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Variable postpartum responsiveness among humans and other primates
with “cooperative breeding”:Acomparativeand
evolutionary perspective
Sarah B. Hrdy
Citrona Farms, 21440 County Road 87, Winters, CA 95694, USA
abstractarticle info
Article history:
Received 7 August 2015
Revised 21 October 2015
Accepted 26 October 2015
Available online 28 October 2015
Keywords:
Allomaternal care
Alloparental provisioning in primates
Cooperative breeding
Postpartum responsiveness
Infanticide
Abandonment
Social support
This article is part of a Special Issue “Parental Care”.
Until recently, evolutionists reconstructingmother–infant bonding among humanancestors relied on nonhuman
primate models characterized by exclusively maternal care, overlooking the highly variable responsiveness ex-
hibited by mothers in species with obligate reliance on allomaternal care and provisioning. It is now increasingly
recognized that apes as large-brained, slow maturing, and nutritionally dependent for so long as early humans
were, could not have evolved unless “alloparents”(group members other than genetic parents), in addition to
parents, had helped mothers to care for and provision offspring, a rearing system known as “cooperative breed-
ing.”Here I review situation-dependent maternal responses ranging from highly possessive to permissive, tem-
porarily distancing, rejecting, or infanticidal, documented for a small subset of cooperatively breeding primates.
As in many mammals, primate maternal responsiveness is influenced by physical condition, endocrinological
priming, prior experience and local environments (especially related to security). But mothers among primates
who evolved as cooperative breeders also appear unusually sensitive to cues of social support. In addition to
more “sapient”or rational decision-making, humankind's deep history of cooperative breeding must be consid-
ered when trying to understand the extremely variable responsiveness of human mothers.
© 2015 Elsevier Inc. All rights reserved.
Adding allomothers to the maternal mix
In the second half of the twentieth century, Jay Rosenblatt, a psycho-
therapist interested in human emotions, turned his attention to the physio-
logical underpinnings of maternal responses. His experiments with rats and
other laboratory animals ushered in motherhood's Age of Psychobiological
Enlightenment. Ensuing research in his and other laboratories illuminated
the roles of hormones acting on the brain during gestation, at birth, and
following the onset of lactation priming mothers to nurture newborns.
Over time, Rosenblatt and colleagues also documented the roles of infantile
cues, local environments and past experiences in eliciting and modulating
maternal behaviors most likely to ensure infant survival and well-being
(reviewed in Lonstein et al., in press; Fleming et al., 2016-in this issue;
Barrett and Fleming, 2011; Numan and Insel, 2003). Their findings
complemented the writings of another psychotherapist and psychiatrist,
John Bowlby, who relied on animal (especially nonhuman primate) models
to inform his ideas about infant-to-mother attachments and the part these
powerful relationships play in future psychological development. These
early research programs tended to focus on mothers as the main—and as
is true for most mammals—the exclusive, nurturers of young.
This central role of mothers was consistent with long-standing
evolutionary assumptions about early humankind's division of labor
between man-the-hunter-provider and mother-the-nurturer (Darwin,
1874; Kaplan et al., 2000; Lovejoy, 1981). And why not? Across traditional
societies, the continued presence of the mother during the first two years is
the single best predictor of infant survival (e.g., Sear and Mace, 2008).
Meanwhile, the model organisms selected for study—such as the rats in
Rosenblatt's lab, or the macaques, baboons, chimpanzees and gorillas in
the laboratory and field studies that Bowlby selected as templates for
early human parenting (1971, 228–229)—fit matrifocal presumptions. So
did caretaking in other model organisms, including mice or marmosets, or
for that matter, humans, provided these mothers were singly housed in
cages, or in the human case spent their days isolated with their infant with-
in walled dwellings rather than in social groups. By century's end, however,
it was increasingly clear that among hominins living by hunting and
gathering in African contexts more typical of what Bowlby referred to as
humankind's Environment of Evolutionary Adaptedness,awidercastof
characters, would have been required to insure survival of offspring.
Given the roughly 13 million calories needed to provision human
offspring between birth and age 18 or so, when children in foraging
societies begin to produce as much as they consume (Kaplan, 1994),
children had to be provisioned long past weaning and required more
than a mother by herself could provide. Given the vagaries of hunting,
Hormones and Behavior 77 (2016) 272–283
E-mail address: sbh@citrona.com.
http://dx.doi.org/10.1016/j.yhbeh.2015.10.016
0018-506X/© 2015 Elsevier Inc. All rights reserved.
Contents lists available at ScienceDirect
Hormones and Behavior
journal homepage: www.elsevier.com/locate/yhbeh
a father by himself also could not provide calories as reliably as growing
children need to be fed (O'Connell et al., 1999). Such constraints led to
customary sharing such that hunters not only provisioned their own
families, but shared with other group members, providing insurance
against recurrent shortages critical for long-term survival (Cashdan,
1990; Marlowe, 2010). Mothers received help not only from fathers
but from other male and female allomothers as well (Hrdy, 1999,
2009). Note that the term “alloparent”is only used when paternity is
known so researchers can ascertain that a given allomother is “other
than”a parent.
Among Africans still living by hunting and gathering when they
were first studied, meat and honey brought in by men accounted
for some 40% of calories consumed. The majority of the diet came
from plant-foods collected by women, with older women past repro-
ductive age contributing disproportionate shares (Hawkes et al., 1989;
Hawkes et al., 1998; Marlowe, 2010:Fig. 5.11). Older siblings and
cousins sometimes provided gathered food such as berries, but more
often they helped with childcare (Crittenden and Marlowe, 2013;
Henry, 2000). Even though mothers remained key attachment figures,
co-sleeping with their infants at night as in all primates, human infants
may be cared for by male and female group members other than
their mother 30% or more of the day time as well as sometimes being
briefly suckled by other lactating women (Hewlett and Winn, 2014;
Hrdy, 2009). In this way, infants become attached to multiple
allomothers rendering standard measures of attachment security such
as Ainsworth's Strange Situation procedure unusable in hunter–gather-
er contexts. Where familiar allomothers are almost always nearby and
infants have several attachment figures, they do not object totemporary
disappearances by their mother the same way as do infants in the
Western samples typically studied by developmental psychologists
(Meehan and Hawks, 2013; cf. prescient early critique by Van
IJzendoorn et al., 1992).
Cooperative breeding followed by (even) longer childhoods,
bigger brains
New evidence and reassessments of older studies are leading to a
paradigm shift among evolutionary anthropologists. It is increasingly
assumed that alloparental care and especially provisioning from males
and females other than parents,in addition to parents, was essential to
keep Pleistocene youngsters safe and fed (Hewlett and Lamb, 2005;
Hrdy, 1999, 2009; Burkart et al., 2009; Konner, 2010; Meehan and
Crittenden, in press; Trevathen and Rosenberg, in press). Nutritional
subsidies provided by allomothers would have been particularly critical
around the time of weaning when primates are most vulnerable to
malnutrition.
The importance of allomaternal provisioning was magnified in
the case of young hominins simultaneously surviving, growing,
and also building and maintaining increasingly large brains (Isler and
van Schaik, 2012). The significance of provisioning past weaning is
underscored by scans of developing human brains indicating that ener-
gy demands to support synapse formation peaks between 4 and 5 years,
after most hunter–gatherer children begin to be, or are, weaned and
when, in many cases, their mother would be pregnant with or nursing
a subsequent infant (Kuzawa et al., 2014). All apes take a long time to
mature, but escalating demands from this unusually greedy organ
consuming glucose at a rate up to 66% of resting metabolism, required
even more extreme trade-offs with somatic growth. Thus youngsters
in the line leading to the genus Homo began growing up even more
slowly than other apes, further extending “childhood”and increasing
the need for nutritional subsidies from male and female group members
other than the mother (Kuzawa et al., 2014).
I have conservatively estimated that cooperative breeding began to
emerge with Homo erectus around two million years ago (Hrdy, 2009).
Paleontologists such as Jeremy De Silva (2011, in press) hypothesize
that selection pressures favoring shared care and provisioning were
underway even earlier, perhaps with australopithecines some three
million years ago. The evolutionary chronology remains murky. But so
far as sequence goes, logic dictates that shared care and provisioning
of young must have begun to emerge before (or co-evolved with?),
the doubling of brain sizes between australopiths and H. erectus (from
ca. 450 to ~900 cm
3
). That is, cooperative breedingmust have preceded
the evolution of hyper-long childhoods and the tripling of brain size to
1350 cm
3
of gray matter that characterize “anatomically modern
humans”(at least by 200,000 years ago) and before “behaviorally
modern”humans' capacities for symbolic thought and sophisticated
language over the past 150,000 years (Fig. 1).
Breeding systems inwhich alloparents in addition to parents help to
care for and provision offspring are uncommon but scarcely unique.
Cooperative breeding has evolved many times across insect, avian and
mammalian taxa. Among vertebrates, cooperative breeding has been
studied longest among birds. Well known for biparental nest-building,
egg tending and care of nestlings (Lynn, 2016-in this issue; Angelier
et al., 2015-in this issue), alloparents in addition to parents are observed
to tend and provision chicks in some nine percent of 10,000 avian spe-
cies (Cockburn, 2006). Longitudinal studies of cooperatively breeding
birds with known individuals and data on lifetime reproductivesuccess
have yielded rich troves of data against which to test Hamilton's Rule
and other theories that explain why individuals might evolve so as to
help care for someone else's offspring (Koenig and Dickinson, 2004).
Since such theories can be applied to cooperation and conflict within
families generally, the term has been extended to humans as well
(Emlen, 1995). It is important to note that the descriptor “cooperative”
notwithstanding “cooperative breeding”does not imply absence of con-
flict. There can be considerable competition between mothers for
allomaternal assistance; between sibs for resources; between males
for mates, even indirect competition between infants for succor. Nor
does shared care and provisioning of young by themselves explain
cooperation in other domains.
Cooperative breedingevolves through various routes. Typically, high
within-group genetic relatedness is required to get it started but the
threshold for shared care of infants is already set low among primates.
Typically new infants are magnetically attractive to at least some
other group members and rudimentary forms of alloparental caretaking
are documented for a slim majority of species of the several hundred
species in this highly social order (Hrdy, 2009).
Even in primate species without full-fledged cooperative breeding
(i.e. extensive alloparental care plus provisioning), mothers may allow
other group members to hold and carry their young resulting in consid-
erable “parenting practice”and sensitization prior to actual parenthood.
For example among infant-sharing langur monkeys (Semnopithecus
entellus) females remain for life in natal groups composed of overlap-
ping generations of matrilineal kin accompanied by one or more
males who enter from outside the group. Since diets are composed
largely of leaves, there is little inter-individual competition for food;
dominance relations among females on average related as closely as
second cousins, tend to be relaxed. Thus pre- and post-reproductive
females are available to protect and/or carry young born to other
females and mothers permit them to. Mothers need not (as among
extremely hierarchical macaques) fear that their infant will fail to be
returned, or as among chimpanzees fear that an unrelated female will
harm (even cannibalize) her infant. Langur mothers tolerate other
females taking their infants as early as the first day of life and
allomothers carry them up to 50% of daytime (Hrdy, 1977: Ch. 7).
Nulliparous juvenile and subadult females are especially attracted to
new babies, take them most frequently, try hardest to pacify them so as
to keep them from complaining and attracting competing caretakers,
and keep hold of borrowed babies for the most minutes (Fig. 2).
Nulliparae are presumably gaining valuable caretaking experience.
Allomothers may also be experientially priming themselves for subse-
quent parenthood (cf. Storey and Ziegler, 2015-in this issue). In addition
to juvenile and subadult females, the second most motivated category
273S.B. Hrdy / Hormones and Behavior 77 (2016) 272–283
of langur allomother includes adult females in the late stages of preg-
nancy, followed by mothers who have just given birth and who briefly
take and inspect a second infant in addition to their own. Like
Rosenblatt's rats, these langurs are presumably hormonally primed to
be especially attracted to babies (Hrdy, 1977: Tables 7.5 and 7.9).
Difficulties defining solicitous vs. “abusive”care
Depending on their own reproductive state, langur allomothers
exhibit varying levels of interest and solicitude. In contrast to either
inexperienced or very pregnant females, experienced parous females
will take and inspect infants but soon tire of them. Desperately clinging
infants may be forcibly pushed away, held upside down to inspect their
genitals, even pressed against the ground, or sat upon, resulting in pite-
ous complaints prompting retrieval by either the mother or another
allomother. Brutal as parous allomothers appear (Fig. 3), no injury to
borrowed charges has been observed. Even an infant left on the ground
will be picked up by either the mother or another allomother within
two minutes.
Langur infants do not like being pulled from their mother and com-
plain loudly. Nevertheless, infant-sharing is typical for allbut a few spe-
cies in the sub-family Colobinae and over half of the several hundred
species in the order Primates exhibit at least some allomaternal care.
Mothers who allow their infants to be taken are neither neglectful nor
abusive. Rather, they are preoccupied with staying fed and benefit
from having group members whose intentions are sufficiently benign
that a mother can temporarily entrust care of her infant to others. In
this respect it is worth noting that the handful of non-infant-sharing
exceptions within the sub-family colobinae are all species where
females move between groups and so (like chimpanzees) rarely have
Fig. 1. Artist Viktor Deak's imaginative reconstruction of a H. erectus mother passing her infant to a juvenile allomother 1.8 million years ago (copyright SBH Lit, reproduced with
permission).
Fig. 2. A pregnant nullipara takes a langur infant from a juvenile female who has beencarrying it.
274 S.B. Hrdy / Hormones and Behavior 77 (2016) 272–283
matrilineal kin nearby (Hrdy, 2009). It takes two conditions for shared
care to emerge. The normal possessiveness and extreme protectiveness
of a new mother has to be relaxed, and she has to feel sufficiently
trusting or tolerant of nearby group members to allow another individ-
ual access to her new infant. Obviously it would be interesting to know
more about neuroendocrinological status of postpartum primates
with and without trusted associates nearby, but I know of no relevant
research.
As Drury et al. (2016-in this issue) emphasize, and the langur cases
discussed above illustrate, caution is called for when applying a cultur-
ally laden term like “abuse”to nonhuman animals. A lot depends on
who is doing what to whom, why, and especially on whether or not
the “abused”infant is harmed. One species' “negative early caregiving”
is another creature's normal. Furthermore, in environments where it
is as challenging to avoid being eaten as it is to stay fed, mothers
who reject their infants or leave a vocalizing infant unattended, would
be unlikely to remain mothers for long. Unless that rejecting mother
learned from that experience to be more attentive with subsequent in-
fants, heritable traits leading to maternal neglect would be selected
against and disappear form the population's gene pool. When a mother
forcibly restrains her infant, she is less likely to be abusing it than
protecting her infant from some perceived threat. Nor can infant
complaints be taken as reliable indicators of maternal “abuse.”Infants
protest when mothers deem it too dangerous for them to move about
or at weaning, when tantrums may be accompanied by rough but
non-injurious punishments (e.g., slapping).
Primate mothers closely resemble other mammals among whom
steroid hormones during gestation, peptide hormones after birth, and
neurological systems all collaborate to render it rewarding for mothers
to taste, smell, and remain close to their babies and bond to them
(Feldman et al., 2010; Jenkins et al., 2016-in this issue;Lonstein et al.,
in press; Numan and Insel, 2003; Pryce et al., 1993). Under natural con-
ditions in the wild it takes dire circumstances for an experienced an-
thropoid mother to abandon her infant and they are even less likely to
do so than parous mothers among many nonprimate mammalian spe-
cies. Rare exceptions include a mother gorilla with twins who became
ill, or a langur mother who found herself subject to chronic stalking by
an infanticidal male (reviewed in Hrdy, 1999). Ape mothers in particu-
lar stand out for single-minded, highly protective possessiveness, re-
maining in continuous skin-to-skin contact with their baby for months
after birth. It is against this primate background that the extremely
variable responsiveness of human mothers seems unusual. For compa-
rable variability we must turn to other primates with shared care and
provisioning.
From shared care to full-fledged cooperative breeding
Since langurs are leaf-eaters, there would be little advantage to
allomaternal provisioning and they do not share food. Among primates
generally, shared care is fairly common, but provisioning the offspring
of other primates either via allomaternal suckling or actual delivery of
food to nearly weaned immatures is very unusual. Animal prey in
particular is highly prized among those apes that consume it, and it is
difficult to explain how voluntary delivery and offering of prey to others
ever became established in the hominin line (Hrdy, in press-b). Never-
theless,such provisioning must have been essential to permit the evolu-
tion of the larger brains and longer childhoods in the line of apes leading
to the genus Homo.
Today, the best documented cases of provisioning among still extant
primates are found among phylogenetically very distant New World
monkeys, monogamous species in the genus Aotus (Fernandez-Duque
et al., 2009) and the many species in the subfamily Callitrichidae
where the majority of calories consumed by just-weaned young are
provided by fathers and other allomothers (Burkart and Finkenwirth,
2015; Rapaport, 2006) as is also the case among human hunter–gath-
erers. Once underway, with alloparental provisioning as well as obligate
care embedded in the life history of a particular species, cooperative
breeding plays out in various ways. In the case of cooperative breeders
characterized by rigid female dominance hierarchies as marmosets
and tamarins are, millions of years of cooperative breeding have led to
the evolution of some highly derived and quite surprising, physiological
adaptations. Dominant female have been selected so as to eliminate
infants born to subordinates thereby increasing the number of helpers
available for their own offspring.
As predicted by Rosenblatt's work, there tends to be a correlation be-
tween urinary estradiol levels during pregnancy and post-partum
infant-directed behaviors (such as licking and carrying) among
callitrichids (e.g. red-bellied tamarins, Saguinus laibatus,Pryce et al.,
1993). Nevertheless, there are circumstances when pregnant callitrichids
respond quite differently. Instead of extremely pregnant females finding
babies especially attractive and seeking to nurture them, some marmoset
and tamarin females in the late stages of pregnancy actually find infants
aversive. Even experienced multiparous marmosets who previously suc-
cessfully reared young exhibit longer latencies to approach during late
pregnancy (Saltzman and Abbott, 2005).
Some dominant females in the later stages of pregnancy even attack
and bite to death infants born to subordinates. This risk probably
explains why subordinate females avoid reproduction in the vicinity
of potentially infanticidal alphas—sometimes their own mother
(Digby, 2001; Digby and Saltzman, 2009; Saltzman and Abbott, 2005,
Fig. 3. A middle-aged, multiparous allomother who has taken and infant but is tired of
carryingit, presses it to the ground. The infant was quickly retrieved, uninjured, by anoth-
er allomother (S.B. Hrdy/Anthro-photo).
275S.B. Hrdy / Hormones and Behavior 77 (2016) 272–283
see also Clutton-Brock, in press for similar cases among other coopera-
tively breeding mammals). In spite of such risks, subordinate female
common marmosets sometimes do risk giving birth, as for example
after ovulating and soliciting matings from males belonging to another
group during inter-troop encounters (Lazaro-Perea, 2001). Such
inconsistencies underscore just how situation-dependent and variable
reproductive and parenting behaviors among cooperative breeders are.
Across vertebrates, alloparental care combined with provisioning
have most often evolved among highly social species already character-
ized by altricial, fairly slow maturing, young under ecological conditions
which make it especially challenging to keep recently fledged or
weaned offspring provided with palatable foods. Such conditions
include extreme fluctuations in rainfall or difficult-to-extract or process
food requiring adult provisioning (Hrdy, 2009; Jetz and Rubenstein,
2011). As it happens, such conditions pertained in areas of early
Pleistocene Africa 1.8 million or so years ago, areas where earlyhominin
remains are found today (Magill et al., 2013; O'Connell et al., 2002;
Potts, 1996).
Although relatively recent by the standards of cooperative breed-
ing's far longer evolutionary history among marmosets and tamarins,
two to three million years is sufficient for Darwinian selection to have
begun to shape responses of all involved, mothers, fathers, alloparents
and infants. Elsewhere I have explored cooperative breeding's implica-
tions for the unusually variable expression of paternal commitment
within and between human societies (Hrdy, 2008, 2009). I have also
examinedhow the need to appeal to, and elicit succor from, allomothers
as well as mothers would have affected infant development, generating
novel ape phenotypes which over evolutionary time would have been
subjected to novel selection pressures favoring those immature apes
best at monitoring the thoughts and feelings of others and ingratiating
themselves with prospective caretakers, resulting in the emergence as
early as several million years ago of more “emotionally modern”apes
better able to read, and more interested in, the intentions of others
(Hrdy, 2009; in press-a). Here I focus on the extreme variability of re-
sponsiveness in pregnant females and new mothers, both those with
and without prior maternal experiences.
Human mothers as outliers among hominoid primates
Nonhuman ape mothers are all characterized by exclusive care of
their new infants. They stand out for single-minded dedication to their
infants. Poachers are well aware that to capture a baby gorilla or orang-
utan to sell in local markets, they first must shoot the highly protective
mother. Otherwise she is not going to let go. Theirs is a reflexive protec-
tiveness. Similarly, Old World monkey mothers carry and suckle infants
no matter what, even those born with palsy or missing limbs (Berkson,
1974; Turner et al., 2005). Both Old World monkey and ape mothers
continue to carry for days the desiccating corpses of infants that die
(Fig. 4). Exceptions to such reflexive protectiveness among wild primate
mothers almost all fall among species with obligate allomaternal care.
For example, among cooperatively breeding callitrichids, even experi-
enced mothers who have already successfully reared infants may not
only ignore infants who cease to move, but sometimes abandon still vo-
calizing infants.
Infanticide is widespread among primates and a major source of
infant mortality. However, perpetrators virtually always attack the
offspring of others, not their own infants (Hausfater and Hrdy, 1984;
Parmigiani and vom Saal, 1994; van Schaik and Janson, 2001). Yes,
inexperienced first-time monkey and ape mothers may prove in-
competent or neglectful, and may even abandon infants altogether,
especially in captivity or if a primipara lacked opportunities for
prior caretaking experiences. Cases of mothers dragging or
neglecting infants such as those reported among free-ranging
Japanese macaques (e.g., Hiraiwa, 1981; Schino and Troisi, 2005)
typically involve first-time young mothers or females who had lost
their own mother and so presumably had less exposure to younger
sibs.Intheserespects,humanprimatesareoutliers.Asinotherpri-
mates, infanticide is widely documented across both traditional
and modern human societies. But unlike other primates, the likeliest
perpetrator is the mother herself, usually in the hours or days right
after birth. With the exception of cases summarized below, all in-
volving species with obligate allomaternal care, I know of no other
instances from nature where an experienced nonhuman primate
mother inflicted injury on her own infant.
As in all mammals, new human mothers are acutely sensitive
to the sight, smells and vocalizations of newborns. Yet unlike their
self-sacrificingly dedicated Great Ape relations, there are a range of
circumstances where postpartum mothers, including even experienced
mothers, seem peculiarly insensitive to infantile appeal (kindchenschema)
or infantile signals of distress, voluntarily abandoning or even killing their
own infants (Drury et al., 2016-in this issue; Overpeck et al., 1998;
Resnick, 1970).
Fig. 4. Old World monkey and non-human ape mothers are not known to discriminate based on infantile attributes and will continue to carry the corpse of a dead baby for days as this
young langur monkey mother is doing (S.B. Hrdy/AnthroPhoto).
276 S.B. Hrdy / Hormones and Behavior 77 (2016) 272–283
Maternal rejection of newborn humans is understandably a sensitive
topic. Even anthropologists with relevant data can be reluctant to pub-
lish them. Nevertheless, numerous historical, sociological, institutional
as well as ethnographic sources, testify to the widespread occurrence
of postpartum abandonments or infanticide of newborns considered
premature or otherwise poorly timed (e.g., born too close to an older
sib); born female when males are preferred, or vice versa, or born defec-
tive in various real or culturally arbitrary ways rendering them unlikely
to prosper. Space here does not permit review of what is a vast, if largely
non-quantitative, often anecdotal or otherwise problematic literature
(see Hrdy,1999:chapters12–14; regarding scholarly reluctance to pub-
lish, see pp. 289–297).
Curiously insensitive, and in the human case, even discriminating,
primate mothers
Whether in industrialized societies where infanticide is against the
law or in traditional societies where abandonment or infanticide are
regarded as lamentable but sometimes necessary, this under-reported
and way under-studied phenomena cannot always, or even typically,
be dismissed as the result of “deranged”or pathological behavior.
Rather, the scale and patterning of maternal abandonment and infanti-
cide among humans (e.g., Badinter, 1981; Bonnet, 1993; Bugos and
McCarthy, 1984; Schiefenhövel, 1989; Sheper-Hughes, 1992)raises
the possibility of some dampening of maternal responses in postpartum
mothers, a dampening that in some cases permits new mothers to
discriminate against offspring born at the “wrong”time or possessing
the “wrong”attributes, in ways that have not been observed in other
anthropoid primates. Such limited ethological evidence as is available
also suggests that mothers may sometimes find it aversive rather
than rewarding to hear cries from a very low birthweight, premature
or sickly-seeming infant or to look at a baby with facial disfigurement
(Barden et al., 1989; Frodi et al., 1978; Mann, 1992). Such effects may
co-occur or be exacerbated in mothers experiencing severe postpartum
depression, stress, or anxiety (Agrati and Lonstein, 2016-in this issue;
Brummelte and Galea, 2015-in this issue; Lonstein et al., in press;
Haim et al., 2016-in this issue).
In respect to relinquishing care or, under certain circumstances,
ceasing altogether to care for babies, human mothers more nearly
resemble non-primate litter-bearing mammals than other higher pri-
mates. Faced with severe scarcity or when disturbed, mammalian
mothers are known to abandon dens or nests, or as in the case of
lions, whole litters. Mothers with multiple young may also discriminate
between infants based on specific attributes such as a kangaroo mother
closely pursued by a predator who jettisons an older joey while
retaining a tinier joey latched to her teat or a mother with a large litter
who shunts aside a runt (e.g., Hoogland, 1994, for prairie dogs; the
author's personal observationfor domestic dogs). Litter-bearing rodents
as well may differentially care for young in ways that differentially
affects their development (Jenkins et al., 2016-in this issue; Ragan
et al., 2016-in this issue).
Over the course of hominin evolution, more closely stacked
dependents emerged in concert with allomaternal provisioning which
permitted shorter intervals between births of slow maturing young.
These “as-if”litters would have producedcircumstances where hominin
mothers benefit from being able to calibrate investment in line with
local conditions but also in line with attributes relevant to one infant's
viability relative to that of a current older, or as yet unborn, sibling. I hy-
pothesize that more discriminative maternal responsiveness at emo-
tional levels not only co-evolved in humans with larger brains,
increased foresight and capacities for conscious decision-making and
various cultural criteria—a generally accepted premise—but also co-
evolved with a dampening of reflexive maternal responsiveness
postpartum that facilitated the adjustment of a mother's level of com-
mitment in line with how much allomaternal support was available.
Apart from humans, the main (and so far only?) primate instances of
maternal infanticide known to involve experienced mothers under
natural conditions occurred in species with obligate allomaternal care.
Every report known to me is summarized below. All occurred either
among monogamous species with obligate paternal care or else
among monogamous or polyandrous cooperative breeders with
alloparental as well as parental care and provisioning. Perhaps because
Callitrichidae have relied on allomaternal care and provisioning many
millions of years longer than hominins have, the “dampening”processes
involved are even more pronounced.
Comparative evidence from long-time cooperative breeders
As Bales and Saltzman (2016-in this issue) and Drury et al. (2016-in
this issue) stress, it is important to select ethologically appropriate
models. But in the case of social neuroscientists interested in the under-
pinnings of maternal responses under the range of conditions which
characterized human mothers during the course of evolution, this pre-
sents special challenges. Neither the often-studied rhesus macaque
nor any of our phylogenetically closest Great Ape relations whopossess
human-like neural structures and nearly identical reproductive physiol-
ogies, raise infants the way our hominin ancestors did. But if we turn to
other primates with cooperative breeding, they are not only phyloge-
netically very distant from humans, they have also been cooperative
breeders millions of years longer under conditions of within-group
breeding competition far more extreme than those among band-level
hunter–gatherers.
Humans last sh ared common ancestors wit h cooperatively breed-
ing New World monkeys in the subfamily Callitrichidae more than
35 million years ago. During much of that time, fast-breeding marmo-
set and tamarin mothers were producing twins or triplets weighing up
to one fifth of their body weight as often as twice a year, in the process
becoming neurologically as well as physiologically adapted to
allomaternal assistance. I hypothesize that their obligate reliance on
allomaternal support was implicated in the evolution in these species
of mechanisms for somehow bypassing ordinary neurophysiological se-
quelae to the hormonal changes accompanying primate gestation.
When late-stage pregnant females encounter infants, instead of
responding positively, they attack them. Of seven wild callitrichids ob-
served biting to death another female's infant, five were pregnant
(Culot et al., 2011: Table 1). These pregnant females ignored visual
cues or distress vocalizations that in other contexts signal “cuteness”
or elicit care, sometimes targeting the vocalizing face.
Even stranger, in primates with obligate allomaternal care, new
mothers may sometimes directly attack their own infants. Under pres-
sure to reduce metabolic costs from carrying and nursing babies, tama-
rin and marmoset mothers in the genera Callithrix and Saguinus,aswell
as mothers among monogamous, biparental care species in the genera
Callicebus and Aotus, pass babies off to others (usually males) after
they suckle them. But if babies continue to cling, they may attempt to
forcibly scrape babies off, or bite their hands or feet. In extreme cases,
mothers may bite off hands in their effort to force clinging babies to
let go (Cooper, 1964, cited in Hershkovitz, 1977:788; Hoffman et al.,
1995:402; Huck and Fernandez-Duque, 2013:378; Ross et al., 2007).
Unless fathers pick them up, complaining neonates may be left on the
ground where they fell (e.g., Epple, 1970:66).
Interpreting surprisingly high frequencies of rejected infants among
callitrichids is problematic. Because these tiny, arboreal, monkeys are
difficult to observe in the forests where they live, most reports of
abandonments derive from infants or their corpses, found on the floor
of breeding colonies (Bardi et al., 2001; Epple, 1970:66; Johnson et al.,
1991; Rothe, 1975:316–317) and even species of primates not known
to reject infants in the wild are known to do so in captivity. But even
taking this consideration into account, rates of infant rejection among
callitrichids seem unusually high. Furthermore, only among cooperatively
277S.B. Hrdy / Hormones and Behavior 77 (2016) 272–283
breeding primates have mothers in natural habitats ever been observed to
deliberately wound their own infants.
In tens of thousands of hours that chimpanzees, baboons, and other
primates have been observed in nature, mothers are almost unfailingly
protective. Yet in spite of far fewer observation hours, monogamous or
cooperatively breeding species with obligate reliance on allomaternal
care are the only nonhuman primates where mothers living in natural
settings have been observed to deliberately mutilate, and in three
cases, almost certainly kill, their own infants. These mothers appear
sufficiently inured to infantile signals of distress as to not only push
their baby away, but in their effort to unburden themselves, bite it
to death.
By now, infanticide (mostly by males but also by females) is reported
for more than 50 species of primates (Palombit, 2012). But in these pro-
simian, monkey and ape cases individuals attack the offspring of others.
The only three exceptions of maternal infanticide from nature involve
species with obligate allomaternal care. It's worth a closer look.
To date there are ten reports of infanticide among wild-living non-
human primates with either obligate paternal or alloparental care:
nine involve cooperatively breeding callitrichids (Bezerra et al., 2007;
Culot et al., 2011: Table 1; Digby and Saltzman, 2009; Tirado-Herrera
et al., 2001) and one involves monogamous biparental-care Callicebus
nigrifrons (Cäsar et al., 2008). In seven of these ten cases, a breeding
female killed another female'sinfant. But in the Callicebus and two
tamarin cases, living babies were almost certainly bitten to death by
their own mothers.
The existence of many firsthand observations of maternal rejections
raises the possibility that some of the many dozens of mutilated, often
headless or partially cannibalized, infants found on the floor of breeding
colonies were also bitten by mothers (Bardi et al., 2001). Quite possibly,
a nonresponsive infant gets reclassified as “prey”, inviting consumption.
But the contrast with other primate mothers who remain protective
of comatose or dead babies for days leads me to suspect some neuro-
physiological dampening of bonding mechanisms in postpartum
callitrichids. This might help explain why some marmoset mothers fail
to discriminate between their own infant and unfamiliar infants
matched for age (Saltzman and Abbott, 2005).
Neural overrides to gestational and postpartum priming?
Clearly, the acute responsiveness to infantile signals of need and
distress that ordinarily emerges during mammalian pregnancy and
which in some species emerges following previous exposure to infants
(Akbari et al., submitted for publication; Drury et al., 2016-in this
issue; Lonstein et al., in press; Numan and Insel, 2003)doesnotalways
operate. Such responses seem particularly variable among primates
with obligate reliance on allomaternal care and provisioning. In field
primatology's first report of maternal infanticide (Tirado-Herrera et al.,
2001), a saddle-backed tamarin (Saguinus fusicollis) gave birth in a
group containing several males and a second (pregnant) female. On its
first day of life, the mother dropped her infant several times, only to
have it retrieved by one of the males, until when once again reunited
with its mother, she “took a vertical position on a (tree) trunk, gripped
the infant, and bit into its face. The infant moved its arms and legs.
Further bites were directed to the face and to the brain case.”The corpse
fell to the ground, revealing that the baby's brain had been entirely
consumed. In the second case, a mother mustached tamarin (Saguinus
mystax), who had successfully reared three sets of twins at times
when four or five males were on hand to help, gave birth when there
were only two or three males as well as a second breeding female in
the group. This mother as well was observed biting and eating
the head of her baby. Her son was vocalizing shortly before, but ob-
servers could not be certain he was still alive when the mother began
biting (Culot et al., 2011:182).In a third case, a black-fronted titi mother
(C. nigrifrons) gave birth to a healthy male carried mostly by her mate
until the third day, when, on its being returned to his mother, she
began to bite the face of her vocalizing son, eventually dropping the
corpse to the ground (Cäsar et al., 2008).
Apart from humans, only among these New World monkeys with
extensive paternal and/or alloparental involvement do we find primate
mothers under natural conditions sufficiently inured to infantile signals
of distress as to deliberately injure one, even mutilate a still vocalizing
face or preferentially consume the brains—a risky predilection in a
mother who, like most mammals, will consume the placenta right
after giving birth. Under most conditions such a mother has good rea-
sons to distinguish her neonate from, say, the afterbirth.
Obviously these mothers are not conceiving and gestating babies in
order to discard or recycle them. Abandonmentand cannibalism are last
resorts. Faced with insufficient assistance and hence a low likelihood of
successfully rearing her infant(s), a cooperatively breeding mother's
best option would be to terminate investment, the sooner the better
(cf. the Bruce Effect where spontaneous abortions or reabsorption of
fetuses occurs in pregnant mice, langurs or gelada baboons when in
the presence of a potentially infanticidal conspecific). Systematic analy-
ses of circumstances surrounding a large sample of captive callitrichid
rejections are consistent with this interpretation. Massimo Bardi et al.
(2001) used stepwise multiple regression to evaluate factors affecting
survival to one year for 1093 Saguinus oedipus born between 1984 and
1993 at the New England Regional Primate Center. Fifty percent (546)
were rejected and an additional 12% (134) were killed before they
could be removed and hand-reared. In 89% of these cases, termination
of investment ended within three days of birth. It is worth noting that
the postpartum timing of these rejections echoes the timing of infanti-
cides among both traditional (Hrdy, 1999) and modern human socie-
ties. Of 3312 infanticides recorded by the U.S. Centers for Disease
Control between 1989 and 1998, the incidence peaked in the first
week, with 82.6% of cases occurring on the first day. Thus, mothers
were almost certainly present and implicated (Paulozzi, 2002; see also
Bonnet, 1993; Overpeck et al., 1998).
Among callitrichids, mothers are the major caretakers immediately
after birth making it likely that mothers are primarily responsible for
these rejections (Bardi et al., 2001:167). Bardi's further analysis
suggests that these mothers were responding to the availability of care-
takers or topre- or postpartum signals of paternal willingness to help. In
Bardi's breeding colony sample the best predictor of maternal rejection
was shortage of allomaternal assistance. When older siblings were avail-
able 54.9% of infants were accepted, compared with 17.2%when absent.
Mothers in poor health and those bearing triplets were more likely to
abuse infants. Rates of rejection were also higher for inexperienced
(64.1%) compared with experienced mothers (39.5%) and for younger
parents of either sex than for older ones. Nevertheless, infanticide in
the wild cases cannot be attributed to inexperienced individuals since
mothers who abused or rejected offspring were known to have success-
fully reared young previously. Furthermore it is noteworthy that in
Bardi's sample, the tamarin mothers without prior caretaking experi-
ence were less, not more, likely than experienced mothers to mutilate
babies they rejected. Compared with the 8.2% of inexperienced mothers
who abused infants the rate for parous females was nearly twice that
(15.2%) suggesting that mutilations were due to something other than
inexperience or incompetence.
Are callitrichid mothers polling available help?
Once established, dampening of maternal responsiveness provides
novel evolutionary opportunities. In the case of callitrichids, it may
have provided opportunities for mothers to elicit information about
availability of help. Adult male callitrichids, especially progenitors,
1
1
The usual uncertainty surrounding primate paternity is especiallycomplicated among
callitrichids. Not onlycan twins and tripletsbe sired by more than one of the severalmales
a polyandrous mothermates with, but the possibility ofcells migrating between fetusesin
utero can result in chimeric individuals (Ross et al., 2007).
278 S.B. Hrdy / Hormones and Behavior 77 (2016) 272–283
respond to infant vocalizations as readily as mothers do (Sánchez et al.,
2014), and sometimes more readily. When mothers push their babies
(typically twins) off and they vocalize, it is males who usually retrieve
and carry them, eventually returning them to their mother to nurse.
Thus rejecting mothers can poll fathers, gaining information about
their readiness to retrieve and carry infants. Some information about
probable male assistance may already have surfaced prior to birth.
Tamarin fathers gain up to 8% of their body weight during a mate's
pregnancy in anticipation of the extra effort they will expend carrying
babies (Ziegler et al., 2004). No doubt building up reserves in advance
makes energetic sense, but Toni Ziegler's findings suggest that fathers
may also be secondarily signaling to mothers their willingness to stay
and to help rear young.
The point is, some maternal rejections appear “strategic”rather than
terminal. Detailed observations of parental care among wild tamarins
(Leontopithecus rosalia) indicate that mothers adjust investment in
line with how much others are providing (Bales et al., 2002). This may
explain the curious observation that marmoset males, but not mothers,
find chimeric infants especially attractive (Ross et al., 2007,forCallithrix
kuhlii). Perhaps mothers can afford to “relax”if several males (including
progenitors, partial progenitors, or former mates who are possibly
progenitors) are going to pick up the slack. In any event, if the mother
repeats her rejections and no other allomother intervenes, the father
too may terminate investment.
Gauging her mate's probable responsiveness is valuable feedback for
a mother to have sooner rather than later. Males with experience or in
good condition are especially responsive as reflected both by behavior
and in higher prolactin levels (Storey and Ziegler, 2015-in this issue).
Elsewhere, I have speculated that neuroendocrinological changes dur-
ing maternally imposed exposure of males to infants, along with
prolonged intimate contact with infants, might also facilitate the emer-
gence of male provisioning in callitrichids and may perhaps have done
so in prehuman (hominin) apes as well (Hrdy, in press-b)(Fig. 5).
A mother is not a mother is not a mother, and certainly not
amarmoset
Callitrichids, like early humans, make their living by both huntingfor
(small) prey and gathering plant foods. In contrast to other Great Apes,
but again, like callitrichids, humans are highly adaptable colonizing
primates whose potential for rapid reproduction when conditions are
good allows them to bounce back after recurrent local population
crashes. Yet these tiny-brained, arboreal, squirrel-like monkeys not
only occupy different habitats but utterly different sensory worlds
than any ape does. Phylogenetically distant callitrichids also have very
different reproductive physiologies characterized by postpartum estrus,
multiple births, a simplex uterus, partible paternity and chimeric prog-
eny. Nor does anything in the ethnographic record for band-level
human hunter–gatherers indicate callitrichid-like skews in female re-
productive success (e.g., Tardif et al., 2013) or suggest that pregnant
hunter–gatherers are motivated to harm infants born to group-mates.
So far as humans go, the sort of competition between mothers that
would lead to one mother eliminating the offspring of another has
only been reported for the more stratified, propertied, human societies
such as emerged in the past 20,000 years. Female reproductive compe-
tition can be particularly pronounced in post-Neolithic societies where
inheritance of land or other resources are at issue. Such cases include
exploitation of reproductively disenfranchised slaves or subordinates,
or wet-nurses coerced into caring for and even suckling the young of
more dominant group members at the expense of their own infants'
survival or reproductive opportunities (reviewed in Hrdy, 1999).
However it is unclear how relevant to human neurophysiology such
relatively recent customs might be.
Clearly,humansare physiologically and cognitively very, very differ-
ent from callitrichids, able to consciously assess current dilemmas and
to make predictions about the future Yet what human mothers share
with these otherwise phylogenetically distant primate relations is an
evolutionary legacy of relying on extensive allomaternal care and provi-
sioning in order to rear young, and perhaps because of it (?) a situation-
dependent dampening of maternal responsiveness in the postpartum
period. It is this respect that humans and callitrichids seem convergent.
Evolved predispositions versus conscious decisions? Or both?
Chimpanzees and other apes are reflexively possessive of their
newborns, remaining in protective, skin-to-skin contact with them for
months after birth until infants themselves begin to take the initiative
to move about. Women's postpartum responses are far more flexible,
more contingent on external cues and varied than in other apes. Almost
everywhere new human mothers tolerate the proximity of familiar (and
one assumes, trusted) conspecifics and voluntarily allow them to hold
their newborns, something no other ape will do. Odder still, under a
Fig. 5. A goldenlion tamarin (Leontopithecus rosalia) male passes twin infants back to their mother so they can nurse. Previousmates of the mother, as well as her older offspring, help to
care for infants and also capture preyto feed them around thetime of weaning. The more male helpers infants have, the better are theirsurvival prospects(drawing by S. Landry,a gift to
the author).
279S.B. Hrdy / Hormones and Behavior 77 (2016) 272–283
range of conditions many mothers through history and prehistory have
drastically reduced levels of care for their own offspring (reviewed in
Hrdy, 2009: Chapter 3), a level of apparent disinterest sometimes
dismissed as pathological or as evidence disproving the existence
of any biological basis for maternal “instincts”(Badinter, 1981;
Sheper-Hughes, 1992). It was the last quarter of the 20th century before
it was recognized that a mother's lifetime reproductive success can take
priority over the well-being of particular offspring so that some of this
maternal retrenchment can be considered as adaptive (Hausfater and
Hrdy, 1984; Parmigiani and Vom Saal, 1994).
As mammalian mothers go, women exhibit a dearth of “fixed action
patterns”post-partum. Although visual and tactile inspections of their
newborns are routine, other behaviors are less predictable. Rarely do
new mothers lick their babies and (New Agers aside) women never
consume placentas as do all but a handful (camellids, many marine
mammals) of other mammals. There exists far more intra-specificvari-
ation in the breeding systems of nonhuman primates than previously
assumed, yet even this variation pales by comparison with the extraor-
dinarily variable and flexible parenting behaviors observed within and
between human societies. Furthermore, humans are virtually the only
apes where experienced mothers are known to voluntarily abandon or
harm their own offspring under natural conditions,
Without doubt, the large human neocortex and extensive capacities
for culture play important roles. Why lick your baby when you can wipe
it clean, bathe it in water or with oil? As discussed, sapient capacities
come into play when mothers discriminate between infants based on
specific physical attributes or cultural ideals. Given that Homo sapiens
parents can consciously calculate future prospects for a given infant,
ascribe more or less value to that infant, and respond accordingly
(Daly and Wilson, 1980, 1984; Scrimshaw, 1984), it is understandable
that some social scientists insist that we first rule out the “consequences
of ordinary practical reasoning”(Driscoll, 2005) or cultural constructs
(Badinter, 1981; Sheper-Hughes, 1992), as well as social pathology
(reviewed in Rees, 2009), before invoking neurobiological adaptations.
But as committed as most primate mothers –especially those with
prior experience –are, human mothers are not the only primates
whose variable responsiveness in the first hours or days after birth
includes rejection of infants and in extreme cases, even infanticide.
Parallels between humans and other cooperative breeders, including
tamarins or marmosets with a mere ten grams of gray matter and no
capacities for perspective-taking (Burkart and Heschl, 2007), make
clear that higher cortical processes are not essential for mothers to
adjust commitment in line with available care.
Biology clearly has considerable influence on maternal and, in
biparental species, paternal behaviors as well. Yet by themselves,
hormones rarely determine parental responsiveness (Bales and
Saltzman, 2016-in this issue; González-Mariscal et al., 2016-in this
issue;Lonstein et al., in press; Lynn, 2016-in this issue; Numan and
Insel, 2016-in this issue; Storey and Ziegler, 2015-in this issue;
Olazábal & Alsina-Llanes, 2016-in this issue). Parity, past experience,
sensitization and learning, along with local conditions, epigenetic
and inter-generational effects sometimes going back several genera-
tions, modulate their impacts (reviewed in Barrett and Fleming,
2011;alsoseeBeery et al., 2016-in this issue; Bridges, 2015-in this
issue; Lonstein et al., in press; Lomanowska and Melo, 2016-in this
issue; Mileva-Seitz et al., 2016-in this issue; Stoltzenberg and Cham-
pagne, 2016-in this issue). When we consider large-brained H. sapi-
ens with all our “later-evolving associative, and mentalizing brain
networks,”as described by Ruth Feldman (2016-in this issue), Kim
et al. (2016-in this issue),andPawluski et al. (2016-in this issue),
the underlying potentials so essential to our extraordinarily flexible
family systems, capacities for coordinated endeavors and culture-
generated adaptability to a range of habitats, things become more
complicated still. Yet I am convinced that even the most rational cal-
culations by parents are colored and complicated by humankind's
deep history of cooperative breeding.
Counteracting the overrides even before we understand them
Patterns revealed by comparisons across species are useful for
generating hypotheses and predictions. But the comparative method
is rarely sufficient to identify, much less explain, underlying mecha-
nisms. It is my hope that the innovative experimental approaches
reviewed in this special issue that have yielded so many insights into
the nature of maternal responses that enhance the survival of imma-
tures can also help us learn how maternal responses come to be so
much more conditional among cooperative breeders. Until then though,
do evolutionary and comparative perspectives have anything useful
to offer?
Although only sporadically practiced among post-industrial people,
breast-feeding and co-sleeping are primate universals. Around the
world, women in traditional societies still breast-feed and sleep with
their babies. As amply shown by articles in this special issue, such inti-
mate contact with infants has neurophysiological effects correlated
with maternal responsiveness toward infants (e.g., Meliva-Seitz et al.,
2016-in this issue; Jonas and Woodside, 2016-in this issue and other ar-
ticles in this issue) and is inversely correlated with neglect or abuse
(e.g., Strathearn et al., 2009). Anecdotal evidence strongly suggests
that intimate contact with nursing infants postpartum can override a
mother's reason-based assessment of future prospects, including her
premeditated decision to abandon her infant (Hrdy, 1999:315ff,
454ff). Even absent parturition or breast-feeding, intimate contact
with infants has transformative effects on the neurophysiology of both
male and female allomothers (Glocker et al., 2009; Kringelbach et al.,
2008; Lonstein et al., in press; Stolzenberg and Champagne, 2016-in
this issue, and especially Abraham et al., 2014; also summarized by
Storey and Ziegler, 2015-in this issue).
But holding her baby close and the establishment of breastfeeding
are not foregone post-partum events. For example, human mothers
may experience delays, or even dampening in postpartum responsive-
ness. As in other cooperatively breeding primates, their responses
appear shaped by both social context and available support as well as
by particular attributes of their infant, something not yet reported for
any other primate. In no other primate are mothers known to discrimi-
nate on the basis of specific infant attributes (robustness, sex, birth
weight, culturally arbitrary traits such as too much or too little hair
or other perceived defects). No doubt, culture and rational assessments
concerning a child's future prospects are involved. But another possibil-
ity is that the dampening of maternal responsiveness to infant
cues postpartum seen in cooperative breeders provided novel opportu-
nities for selection to operate in this realm, but as to how and through
which mechanisms, I am not qualified to even guess. I can however pro-
vide neuroscientists with several (hopefully testable) predictions.
Situation-dependent neural overrides to maternal responsiveness
should be situated in more ancient portions of the brain than discrimi-
native solicitude based on specific infant attributes, and these discrimi-
nations will not be entirely conscious.
The neurophysiological underpinnings for flexible parental commit-
ment are beginning to be explored in humans but remain completely
unstudied in other apes. More research is needed but finding ethical
and humane ways of doing so will be a challenge. Based on recent dis-
coveries about the neurophysiological bases of parental responsiveness
(e.g., Abraham et al., 2014; Bell et al., 2014, 2015; Cong et al., 2014;
Dulac et al., 2014; Kim et al., 2016-in this issue; Numan and Young,
2016-in this issue; Pereira and Ferreira, 2016-in this issue; Wu et al.,
2014; Tsuneoka et al., 2015), Rosenblatt's successors inthe field of social
neuroscience are well positioned to learn why post-partum responses
in human mothers, even experienced ones, are so much more contin-
gent than in most other primates. In the meantime comparative and
evolutionary perspectives and hypotheses about the evolutionary func-
tions of maternal distancing can at least help us understand why some
interventions are proving more effective than others and thus worth
pursuing.
280 S.B. Hrdy / Hormones and Behavior 77 (2016) 272–283
In particular, the proposal that a deep hominin legacy of cooperative
breeding produced new mothers peculiarly sensitive to their percep-
tions of available assistance can explain why social support sometimes
proves a better predictor of postpartum commitment than economic
circumstances (e.g., Bonnet, 1993:509;Hrdy, 1999: 371ff). It also
helps to explain why aversive emotions toward infants postpartum
tend to co-occur with feelings of “social isolation”(Bonnet, 1993:
504), why the presence of “doulas”during birth can matter so much
(Meyer et al., 2001), why the responsiveness of an “at-risk”young
mother is enhanced by her grandmother's presence in the same house
(Spieker and Bensley, 1994), or why even such trivial seeming interven-
tions as brief home visits to pre-and post-partum mothers by a support-
ive social worker prove so beneficial (Eckenrode et al., 2000; Olds et al.,
1997).
Acknowledgments
Brief portions of this article were excerpted from an in press chapter
entitled “Of marmosets, men, and the transformative power of babies,”
in Costly and Cute:How Helpless Newborns Made Us Human, edited by
W. Trevathen and K. Rosenberg. As usual, heartfelt thanks to Sue Carter
for mentoring an anthropologist voyaging in the unfamiliar realms of
social neuroscience, to Alison Fleming for asking me to reflect on the ex-
traordinary wealth of new findings expertly reviewed in this special
issue, to callitrichidologists Karen Bales, Judith Burkart, Leslie Digby,
and Lisa Rapaport for criticisms of the earlier book chapter and to
Toni Ziegler for valuable insights.
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