Jeffrey E. Fite

Interactions among Paternal Behavior, Steroid Hormones, and Parental Experience in Male Marmosets (Callithrix kuhlii)

Male black tufted-ear marmosets (Callithrix kuhlii) contribute to the rearing of their offspring. Here we evaluated predictions of hypotheses suggesting that (1) T and E2 influence infant-care behavior in male marmosets, (2) levels of T and E2 are modulated by paternal experience, and (3) paternal behavior and levels of T and E2 in male marmosets covary with stress. We observed the behavior of marmosets in their family groups following the birth of infants and evaluated urinary concentrations of T, E2, and the stress hormone cortisol (CORT) among fathers before and after the birth of young. Urinary levels of T, E2, and CORT were lower among males who carried infants at high rates than males who carried at low rates, and T and CORT levels were negatively correlated with carrying rates across all males. Males had significantly lower T levels while carrying the second compared to the first litter and slightly lower rates of infant-carrying, possibly due to assistance provided by offspring of the first litter. There were increases in CORT levels of fathers after the birth of the first litter, but decreases in CORT after the birth of the second. Our results suggest a relationship in C. kuhlii between paternal behavior, hormones, and paternal experience. Rates of infant-carrying appear to be linked to hormone levels, and hormone levels in turn are affected by experience caring for young. Our data also suggest that T, E2, and CORT have synergistic influences on infant-carrying behavior or alternatively that associations between T and E2 and rates of infant-carrying are influenced by stress or other glucocorticoid-related variables. Finally, we propose a hypothesis suggesting that experience-related changes in hormones reinforce the commitment of males to successful breeding partnerships.

Pre- and postpartum sex steroids in female marmosets (Callithrix kuhlii) : Is there a link with infant survivorship and maternal behavior ?

Recent studies in primates have suggested that pre- and peripartum sex steroid hormones may be important determinants of maternal behavior and motivation, since higher levels of prepartum estrogen are associated with maternal competency and infant survivorship. To test the cross-species generality of this finding, we monitored excreted profiles of estradiol (E(2)), progesterone metabolites (pregnanediol glucuronide; PdG), and E(2):PdG ratios throughout pregnancy in black tufted-ear marmosets (Callithrix kuhlii). Additionally, we wanted to determine the extent to which variability in maternal carrying effort was related to hormonal factors and relative levels of maternal experience. For six females, hormonal profiles were determined by enzyme immunoassay for two pregnancies, one in which infants survived at least 2 weeks postpartum and one in which infants did not survive. Our within-subjects analyses revealed significant differences in mean prepartum E(2) levels for females in the different infant survival conditions. In contrast to previous findings, however, females exhibited significantly higher prepartum E(2) levels when their infants did not survive a minimum of 2 weeks postpartum, relative to when their infants did survive. Maternal carrying effort was also negatively and significantly correlated with prepartum E(2) levels. Unlike previous reports in callitrichid primates, then, our data suggest that high concentrations of prepartum E(2) in callitrichid primates are not necessarily associated with competent maternal behavior and may instead be associated with poor infant survivorship and inadequate maternal care. Further, our results appear to be convergent with research focusing on human mothers and may represent a common underlying mechanism linking prepartum estrogen and postpartum affect and behavior in some primates.

Elevated urinary testosterone excretion and decreased maternal caregiving effort in marmosets when conception occurs during the period of infant dependence.

The proximate mechanisms that regulate transitions in mammalian female reproductive effort have not been widely studied. However, variation in circulating levels of the androgenic steroid hormone testosterone (T) appears to mediate a trade-off between investment in current and future offspring in males [Ketterson, E.D., Nolan, V., Jr., 1992. Hormones and life histories: an integrative approach. Am. Nat. 140, S33-S62; Ketterson, E.D., Nolan, V., Jr., 1994. Hormones and life histories: an integrative approach. In: L.A. Real (Ed.), Behavioral Mechanisms in Evolutionary Ecology, University of Chicago Press, Chicago, pp. 327-353; Ketterson, E. D., Nolan, V., Jr., 1999. Adaptation, exaptation, and constraint: A hormonal perspective. Am. Nat. 154S, S4-S25]. The purpose of this study was to investigate the possibility that T is also associated with transitions in the reproductive effort of females, by examining the relationship between urinary T excretion, maternal caregiving behavior, and the timing of the postpartum conception in female Wieds black tufted-ear marmosets (Callithrix kuhlii). We examined the maternal carrying effort and peripartum T profiles of six females across two conditions: (1) when they conceived during the period of infant dependence (DPID), such that gestation was coupled with lactation; and (2) when the same females conceived after the period of infant dependence (APID). We also assessed the relationship between postpartum T levels and caregiving effort. When female marmosets conceived DPID, they dramatically reduced their caregiving effort, and had higher levels of urinary T, relative to when they conceived APID. Further, the litter-to-litter changes in maternal caregiving effort that we observed were related to variation in urinary T excretion; as weekly levels of urinary T excretion increased, concurrent caregiving effort declined. Our results suggest that variation in T secretion may regulate transitions in female reproductive behavior, and that the regulation of male and female parental behavior may be mediated by homologous neuroendocrine mechanisms.

Nighttime Wakefulness Associated with Infant Rearing in Callithrix kuhlii

Parent-infant cosleeping occurs in human and nonhuman primates, yet studies on the impact of cosleeping on parental sleep patterns have been limited to human mothers. We examined the effects of cosleeping on the nighttime wakefulness of a biparental New World primate, Wieds black tufted-ear marmoset (Callithrix kuhlii). We compared the sleep patterns of marmoset parents caring for young infants to those without infants, using an 8 mm videocamera and timelapse VCR under infrared illumination. The presence of young infants significantly impacted the sleep of mothers but not fathers. In fact, mothers rearing young infants were awake >3 times as often as mothers without infants. We also examined the nighttime wakefulness of marmoset parents across the first 9 weeks of infant life (birth through weaning). Although callitrichid mothers tend to reduce their daytime investment in offspring very early in infant life by relinquishing the care of infants to fathers and alloparents, increased nighttime wakefulness was not limited to the early postpartum period for the mothers. Instead, mothers exhibited more nighttime wakefulness than fathers did across the first 9 weeks of infant life. Our results indicate that the presence of infants has a greater impact on the sleep patterns of Callithrix kuhlii mothers than fathers, suggesting that mothers are more involved in infant care than previously realized and that fathers are not nearly as involved in nighttime care as their behavior during the day would suggest.

FAMILY LIFE IN MARMOSETS: CAUSES AND CONSEQUENCES OF VARIATION IN CAREGIVING

Publisher Summary It is critical that one understand both the causes of variation in the quality and quantity of care provided to offspring in a family environment, and the consequences of this variation for later biobehavioral profiles in adolescents and adults. This chapter examines both issues in marmosets, who are mostly monogamous, biparental, and family-living primates from the eastern coastal forests of Brazil. This chapter highlights both endocrine and genetic influences on variation in maternal and paternal care, and documents the preliminary evidence of the pervasive and persistent effects of variation in early care for later somatic, physiological, and behavioral functioning in marmosets. Understanding of social contributions to epigenesis is growing rapidly, particularly those aspects of development that are systematically influenced by variation in early maternal care. In this sense, variation in the nature of dyadic interactions between mothers and offspring can alter developmental trajectories in important ways. The data presented in the chapter provides a compelling argument that family contexts, with the possibility of triadic and higher order social interactions, also constitute an important component of early epigenesis. The marmoset is an ideal animal model for evaluating these influences, since there are multiple classes of individuals providing care for offspring. Further, the ability to identify important sources of variation in care, and to track the consequences of these differences longitudinally, makes the marmoset particularly useful for providing insights into the ways in which family social environments shape offspring.

Family Life In Marmosets

Publisher Summary It is critical that one understand both the causes of variation in the quality and quantity of care provided to offspring in a family environment, and the consequences of this variation for later biobehavioral profiles in adolescents and adults. This chapter examines both issues in marmosets, who are mostly monogamous, biparental, and family-living primates from the eastern coastal forests of Brazil. This chapter highlights both endocrine and genetic influences on variation in maternal and paternal care, and documents the preliminary evidence of the pervasive and persistent effects of variation in early care for later somatic, physiological, and behavioral functioning in marmosets. Understanding of social contributions to epigenesis is growing rapidly, particularly those aspects of development that are systematically influenced by variation in early maternal care. In this sense, variation in the nature of dyadic interactions between mothers and offspring can alter developmental trajectories in important ways. The data presented in the chapter provides a compelling argument that family contexts, with the possibility of triadic and higher order social interactions, also constitute an important component of early epigenesis. The marmoset is an ideal animal model for evaluating these influences, since there are multiple classes of individuals providing care for offspring. Further, the ability to identify important sources of variation in care, and to track the consequences of these differences longitudinally, makes the marmoset particularly useful for providing insights into the ways in which family social environments shape offspring.

Chapter 30 – Family Life In Marmosets: Causes and Consequences of Variation in Caregiving

Publisher Summary It is critical that one understand both the causes of variation in the quality and quantity of care provided to offspring in a family environment, and the consequences of this variation for later biobehavioral profiles in adolescents and adults. This chapter examines both issues in marmosets, who are mostly monogamous, biparental, and family-living primates from the eastern coastal forests of Brazil. This chapter highlights both endocrine and genetic influences on variation in maternal and paternal care, and documents the preliminary evidence of the pervasive and persistent effects of variation in early care for later somatic, physiological, and behavioral functioning in marmosets. Understanding of social contributions to epigenesis is growing rapidly, particularly those aspects of development that are systematically influenced by variation in early maternal care. In this sense, variation in the nature of dyadic interactions between mothers and offspring can alter developmental trajectories in important ways. The data presented in the chapter provides a compelling argument that family contexts, with the possibility of triadic and higher order social interactions, also constitute an important component of early epigenesis. The marmoset is an ideal animal model for evaluating these influences, since there are multiple classes of individuals providing care for offspring. Further, the ability to identify important sources of variation in care, and to track the consequences of these differences longitudinally, makes the marmoset particularly useful for providing insights into the ways in which family social environments shape offspring.