Religious Involvement Is Associated With Higher Fertility and Lower Maternal Investment, but More Alloparental Support Among Gambian Mothers.

OBJECTIVES: Human childrearing is cooperative, with women often able to achieve relatively high fertility through help from many individuals. Previous work has documented tremendous socioecological variation in who supports women in childrearing, but less is known about the intracultural correlates of variation in allomaternal support. In the highly religious, high-fertility setting of The Gambia, we studied whether religious mothers have more children and receive more support with their children. METHODS: We randomly sampled 395 mothers and 745 focal children enrolled in the Kiang West (The Gambia) Longitudinal Population Study cohort. Structured interviews asked mothers who and how often people invest in their children, and about their religious practices. Data were collected at participants' homes on electronic tablet-based long-form surveys and analyzed using the Bayesian hierarchical models. RESULTS: Religiosity was weakly associated with women's higher age-adjusted fertility. Maternal religiosity was negatively related to maternal investment in focal children, but positively associated with total allomaternal support. Specifically, a woman's religiosity was positively associated with allomaternal support from matrilineal kin, other offspring, and affinal kin, but unrelated to paternal, patrilineal, and non-kin investment. CONCLUSIONS: These results suggest that higher fertility among religious mothers may be supported by high levels of investment from biological and affinal kin. Matrilineal kin, other siblings, and affinal kin seem to be the most responsive to a woman's religiosity. Our findings cast doubt on interpretations of women's religious behaviors as signals of fidelity, and instead suggest they may be part of strategies to enable collective allomaternal resources and higher relative fertility.

Sex and Age Differences in Ontogeny of Alloparenting: A Relation to Forebrain DRD1, DRD2, and HTR2A mRNA Expression?

Alloparenting refers to the practice of caring for the young by individuals other than their biological parents. The relationship between the dynamic changes in psychological functions underlying alloparenting and the development of specific neuroreceptors remains unclear. Using a classic 10-day pup sensitization procedure, together with a pup preference and pup retrieval test on the EPM (elevated plus maze), we showed that both male and female adolescent rats (24 days old) had significantly shorter latency than adult rats (65 days old) to be alloparental, and their motivation levels for pups and objects were also significantly higher. In contrast, adult rats retrieved more pups than adolescent rats even though they appeared to be more anxious on the EPM. Analysis of mRNA expression using real-time-PCR revealed a higher dopamine D2 receptor (DRD2) receptor expression in adult hippocampus, amygdala, and ventral striatum, along with higher dopamine D1 receptor (DRD1) receptor expression in ventral striatum compared to adolescent rats. Adult rats also showed significantly higher levels of 5-hydroxytryptamine receptor 2A (HTR2A) receptor expression in the medial prefrontal cortex, amygdala, ventral striatum, and hypothalamus. These results suggest that the faster onset of alloparenting in adolescent rats compared to adult rats, along with the psychological functions involved, may be mediated by varying levels of dopamine DRD1, DRD2, and HTR2A in different forebrain regions.

Inhibition of alloparental behavior by acute stress in virgin male California mice (Peromyscus californicus).

In many biparental mammals, such as California mice (Peromyscus californicus), fathers display affiliative behavior toward unfamiliar infants whereas reproductively naïve adult males show highly variable responses. Sources of this variability are not well understood, but evidence suggests that stress can either enhance or inhibit alloparental care. We evaluated immediate and delayed effects of acute stress on pup-directed behavior in adult virgin male California mice. Mice underwent three 10-minute tests with unfamiliar pups at 48-hour intervals. Stressed mice (N=22) received a subcutaneous oil injection immediately before tests 1 and 2, whereas controls (N=22) were left undisturbed. In controls, but not stressed mice, latency to approach the pup decreased and duration of alloparental behavior increased across the three tests. At each time point, stressed males were less likely than controls to perform alloparental behavior. Controls spent significantly more time performing alloparental behavior than stressed mice in tests 1 and 2 but not in test 3. Pup-directed aggression did not differ between the groups at any time point. These findings suggest that acute stress can both inhibit alloparental behavior in the short term and prevent the increase in alloparental behavior that typically occurs with repeated exposure to pups in virgin male California mice.

Alloparental Support and Infant Psychomotor Developmental Delay.

Receiving social support from community and extended family has been typical for mothers with infants in human societies past and present. In non-industrialised contexts, infants of mothers with extended family support often have better health and higher survival through the vulnerable infant period, and hence shared infant care has a clear fitness benefit. However, there is scant evidence that these benefits continue in industrialised contexts. Better infant health and development with allocare support would indicate continued evolutionary selection for allocare. The research reported here used multiple logistic regression analysis to test whether a lack of family and other social support for mothers was associated with an increased risk of developmental delay in 9-month-old infants in the UK Millennium Cohort (analysis sample size, 15,696 infants). Extended family-based childcare during work hours and more maternal time spent with friends were the most influential kin and social support variables: infants of mothers with kin-based childcare versus all other childcare arrangements had a lower risk of developmental delay (OR = 0.61, 95% CIs: 0.46-0.82). Infants of mothers who spent no time with friends when compared with those who saw friends every day had double the odds of delay. Greater paternal involvement in infant care was associated with a lower odds of developmental delay. In conclusion, shared care of infants and social support for mothers may influence fitness-related traits in industrialised societies rather than being factors that influenced selection only in the past and in societies which retain close kin networks and a strong local community focus.

Adoption, Fostering, and Parental Absence in Vanuatu.

Alloparenting, wherein people provide care to children who are not their biological offspring, is a key aspect of human child-rearing. In the Pacific, many children are adopted or fostered by custodial alloparents even when both biological parents are still alive. From a behavioral ecology perspective, such behaviors are puzzling: why parent someone else's child at your expense? Furthermore, little is known about how these arrangements are made in Pacific Islander societies today, who provides care, and what kinds of outcomes fostered children experience. A better understanding of these proximate factors may help reveal the ultimate drivers behind custodial alloparenting. Here, we report findings from a survey carried out with the caregivers of 282 children in rural areas of Vanuatu, an island nation in Melanesia. Most fostered and adopted children lived with relatives such as aunts, uncles, and grandparents (87.5%) rather than unrelated caregivers, with a strong preference for maternal kin. The most common reasons for these arrangements were that the parents had separated (16.7%), were engaging in labor migration (27.1%), or a combination of both (27.1%). Results for investment in children's education and their educational outcomes were mixed, although children removed from crisis situations did more poorly than children removed for aspirational reasons. Our findings suggest that custodial alloparenting helps families adapt to socioeconomic transitions and changing marriage practices. Outcomes may depend on a range of factors, such as the reason children were transferred out of the natal home to begin with.

Alloparenting by Helpers in Striped Hyena (Hyaena hyaena).

In an ongoing study of the striped hyena (Hyaena hyaena), we observed that in the nine different females, alloparenting by the daughters of a previous litter was not uncommon and occurred on fifteen different occasions, twice with two helpers. Alloparenting persisted from when the cubs are approximately a month old until they reach the age when they go out foraging with their mothers at 10-12 months. Helpers perform most maternal duties, except suckling, even in the mother's presence. Helpers accrued indirect fitness and practiced parenting before reaching sexual maturity. Future studies must study the reproductive biology of the striped hyena in the wild throughout its geographic range to elucidate additional breeding properties that have not yet been identified. The continued persecution of striped hyenas and the lack of information about their breeding rituals and capabilities in the wild mean that this study of their different reproduction strategies, focusing on surrogate mothers, is of great conservation importance. The fact that we have found cooperative breeding in this solitary species suggests that there is much more to uncover of the enigmatic striped hyena in the wild.

Editorial Perspective: What can we learn from hunter-gatherers about children's mental health? An evolutionary perspective.

Humans lived as hunter-gatherers for more than 95% of our evolutionary history, thus studying contemporary hunter-gatherer populations offers insight into the conditions children may be psychologically adapted to. Here, we contrast hunter-gatherer childhoods with those of WEIRD (Western Educated Industrialised Rich Democratic) societies and consider the implications for children's mental health. Hunter-gatherer infants receive continuous physical contact and more sensitive and responsive caregiving than is typical of WEIRD societies, due to the extensive involvement of alloparents (non-parental caregivers) who generally provide 40-50% of their care. Alongside positive attachment outcomes, alloparenting likely reduces the harms of family adversity and risk of abuse/neglect. From late infancy, hunter-gatherers spend their time in mixed-age 'playgroups' where they learn via active play and exploration without adult supervision. This contrasts with WEIRD norms surrounding the need for adult supervision of children, as well as with the passive teacher-led classrooms, which could potentially lead to suboptimal learning outcomes and pose difficulties to children with ADHD. Based on this preliminary comparison, we consider practical solutions to potential harms arising from discordance between what children are adapted to and exposed to. These include infant massage and babywearing; increased sibling and extra-familial involvement in childcare; and educational adjustments.

A Longitudinal Study of Parenting Conditions on Two Adult, North American River Otters' (Lontra Canadensis) Repetitive Behavior.

Captive animal welfare research focuses on husbandry, enrichment, enclosure space, visitor effects, and opportunities for species-typical behavior (e.g., foraging, territoriality, and social interaction). And yet, one of the most biologically relevant opportunities for species-typical behavior, parenting, has received little attention. The goal of this longitudinal investigation was to explore the differential variability of repetitive behavior across three parenting conditions (i.e., No parenting, parenting, and foster parenting) among captive, wild-rescued, North American river otters. This study represents anatural ABAC design, the conditions reflect differential parenting phases: No parenting (A), Parenting biological pups (B), and Alloparenting nonbiological pups (C). The behavior of two adult North American river otters at the Oregon Zoo were observed from April2016 through March2020 during the different parenting contexts. The frequency of repetitive behaviors was lowest during parenting and highest during the non-parenting conditions. Although data for season, weather, and visitor variables were also collected throughout this study; parenting condition was the only consistent moderator of abnormal repetitive behavior observed.

Transcriptomic analysis of paternal behaviors in prairie voles.

BACKGROUND: The importance of fathers' engagement in care and its critical role in the offspring's cognitive and emotional development is now well established. Yet, little is known on the underlying neurobiology due to the lack of appropriate animal models. In the socially monogamous and bi-parental prairie vole (Microtus ochrogaster), while 60-80% of virgin males show spontaneous paternal behaviors (Paternal), others display pup-directed aggression (Attackers). Here we took advantage of this phenotypic dichotomy and used RNA-sequencing in three important brain areas to characterize gene expression associated with paternal behaviors of Paternal males and compare it to experienced Fathers and Mothers. RESULTS: While Paternal males displayed the same range and extent of paternal behaviors as experienced Fathers, we observed structure-specific transcriptomic differences between parental behaviors phenotypes. Using differential expression, gene set expression, as well as co-expression network analyses, we found that phenotypic differences between Paternal males and Attackers were mainly reflected by the lateral septum (LS), and to a lower extent, the nucleus accumbens (NAc), transcriptomes. In the medial preoptic area (MPOA), the profiles of gene expression mainly reflected differences between females and males regardless of their parental behaviors phenotype. Functional enrichment analyses of those gene sets associated with Paternal males or Attackers in the LS and the NAc revealed the involvement of processes related to the mitochondria, RNA translation, protein degradation processes, as well as epigenetic regulation of gene expression. CONCLUSIONS: By leveraging the natural phenotypic differences in parental behaviors in virgin male prairie voles alongside fathers and mothers, we identified a marked structure- and phenotype-specific pattern of gene expression associated with spontaneous paternal behaviors independently from fatherhood and pair-bonding. The LS transcriptome related to the mitochondria, RNA translation, and protein degradation processes was thus highlighted as a primary candidate associated with the spontaneous display of paternal behaviors. Altogether, our observations further characterize the behavioral and transcriptomic signature of parental behaviors in the socially monogamous prairie vole and lay the groundwork to further our understanding of the molecular underpinnings of paternal behavior.

The interaction engine: cuteness selection and the evolution of the interactional base for language.

The deep structural diversity of languages suggests that our language capacities are not based on any single template but rather on an underlying ability and motivation for infants to acquire a culturally transmitted system. The hypothesis is that this ability has an interactional base that has discernable precursors in other primates. In this paper, I explore a specific evolutionary route for the most puzzling aspect of this interactional base in humans, namely the development of an empathetic intentional stance. The route involves a generalization of mother-infant interaction patterns to all adults via a process (cuteness selection) analogous to, but distinct from, RA Fisher's runaway sexual selection. This provides a cornerstone for the carrying capacity for language. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

A milk-sharing economy allows placental mammals to overcome their metabolic limits.

SignificanceHere, we demonstrate that a naturally evolving behavior (allonursing) has greater effect on reproductive power (mass per unit of time) and output (litter mass at birth) than does artificial selection (domestication). Additionally, we demonstrate the importance of resource optimization afforded by sociality (rather than resource abundance per se) in shaping a species' life history profile and its ability to overcome its own physiological constraints.

How a pregnant woman's relationships with her siblings relate to her mental health: a prenatal allocare perspective.

BACKGROUND: In cooperatively breeding species, individuals may promote their inclusive fitness through allomothering. Humans exhibit some features of cooperative breeding, and previous studies have focused on allomothering by grandparents and juvenile siblings in the postnatal period. We hypothesize that a pregnant woman's relationships with her siblings (offspring's maternal aunts and uncles) are beneficial for maternal affect in ways that can enhance the siblings' inclusive fitness. Maternal affect during pregnancy is a salient target of allocare given the detrimental effects of antepartum mood disorders on birth and infant outcomes. METHODOLOGY: We test our hypotheses in a cohort of pregnant Latina women in Southern California (N = 201). Predictor variables of interest include number of siblings a participant has, if she has sisters, frequency of seeing siblings, and frequency of communication with siblings. Outcome variables measuring maternal affect include depression, state anxiety, pregnancy-related anxiety and perceived stress. RESULTS: Having at least one sister and greater frequency of communication with siblings were associated with fewer depressive symptoms during pregnancy. No significant associations were found between sibling variables and other measures of affect. CONCLUSION AND IMPLICATIONS: Results suggest that how frequently you communicate with, and not how often you see, siblings could be protective against risk of antepartum depression. Sibling allomothering could impart effects through social-emotional support rather than instrumental support, as a strategy to benefit the prenatal environment in which future nieces and nephews develop. Allomothering may be particularly important in cultural contexts that value family relationships. Future studies should investigate other communities.

Pet Parenting in the United States: Investigating an Evolutionary Puzzle.

Fertility rates continue to decline globally amidst the second demographic transition, marked by urbanization, increased educational attainment, and most importantly, a new flexibility in life-course organization. As a result, some individuals are choosing to bring companion animals in the home rather than raising children. Purpose The purpose of this study is to explore whether these transitions result in differential companion animal attachment and caregiving behavior in the homes of parents (or those who desire to become parents) and nonparents or childfree "pet parents." Methods A total of 917 respondents completed an online survey via Qualtrics that included demographic questions, the Lexington Attachment to Pets Scale (LAPS), and Likert-scale questions designed to probe direct and indirect caretaking behaviors. Results Nonparents reported more Generalized Attachment and more Affective Responsiveness to their companion animals, as well as increased investment in General Care. They also reported more People Substituting on the LAPS. Parents and nonparents reported similar agreement regarding Animal Rights/Welfare and Training and Play. Conclusion I conclude that nonparents' investment in companion animals much like parents invest in children, but in ways that meet species-specific needs. This supports the notion that nonparents may be nurturing companion animals as a trade-off to raising children, but not as a substitute. This is an evolutionarily novel application of parenting strategies in a new, flexible environment.

A preliminary analysis of wound care and other-regarding behavior in wild chimpanzees at Ngogo, Kibale National Park, Uganda.

Caring for others is a key feature of human behavior. Mothers, fathers, siblings, grandparents, and other group members provide care in the form of provisioning, protection, and first aid. To what extent is other-regarding behavior present in our primate relatives? Here we describe an unusual incident of other-regarding behavior toward an injured juvenile female chimpanzee (Pan troglodytes schweinfurthii) at Ngogo in Kibale National Park, Uganda. After the juvenile received a mild head wound from an adult female, several adolescent and juvenile chimpanzees gathered to touch, lick, and peer at the wound. One adolescent male wiped a leaf across the cut. Another adolescent male later groomed the injured female and briefly carried her. Across a 5-year period, we observed only three other instances of other-directed wound care in chimpanzees, occurring in 4% (4/100) of cases in which we observed individuals with fresh wounds, and 57 other instances of allomaternal carrying. Despite the infrequency of such behaviors, our study adds another chimpanzee field site to the list of those where other-directed wound care has been observed. Observations from wild chimpanzees provide insight into empathy and may inform our understanding of the evolution of other-regarding behavior in humans.

The expression of care: Alloparental care frequency predicts neural control of facial muscles in primates.

The adaptive value of facial expressions has been debated in evolutionary biology ever since Darwin's seminal work. Among mammals, primates, including humans, exhibit the most intricate facial displays. Although previous work has focused on the role of sociality in the evolution of primate facial expressions, this relationship has not been verified in a wide sample of species. Here, we examine the relationship between allomaternal care (paternal or alloparental) and the morphology of three orofacial brainstem nuclei (facial; trigeminal motor; hypoglossal) across primates to test the hypothesis that allomaternal care explains variation in the complexity of facial expressions, proxied by relative facial nucleus size and neuropil fraction. The latter represents the proportion of synaptically dense tissue and may, therefore, correlate with dexterity. We find that alloparental care frequency predicts relative neuropil fraction of the facial nucleus, even after controlling for social system organization, whereas allomaternal care is not associated with the trigeminal motor or hypoglossal nuclei. Overall, this work suggests that alloparenting requires increased facial dexterity to facilitate nonverbal communication between infants and their nonparent caregivers and/or between caregivers. Accordingly, alloparenting and complex facial expressions are likely to have coevolved in primates.

Cooperative care and the evolution of the prelinguistic vocal learning.

The development of the earliest vocalizations of human infants is influenced by social feedback from caregivers. As these vocalizations change, they increasingly elicit such feedback. This pattern of development is in stark contrast to that of our close phylogenetic relatives, Old World monkeys and apes, who produce mature-sounding vocalizations at birth. We put forth a scenario to account for this difference: Humans have a cooperative breeding strategy, which pressures infants to compete for the attention from caregivers. Humans use this strategy because large brained human infants are energetically costly and born altricial. An altricial brain accommodates vocal learning. To test this hypothetical scenario, we present findings from New World marmoset monkeys indicating that, through convergent evolution, this species adopted a largely identical developmental system-one that includes vocal learning and cooperative breeding.

Evidence of cooperative calves' care and providers' characteristics in zebu cattle (Bos indicus) raised under extensive conditions.

Communal rearing has been reported in several mammals, including wild ungulates. However, until now, there was no evidence of any alloparental care in the Bos genus. To test the hypothesis that calves' groups are formed under the care of specific cows, a herd of 31 peri-partum zebu cows raised under pasture conditions were used. Groups of ≥ 3 individuals within a 10-m diameter were estimated using aerial pictures taken every other day at 7:00, 10:30, 13:30, 16:00, and 18:00 h, during 6 weeks. Temperament (exit speed, flight distance, intensity of reaction), age, and parity of each cow were registered. A total of 142 groups were observed, and in all of them, at least one calf was present. A total of 75% of the groups were more calves than cows, and in 65.4% of the cases, there were 1 to 3 cows with 2 to 32 calves. While there were no groups integrated only by cows, there were 3.5% integrated only with calves. The most frequent group was formed by 2 calves and 1 cow (14.8%). Parity was positively related with the number of times that a cow was observed in a group (R2 = 0.19, P = 0.01) and with the number of groups in which her calf was present (R2 = 0.16; P = 0.03). The results of the temperament tests were unrelated to the total number of groups in which a cow was observed nor the number of groups with or without its calf. It was concluded that zebu calves congregate in newborn groups in companion with one or more adults, preferably high parity cows, regardless of their temperament.

Inbreeding depresses altruism in a cooperative society.

In some animal species, individuals regularly breed with relatives, including siblings and parents. Given the high fitness costs of inbreeding, evolutionary biologists have found it challenging to understand the persistence of these inbred societies in nature. One appealing but untested explanation is that early life care may create a benign environment that offsets inbreeding depression, allowing inbred societies to evolve. We test this possibility using 21 years of data from a wild cooperatively breeding mammal, the banded mongoose, a species where almost one in ten young result from close inbreeding. We show that care provided by parents and alloparents mitigates inbreeding depression for early survival. However, as adults, inbred individuals provide less care, reducing the amount of help available to the next generation. Our results suggest that inbred cooperative societies are rare in nature partly because the protective care that enables elevated levels of inbreeding can be reduced by inbreeding depression.

Church attendance and alloparenting: an analysis of fertility, social support and child development among English mothers.

Many aspects of religious rituals suggest they provide adaptive benefits. Studies across societies consistently find that investments in ritual behaviour return high levels of cooperation. Another line of research finds that alloparental support to mothers increases maternal fertility and improves child outcomes. Although plausible, whether religious cooperation extends to alloparenting and/or affects child development remains unclear. Using 10 years of data collected from the Avon Longitudinal Study of Parents and Children (ALSPAC), we test the predictions that church attendance is positively associated with social support and fertility (n = 8207 to n = 8209), and that social support is positively associated with fertility and child development (n = 1766 to n = 6561). Results show that: (i) relative to not attending, church attendance is positively related to a woman's social network support and aid from co-religionists, (ii) aid from co-religionists is associated with increased family size, while (iii) fertility declines with extra-religious social network support. Moreover, while extra-religious social network support decreased over time, co-religionist aid remained constant. These findings suggest that religious and secular networks differ in their longevity and have divergent influences on a woman's fertility. We find some suggestive evidence that support to mothers and aid from co-religionists is positively associated with a child's cognitive ability at later stages of development. Findings provide mixed support for the premise that ritual, such as church attendance, is part of a strategy that returns high levels of support, fertility and improved child outcomes. Identifying the diversity and scope of cooperative breeding strategies across global religions presents an intriguing new horizon in the evolutionary study of religious systems. This article is part of the theme issue 'Ritual renaissance: new insights into the most human of behaviours'.