Prenatal Zika virus infection has sex-specific effects on infant physical development and mother-infant social interactions.

There is enormous variation in the extent to which fetal Zika virus (fZIKV) infection affects the developing brain. Despite the neural consequences of fZIKV infection observed in people and animal models, many open questions about the relationship between infection dynamics and fetal and infant development remain. To further understand how ZIKV affects the developing nervous system and the behavioral consequences of prenatal infection, we adopted a nonhuman primate model of fZIKV infection in which we inoculated pregnant rhesus macaques and their fetuses with ZIKV in the early second trimester of fetal development. We then tracked their health across gestation and characterized infant development across the first month of life. ZIKV-infected pregnant mothers had long periods of viremia and mild changes to their hematological profiles. ZIKV RNA concentrations, an indicator of infection magnitude, were higher in mothers whose fetuses were male, and the magnitude of ZIKV RNA in the mothers' plasma or amniotic fluid predicted infant outcomes. The magnitude of ZIKV RNA was negatively associated with infant growth across the first month of life, affecting males' growth more than females' growth, although for most metrics, both males and females evidenced slower growth rates as compared with control animals whose mothers were not ZIKV inoculated. Compared with control infants, fZIKV infants also spent more time with their mothers during the first month of life, a social behavior difference that may have long-lasting consequences on psychosocial development during childhood.

Meager Milk: Lasting Consequences for Adult Daughters of Primiparous Mothers Among Rhesus Macaques (Macaca mulatta).

Among mammals, primipara who initiate reproduction before full maturity can be constrained in their maternal investment, both due to fewer somatic resources and tradeoffs between their own continued development and reproductive effort. Primipara are particularly limited in their capacity to synthesize milk during lactation, the costliest aspect of reproduction for most mammals, especially primates due to long periods of postnatal development. Due to reduced milk transfer, Firstborns may be at elevated risk for long-term consequences of deficits in early life endowment from their primiparous mothers. Here we investigated mass, growth, stature, and lactation performance among N = 273 adult daughters across N = 335 reproductions, who were their own mother's Firstborn or Laterborn progeny, among rhesus macaques (Macaca mulatta) at the California National Primate Research Center. We further explored mass during infancy of the offspring of Firstborn and Laterborn mothers. Firstborns had accelerated growth during infancy, but had slowed growth during juvenility, compared to Laterborns. Although both Firstborns and Laterborns were the same age at reproductive debut, Firstborns had lower body mass, an effect that persisted throughout the reproductive career. Available milk energy, the product of milk energetic density and milk yield, was on average 16% lower for Firstborns compared to Laterborns, a difference that was only partially mediated by their lower mass. Despite differences in their mothers' energy provision through milk, the mass of infants of Firstborn and Laterborn mothers did not differ at peak lactation, suggesting that infants of Firstborns devote a higher proportion of milk energy to growth than infants of Laterborns. To date few studies have explored how early life conditions shape capacities to synthesize milk and milk composition. Our findings contribute new information among primates on how early life maternal endowments are associated with persistent effects long after the period of maternal dependence well into reproductive maturity.

Monkeys do not show sex differences in toy preferences through their individual choices.

BACKGROUND: As interest in evaluating sex differences in nonhuman animals grows, the finding that male and female monkeys have toy preferences that differ, and that parallel those documented in human children, has garnered significant attention and is leveraged as an argument in favor of a biological contribution for human sex differences. To date, however, only two studies have investigated sex differences in monkeys' toy preferences, both documenting that males prefer toys considered to be "masculine" (such as vehicles) and females prefer toys considered to be "feminine" (such as dolls). Monkeys in these studies were tested in their social groups, making it hard to determine if the sex differences reported reflect actual individual preferences or result from social dynamics present at the time of testing. METHOD: Here, we assessed the preferences of 14 rhesus macaques (N = 7 males; N = 7 females) who were singly tested in a choice test with a variety of toys characterized as masculine (hard non-zoomorphic wheeled toys), feminine (zoomorphic soft toys), neutral (hard non-zoomorphic toys) and ambiguous (zoomorphic or plush vehicles) based on criteria from previous studies. RESULTS: Males and females showed similar preferences for neutral and "masculine" toys and preferred them (i.e., were more likely to interact with them) to "feminine" and sex-ambiguous toys. When they interacted with the toys, both males and females interacted more with neutral than with "masculine" toys. Females, but not males, interacted more with neutral and "masculine" toys than with "feminine" toys. The highest frequency of interaction for any single toy for the male monkeys was with the doll-standing is stark contrast to previous findings. CONCLUSIONS: Our results contrast greatly with the previous study in rhesus monkeys, as well as findings in human children, suggesting that the previously documented sex differences are likely context dependent, and question the existence of a strong biological basis to sex differences in toy preferences.

Maternal social environment affects offspring cognition through behavioural and immune pathways in rats.

The social environment of lactation is a key etiological factor for the occurrence of postpartum disorders affecting women and their children. Postpartum depression and anxiety disorders are highly prevalent in new mothers and negatively affect offspring's cognitive development through mechanisms which are still unclear. Here, using a rat model, we manipulated the maternal social environment during lactation and explored the pathways through which social isolation (vs. the opportunity for limited social interaction with another lactating female, from 1 day before parturition to postpartum day 16) and chronic social conflict (daily exposure to a male intruder from postpartum day 2 to day 16) affect offspring learning and memory, measured at 40 to 60 days of age. We specifically explored the consequences of these social treatments on two main hypothesized mediators likely to affect offspring neurophysiological development: the quality of maternal care and maternal inflammation factors (brain-derived neurotrophic factor, granulocyte-macrophage colony-stimulating factor, intercellular adhesion molecule 1, tissue inhibitor of metalloproteinases 1 and vascular endothelial growth factor) likely to influence offspring development through lactation. Maternal rats which had the opportunity to interact with another lactating female spent more time with their pups which, in turn, displayed improved working and reference memory. Social stress affected maternal plasma levels of cytokines that were associated with cognitive deficits in their offspring. However, females subjected to social stress were protected from these stress-induced immune changes and associated offspring cognitive impairment by increased social affiliation. These results underscore the effects of social interaction for new mothers and their offspring and can be used to inform the development of clinical preventative measures and interventions.

Maternal care affects chicks' development differently according to sex in quail.

Maternal behavior is known to influence the behavioral development of young. Recently, it was demonstrated that maternal behavior also differed according to sex of chicks and brood sex composition. So, here, we explored if these factors influenced behavioral development of quail chicks when they were brooded, and what characteristics of chicks and foster females could best explain this development. We studied three sets of chick pairs brooded by foster females: unisex male, unisex female, and mixed broods. We found that both emotivity profile and sociality depended on the sex: females were more reactive and less social than males. Females' emotivity profile was correlated with brood composition and foster female activity during maternal care. In males, only sociality was correlated with foster females' scores of aggressive rejection. Our results evidence that male and female chicks respond differentially to maternal behavior. This is discussed in terms of ecological and physiological constraints on development according to sex.

Age at reproductive debut: Developmental predictors and consequences for lactation, infant mass, and subsequent reproduction in rhesus macaques (Macaca mulatta).

OBJECTIVES: The age at which females initiate their reproductive career is a critical life-history parameter with potential consequences on their residual reproductive value and lifetime fitness. The age at reproductive debut may be intimately tied to the somatic capacity of the mother to rear her young, but relatively little is known about the influence of age of first birth on milk synthesis within a broader framework of reproductive scheduling, infant outcomes, and other life-history tradeoffs. MATERIAL AND METHODS: Our study investigated the predictors of age at first reproduction among 108 captive rhesus macaque (Macaca mulatta) females, and associations with their milk synthesis at peak lactation, infant mass, and ability to subsequently conceive and reproduce. RESULTS: The majority of females reproduced in their fourth year (typical breeders); far fewer initiated their reproductive career one year earlier or one year later (respectively early and late breeders). Early breeders (3-year-old) benefited from highly favorable early life development (better juvenile growth, high dominance rank) to accelerate reproduction, but were impaired in milk synthesis due to lower somatic resources and their own continued growth. Comparatively, late breeders suffered from poor developmental conditions, only partially compensated by their delayed reproduction, and evinced compromised milk synthesis. Typical breeders not only produced higher available milk energy but also had best reproductive performance during the breeding and birth seasons following primiparity. DISCUSSION: Here, we refine and extend our understanding of how life-history tradeoffs manifest in the magnitude, sources, and consequences of variation in age of reproductive debut. These findings provide insight into primate reproductive flexibility in the context of constraints and opportunities.

Chronic social instability in adult female rats alters social behavior, maternal aggression and offspring development.

We investigated the consequences of chronic social instability (CSI) during adulthood on social and maternal behavior in females and social behavior of their offspring in a rat model. CSI consisted of changing the social partners of adult females every 2-3 days for 28 days, 2 weeks prior to mating. Females exposed to CSI behaved less aggressively and more pro-socially towards unfamiliar female intruders. Maternal care was not affected by CSI in a standard testing environment, but maternal behavior of CSI females was less disrupted by a male intruder. CSI females were quicker to attack prey and did not differ from control females in their saccharin consumption indicating, respectively, no stress-induced sensory-motor or reward system impairments. Offspring of CSI females exhibited slower growth and expressed more anxiety in social encounters. This study demonstrates continued adult vulnerability to social challenges with an impact specific to social situations for mothers and offspring.

Brood size can influence maternal behaviour and chick's development in precocial birds.

Mothers have a crucial influence on offspring development. Variations of maternal behaviour can be due to numerous parameters, for instance costs are related to the size of a brood/litter, which in turn can influence the level of mothers' investment in each offspring. Here we investigated the influence of brood size on the behaviour of Japanese quail mothers and chicks during the mothering period and on offspring development. We compared two types of broods: small broods of three chicks (N=9) and large broods of six chicks (N=9). Behavioural tests assessed chicks' social and emotional traits. Mothers of large broods emitted more maternal vocalisations at the beginning of the mothering period, but at the end they assumed more non-covering postures and trampled chicks more than mothers of small broods. Chicks in large broods huddled up more whereas chicks in small broods rested alone more frequently. Moreover, the social motivation of chicks in large broods was higher than that of chicks in small broods, although their emotional reactivity levels were similar. Our results evidence the importance of brood size for maintaining family cohesion and the influence of brood size on chicks' interactions with their siblings. We evaluated the influence of mothers and siblings on chicks' behavioural development.

Effects of Chronic Social Stress and Maternal Intranasal Oxytocin and Vasopressin on Offspring Interferon-γ and Behavior.

Recent studies support the hypothesis that the adverse effects of early-life adversity and transgenerational stress on neural plasticity and behavior are mediated by inflammation. The objective of the present study was to investigate the immune and behavioral programing effects of intranasal (IN) vasopressin (AVP) and oxytocin (OXT) treatment of chronic social stress (CSS)-exposed F1 dams on F2 juvenile female offspring. It was hypothesized that maternal AVP and OXT treatment would have preventative effects on social stress-induced deficits in offspring anxiety and social behavior and that these effects would be associated with changes in interferon-γ (IFNγ). Control and CSS-exposed F1 dams were administered IN saline, AVP, or OXT during lactation and the F2 juvenile female offspring were assessed for basal plasma IFNγ and perseverative, anxiety, and social behavior. CSS F2 female juvenile offspring had elevated IFNγ levels and exhibited increased repetitive/perseverative and anxiety behaviors and deficits in social behavior. These effects were modulated by AVP and OXT in a context- and behavior-dependent manner, with OXT exhibiting preventative effects on repetitive and anxiety behaviors and AVP possessing preventative effects on social behavior deficits and anxiety. Basal IFNγ levels were elevated in the F2 offspring of OXT-treated F1 dams, but IFNγ was not correlated with the behavioral effects. These results support the hypothesis that maternal AVP and OXT treatment have context- and behavior-specific effects on peripheral IFNγ levels and perseverative, anxiety, and social behaviors in the female offspring of early-life social stress-exposed dams. Both maternal AVP and OXT are effective at preventing social stress-induced increases in self-directed measures of anxiety, and AVP is particularly effective at preventing impairments in overall social contact. OXT is specifically effective at preventing repetitive/perseverative behaviors, yet is ineffective at preventing deficits in overall social behavior.

Contributions of family social structure to the development of ultrasociality in humans.

The evolution of ultrasociality in humans may have involved the evolutionarily significant mechanisms that govern family social structure in many animal species. Adverse effects of ultrasociality in humans may be mediated by maladaptive effects of modern civilization on family groups, as many of the effects on both families and societies are especially severe in dense populations made possible by agriculture.

Brain Reward Pathway Dysfunction in Maternal Depression and Addiction: A Present and Future Transgenerational Risk.

Two research areas that could benefit from a greater focus on the role of the reward pathway are maternal depression and maternal addiction. Both depression and addiction in mothers are mediated by deficiencies in the reward pathway and represent substantial risks to the health of offspring and future generations. This targeted review discusses maternal reward deficits in depressed and addicted mothers, neural, genetic, and epigenetic mechanisms, and the transgenerational transmission of these deficits from mother to offspring. Postpartum depression and drug use disorders may entail alterations in the reward pathway, particularly in striatal and prefrontal areas, which may affect maternal attachment to offspring and heighten the risk of transgenerational effects on the oxytocin and dopamine systems. Alterations may involve neural circuitry changes, genetic factors that impact monoaminergic neurotransmission, as well as growth factors such as BDNF and stress-associated signaling in the brain. Improved maternal reward-based preventative measures and treatments may be specifically effective for mothers and their offspring suffering from depression and/or addiction.

Long-life partners or sex friends? Impact of parental pair bond on offspring personality.

Previous investigations reported that some traits of parental relationships, including pair-bond duration or mate behavioural compatibility, influence subsequent offspring fitness by acting on their behaviour and growth and thus their early survival. We hypothesized that the development of a pair bond between sexual partners would have a prenatal influence. This study investigated the impact of two pairing managements on the egg characteristics and development of offspring of Japanese quail (Coturnix c. japonica). Thirty males and 30 females were paired either continuously (C; mates together all the time) or non-continuously (NC; pairs met only three times a week for 5 min). Separation-reunion tests evaluated parental pair bond. Egg yolk testosterone and androstenedione levels were evaluated, and the somatic and behavioural development of C and NC chicks was assessed. Our results revealed that members of C pairs were attached to their mates and, although no significant differences in androgen levels could be evidenced between egg sets, a higher proportion of C pairs' eggs were fertilized and their chicks appeared less emotive and more social. Our results revealed that the parental relationship can modulate the behavioural development of their offspring, probably via non-genetic effects, and this could play a major role in the emergence of inter-individual variability.

Fearfulness affects quail maternal care and subsequent offspring development.

Our study investigated relationships between a precocial bird's fearfulness and maternal care, and the implication of maternal care as a vector for non-genomic transmission of fearfulness to chicks. We compared care given to chicks between two sets of female Japanese quail selected to present either high (LTI) or low fearfulness (STI). Chicks, from a broiler line, were adopted by these females following a sensitization procedure. Chicks' fearfulness after separation from their mother was assessed by well-established procedures. LTIs took longer to present maternal responses, pecked chicks more during the first days post-hatch, presented impaired maternal vocal behaviour and were globally less active than STI females. Chicks mothered by LTIs presented more fearful reactions than did chicks mothered by STIs, supporting the hypothesis of a non-genetic maternal transmission of fearfulness. We suggest that the longer latencies required by LTIs to become maternal are a consequence of their greater fear of chicks, and that their lower general and vocal activity could be components of a heightened antipredatory strategy. We discuss the transmission of maternal fearfulness to fostered chicks, taking into account the possible implication of several well-known mechanisms underlying maternal effects.

Precocial bird mothers shape sex differences in the behavior of their chicks.

Compared to mammals and altricial birds, evaluations of differences related to precocial birds' sex have often been limited to sexual behavior. Nevertheless, the extensive use of precocial bird models for investigating behavioral development issues requires in depth knowledge concerning the emergence of sex differences. Here, we evaluated behavioral differences between Japanese quail chicks in relation to their sex. We know that maternal influences are strong and early social environment shapes behavioral development in this species. Therefore, we investigated the emergence of sex differences in two very different early social situations to evaluate the impact of precocial bird mothers on sex differences. We assessed behavioral differences related to sex of (1) non-brooded chicks and of (2) brooded chicks, using various ethological tests to evaluate emotional reactivity and social motivation differences related to sex. Our results show that both non-brooded and brooded chicks present behavioral differences related to sex. They differed greatly according to chicks' early experience. Sex-related differences between maternally deprived (non-brooded) chicks concerned mainly fearfulness, whereas differences between male and female brooded chicks concerned mainly their reactions to social isolation. We hypothesize that mothers attenuate sex differences related to fearfulness by being a model for responses to fear-eliciting situations and by providing a similar secure basis to both males and females. We finally propose that mothers induce differences in chicks' sociality by providing asymmetrical care toward males and females.

Motherless quail mothers display impaired maternal behavior and produce more fearful and less socially motivated offspring.

Early maternal deprivation impairs the behavioral development of young individuals. Recently, strong differences between mothered and maternally deprived chicks have been reported concerning their emotionality, sociality, and spatial skills. Here we investigated long-term and cross-generational impacts of maternal deprivation by comparing the characteristics of the non-reproductive and the maternal behavior of 22 mothered and 22 non-mothered adult female Japanese quail (Coturnix c. japonica) and by comparing the behavior of their respective fostered chicks. We reveal that non-brooded mothers were more fearful and less competent in spatial tasks and expressed impaired maternal care, characterized by more aggression towards chicks, higher activity rates, and more abnormal pacing during the first days of the care period. Chicks' behavior was clearly affected by maternal care inducing strong differences in their fearfulness and social motivation. Our results show both long-term and cross-generational impacts of early maternal deprivation in precocial birds.

Age affects the expression of maternal care and subsequent behavioural development of offspring in a precocial bird.

Variations of breeding success with age have been studied largely in iteroparous species and particularly in birds: survival of offspring increases with parental age until senescence. Nevertheless, these results are from observations of free-living individuals and therefore, it remains impossible to determine whether these variations result from parental investment or efficiency or both, and whether these variations occur during the prenatal or the postnatal stage or during both. Our study aimed first, to determine whether age had an impact on the expression of maternal breeding care by comparing inexperienced female birds of two different ages, and second, to define how these potential differences impact chicks' growth and behavioural development. We made 22 2-month-old and 22 8-month-old female Japanese quail foster 1-day-old chicks. We observed their maternal behaviour until the chicks were 11 days old and then tested these chicks after separation from their mothers. Several behavioural tests estimated their fearfulness and their sociality. We observed first that a longer induction was required for young females to express maternal behaviour. Subsequently as many young females as elder females expressed maternal behaviour, but young females warmed chicks less, expressed less covering postures and rejected their chicks more. Chicks brooded by elder females presented higher growth rates and more fearfulness and sociality. Our results reveal that maternal investment increased with age independently of maternal experience, suggesting modification of hormone levels implied in maternal behaviour. Isolated effects of maternal experience should now be assessed in females of the same age. In addition, our results show, for first time in birds, that variations in maternal care directly induce important differences in the behavioural development of chicks. Finally, our results confirm that Japanese quail remains a great laboratory model of avian maternal behaviour and that the way we sample maternal behaviour is highly productive.