to rear a child from infancy to
nutritional independence, such outlays exceed what a mother could provide by herself. For
this reason, mothers who exclusively relied on ‘’husbands’’ took a chance. But which
children survived when the father died or had little luck in hunting?
Availability of allomothers in pleistocene societies
Researchers estimate that under conditions of low mortality, a twenty-year-old primipara (a
woman who is giving birth for the first time) would have about a 50% chance of having a
forty-year-old mother alive to help her. If higher mortality rates are used, this probability
drops to 25%. Under both mortality conditions, the chance of a new mother having a five-
year old sibling around would be about twice as high as the chance of having a
grandmother. The chances of having one or more cousins would be higher still. Mothers
would typically be coping with incomplete kinship sets. The need to expand the number of
available ‘’kin’’ may help explain why classificatory kinship systems are so common, as well
as why foragers place so much stock in trade networks and other reciprocal relationships.
The debate over residence patterns
Demographic reconstructions of Pleistocene family life rely on assumptions about residence
patterns. Based on a two-pronged set of assumptions, it was long taken for granted that
early humans lived patrilocally. It was assumed that sons remained near father, brothers,
and cousins to form alliances of related males who cooperated to protect their access to
resources. Fairly obviously, if women were moving away to live among their husband’s kin,
this severely constrained the availability of matrilineal relatives. New data, however, suggest
, that ape females do not necessarily migrate. Based on molecular data, wild chimp
‘’brotherhoods’’ may be no more closely related than females are. Furthermore, longitudinal
observations reveal that some females manage to remain in their natal territories. The new
rule of thumb for female chimps is best summarized as ‘’those who can, stay; those who
can’t, leave’’ (Hrdy, 1999).
Allomothers were not just helpful but essential for survival in the Pleistocene
It scarcely comes as news that supportive kin are helpful. What is new is the proposition that
in societies with high rates of mortality, children without allomothers might be significantly
less likely to survive. This is the basis for hypothesizing that alloparental assistance
represents an ancient way of life integral to human adaptations in the EEA.
The sibling factor
One reason why the critical role of allomothers was overlooked was that sociologists studied
Western populations with low rates of child mortality. By the end of the 1980s, however,
anthropologists influenced by sociobiological studies of animals began to ask if allomaternal
assistance mattered for human reproductive success. In a pioneering study, Turke (1988)
found a correlation between the availability of allomaternal assistance and increased
maternal reproductive success in a matrilineal, matrilocal population. In this population,
parents with a daughter to help rear subsequent children had higher reproductive success
than parents whose first two children were sons.
Although the lactating mother would typically be the primary caretaker in the first months, the
prospect of allomaternal assistance promotes maternal commitment. Having child minders
within easy reach, even inexperienced ones, frees the mother to forage more efficiently.
Experienced grandmothers and great-aunts seem to be especially important for the survival
of just-weaned infants. For those whose mother is in poor shape or less than fully
committed, allomothers can be critical at any age.
The importance of real and perceived allomaternal support
Across mammals, the best single predictor of infant survival is maternal commitment. In
humans, however, this commitment is influenced, at least initially, by the mother’s own
perception of pre- and postpartum social support. Mothers short on allomaternal support are
more likely to abandon infants at birth, but even small increases in social support for the
mother enhance how responsive she is to her infant. Even ‘’as if’’ kin in the persons of
visiting nurses can increase maternal respondiveness and lower the incidence of child abuse
in the first two years. When times are tough, the presence of allomaternal support may
matter even more. Prospects for children at risk can be improved through the presence of a
supportive allomother, whether related or an unrelated teacher or mentor.
Hamilton’s rule and the proximate causes of helping
Allomaternal responsiveness
For cooperative breeding to evolve in the first place, group members must be predisposed to
respond to signals of infant need. Most primates are, and females in particular are attracted
to babies and seek to touch, hold, or carry them. Males may be attracted to babies as well,
and in some species have an even lower threshold for responding to them than mothers. In
humans, both sexes respond to infantile behaviors like smiling or babbling and, as first noted
by Konrad Lorenz, both sexes are attracted by ‘’cuteness’’, but there are significant
differences in how sexes respond.
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