Allomothering, allomaternal infant care/handling, or non-maternal infant care/handling is performed by any group member other than the mother. Alloparental care is provided by group members other than the genetic father or the mother and thus is distinguished from parental care. Both are widespread phenomena among social insects, birds and mammals.
Allomothering comprises a wide variety of behaviors including: carrying, provisioning, grooming, touching, nursing (allonursing), and protecting infants from predators or conspecifics. Depending on age-sex composition of groups, alloparents, helpers or "handlers" can be non-reproductive males in polyandrous systems, reproductive or non-reproductive adult females, young or older juveniles, or older brothers or sisters helping to raise their younger siblings.
Non-human primates
The term allomother first appeared in a sociobiological analysis of reproductive strategies among langur monkeys and referred to group members other than the mother who share care of infants.Sarah Blaffer Hrdy, 1975 Male and female strategies of reproduction among the langurs of Abu. Ph.D thesis. Harvard University Allomothering turns out to be common across the primate order and occurs in vervets, cebus monkeys, squirrel monkeys, various macaques, New World monkeys and prosimians as female or male group members assist the mother by carrying or guarding infants from predators, and in some New World monkeys such as tamarins and marmosets, helping to provision them.
Allomaternal care varies greatly across and within different species, families, subfamilies, and groups of primates. Mothers within the same group often vary significantly in the amount of access they allow allomothers. Differing levels of allomaternal care are present in almost 75% of primate species for which there is data and among 100% of callitrichids. Tecot, S. and Baden, A.L. (2015). Primate Allomaternal Care. In Emerging Trends in the Social and Behavioral Sciences (eds R.A. Scott and S.M. Kosslyn). Allomaternal care by adult males is most often provided in species in which there is a relatively high degree of paternity certainty, such as within pair living species. However, unrelated adult males have been observed to provide allomaternal care as in fat-tailed dwarf lemurs and Barbary macaques. Ross, C., & MacLarnon, A. (2000). The evolution of non-maternal care in anthropoid primates: A test of the hypotheses. Folia Primatologica, 71(1), 93-113.
The majority of allomaternal care in group living primate species is provided by females and juveniles. Juveniles are often older siblings, but do not necessarily provide allomaternal care exclusively to their siblings. Allomothering is most common in species with close female relationships and relaxed female dominance hierarchies.
Number of allomothers
The number of allomothers involved in the allomaternal care of a single infant varies by species. In hanuman langurs, infants receive allomaternal care from most of the females within the group, while in capped langurs, one adult female typically acts as the primary allomother for an infant. •Stanford, C. (1992). Costs and Benefits of Allomothering in Wild Capped Langurs (Presbytis pileata). Behavioral Ecology and Sociobiology, 30(1), 29-34.
Infant's age
The age at which infants receive care from allomothers also varies greatly by species. Research on wedge-capped capuchins has found that infants receive no allomaternal care during the first three months of their lives, and they receive the greatest amounts of allomaternal care between the ages of four and six months. However, potential allomothers show interest and investigate infants who are under three months old. Alternatively, research on wild capped langurs found that infants spent about one-third of their time with a single allomother during their first month of life, and after this point, time engaged in allomaternal care declined. Wild Formosan macaque infants receive the highest rates of allomaternal handling between the ages of four and seven weeks, and allomaternal care rates decrease greatly between 20 and 24 weeks of age. Hsu, M. J., Lin, S. I., Lin, J. F., Lin, T. J., & Agoramoorthy, G. (2015). Non-Maternal Infant Handling in Wild Formosan Macaques of Mount Longevity, Taiwan. Folia primatologica; international journal of primatology, 86(6), 491–505.
Infant's sex
There is evidence that some primate species differentially provide allomaternal care based on the infant's sex. This sex-bias in allomaternal care is noted in wild Formosan macaques. In a study of this species, adult females participated in higher rates of allomaternal care with female infants than with male infants, while juvenile females engaged in higher rates of allomaternal care with male infants than with female infants.
Allonursing
Capuchin monkey females have been known to regularly nurse (allonurse) infants who are not their own (cf. wet nurse). In these species allonursing is performed by related and unrelated females. Moreover, about 10% of nursing bouts are attributed to allonursing. Allonursing is a widespread, though infrequent, behavior among female wedge-capped capuchins. Allomothering can also be performed by non-reproductive helpers like in the callitrichids (marmosets and tamarins).
Cooperative breeding
In the callitrichids, allomothering care goes beyond that of many other species and infants are spontaneously provisioned by all group members without a prior begging call on the part of the infants. These species practice facultative cooperative breeding, where a single dominant female reproduces and other group members (fathers, other males and non-reproductive juveniles) provide the majority of care to the infants.
Cognitive and socialization implications Many studies have shown that cooperative breeding and allomothering provide significant benefits for the development, learning, and socialization of offspring. Primates that are cooperative breeders exhibit behavioral elements including territory and group defense, caution, and transference of offspring between different individuals. The cooperative group protects offspring and members physically and provides or shares food through transferring offspring between different individuals. Researchers believe that there are cognitive abilities underpinning these cooperative behaviors that enable individuals to help others. These behavioral elements also lead to the enhancement of other cognitive abilities, especially those that are related to social interactions.
Some studies have suggested that evolutionary pressures may have formed the behavioral elements and even some morphological traits of infants in cooperative breeding species. One possible pressures is the need for infants to develop social skills that enable them to form strong bonds with multiple caregivers, as this can increase their chances to manipulate caregivers to help them survive. Distinctive vocalizations (or other communicative cues) in offspring can also help infants communicate with their caregivers, and may have developed from the need to do so.
Cooperative breeding may have led to the evolution of greater cognitive flexibility and problem-solving abilities in infants. In this hypothesis, navigating complex social situations with multiple caregivers requires a high level of cognitive ability from the infant, including skills like understanding and responding to social cues, communicating effectively, and solving problems. These skills may be useful in other social situations rather than just in infant/alloparent relationships, and current studies addressing this relationship emphasize the need for further research. For example, in current comparative research on different species of primates, it is shown that cooperative-breeder species like callitrichids, due to their greater social tolerance and sensitivity to others' signals, may perform better on tasks requiring social learning, communication, and alliance-making than their independently reproducing sister taxa (for example, squirrel monkeys).
Another important cognitive ability related to sociality and cooperative breeding is prosociality. Comparative studies argue that cooperative breeding in nonhuman primates leads to cognitive changes that increase prosociality and enhance social cognition. These prosocial behaviors are not seen in nonhuman primates that are independent breeders.
Research on prosociality discusses “shared intentionality” as an individual's capacity to share mental representations of goals and intentions with others based on the understanding of basic mental states. Consequently, this capability allows individuals to cooperate with each other and coordinate their actions. Particularly in humans, the characteristics related to shared childcare are thought to contribute to advanced cognitive skills including language, planning, cumulative culture, and intentional teaching. These characteristics are rare in other animals, and require complicated interaction between cognitive development and social behavior.
Proposed explanations
Multiple explanations have been proposed for the adaptive value of allomaternal care and who benefits from it: the mother, the infant, or the allomother.
Kin selection hypothesis
Older siblings promote their own genetic fitness via helping their younger siblings, which is explained by the inclusive fitness theory. Offspring of the same parents are, on average, genetically as equally close to their siblings as they would be to their own offspring. Under kin selection theory, related allomothers may improve their inclusive fitness if the allomothering behaviour contributes to the infant's survival or a faster reproductive rate for the mother, since this will increase the related allomother's genetic success. In captive vervet monkeys research found that juveniles were most likely to provide allocare to an infant sibling or the infant of a high ranking mother. In wedge-capped capuchins, the degree of relatedness best predicts allomaternal interactions. Female siblings are the most likely to act as allomothers to infants. However, kin selection does not account for all allomaternal behavior since non-kin subadults and females often provide allocare. Young females with siblings may simply have more opportunities to care for related infants.
Learning to mother hypothesis
Jane Lancaster noted that there are reproductive benefits for primates as k-strategists in learning to be better mothers, or acquiring mothering skills. Her learning-to-mother hypothesis postulates that primate females with no children of their own participate in allomothering more frequently than expected, and evidence from studies by Sarah Hrdy and Lynn Fairbanks supports this hypothesis. However, experienced and pregnant mothers may also benefit from mothering practice.
The hypothesis is supported by evidence of the success of allomothering as a learning technique. First time mothers have high rates of infant mortality, but the rate is reduced for females who engaged in allomaternal behavior as juveniles prior to the birth of their first offspring. Therefore more experience in alloparenting as a juvenile corresponds with greater reproductive success for the female. Allomothers may face energetic, social, and reproductive costs, but potentially benefit by learning how to parent and practicing parenting skills which results in higher survival rates for their first born offspring. The benefit to the allomother may, however, be potentially costly to the infant and its mother. This hypothesis is disputed by evidence such as the observation that in wild Formosan rock macaques both nulliparous and multiparous adult females engage in similar rates of allomaternal care.
Alliance formation hypothesis