Variations in male parenting behavior and physiology in the common marmoset

Abstract

Infant survival and wellbeing is dependent upon good parenting skills. In some species of primates, fathers are necessary to ensure both positive developmental and social outcomes for their offspring. Common marmosets and the related cotton-top tamarin monkeys provide extensive paternal care of multiple offspring and are essential for infant survival. However, we have found significant variation in a father’s motivation to respond to infant stimuli. Additionally, marmoset males who are experienced fathers are significantly more motivated to respond to infants and infant stimuli than adult males who have yet to be fathers. Expectant fathers appear to be preparing for their energetic role in infant care by responding with increases in multiple reproductive hormones and showing weight gain during their mate’s pregnancy. Male marmosets have been shown to be hormonally responsive to scent signals. Males show increased testosterone shortly after smelling periovulatory scents and lower levels of testosterone following presentation of their own infant’s scent. These two inverse testosterone responses combined indicate that paternal males have a flexible system of responding to socially relevant odor cues. Thus males can be ready to mate when their mate is fertile while continuing to be responsive to their infants when these two events occur simultaneously. A male’s hormonal and physical responsiveness to parenting may be due to pair bonding between the male and his mate. Examining the variability between males in their behavioral, physical, and hormonal responses to their mate’s pregnancy, and infant stimuli provides the means for determining the mechanisms of good parenting in fathers.

Hormonal Correlates of Paternal Care Differences in the Hylobatidae

“…For example, Dixson and George [1982] not only found a reciprocal relationship between testosterone and prolactin in C. jacchus, but they also discovered that males had lower testosterone concentrations after infant carrying. Also in C. jacchus, Prudom et al [2008] and Ziegler et al [2009aZiegler et al [ , 2011 found a similar relationship between lower testosterone concentrations in fathers and direct infant stimuli. Similarly, in C. kuhlii, Nunes et al [2000Nunes et al [ , 2001 found that testosterone concentrations were lower among males who carried infants at high rates than males who carried infants at low rates.…”

“…Prudom et al [2008] and Ziegler et al [2009aZiegler et al [ , 2011 found that fathers demonstrate lower testosterone concentrations following direct stimuli from an infant. Similarly, Dixson and George [1982] discovered that males had lower testosterone concentrations after they had carried infants.…”

“…Still, no studies to date have examined proximate hormonal mechanisms that may be crucial to our understanding of differences in paternal care in the hylobatids. This is surprising, given that in recent years many studies have begun to focus research on hormones as potential mediating factors of paternal care in other biparental primate species, including common marmosets (Callithrix jacchus) [Dixson and George 1982, Ziegler et al, 2009a,b, 2011, black tufted-ear marmosets (C. kuhlii) [Nunes et al, 2000[Nunes et al, , 2001, cotton-top tamarins (Saguinus oedipus) [Ziegler and Snowdon, 2000;Ziegler et al, 1996Ziegler et al, , 2004, and humans (H. sapiens) [Fleming et al, 2002;Gray et al, 2006Gray et al, , 2007Storey et al, 2000].…”

“…Although, paternal care is rare among primates, it is known to occur in several well-studied genera of New World primates, including Callicebus, Aotus, Callimico, Callithrix, Cebuella, Leontopithecus, and Saguinus [Kleiman, 1985;Kleiman and Malcolm, 1981;Ziegler et al, 2004Ziegler et al, , 2009a. The only apes that exhibit paternal care, with the possible exception of Homo sapiens, are members of the family Hylobatidae.…”

When Dads Help: Male Behavioral Care During Primate Infant Development

“…For example, the in fl uence of hormones like prolactin, vasopressin, oxytocin, and testosterone in relation to bonding and infant care, or behavioral trade-offs between care and mate-acquisition have been extensively studied, even if still not completely understood (Bales et al 2004 ;Brockmann et al 2001 ;Gettler et al 2011 ;Goymann et al 2007 ;Gray et al 2007 ;Hirschenhauser and Oliveira 2006 ;Huck et al 2005 ;Schradin and Anzenberger 2002 ;Schradin et al 2003 ;Trainor andMarler 2001, 2002 ;Wing fi eld et al 1990 ;Ziegler 2000 ;Ziegler et al 1996Ziegler et al , 2000 . Differences in hormone production, responsiveness, or ontogenetic exposure may partly explain individual differences in caretaking behavior (Birnie et al 2011 ;Drea 2007 ;Ziegler et al 2009 ) . Other in fl uential factors include the rank, age and previous experience of the caretaker, sex of the infant, group size and composition, relatedness between caretaker and infant or mother, season of conception, or predation risk (Anderson 1992 ;Bercovitch 2002 ;Hoage 1977 ;McGrew 1988 ;O'Brien and Robinson 1991 ;Pryce 1988 ) .…”