Katherine E. Wynne-Edwards

Hormonal correlates of paternal responsiveness in new and expectant fathers

Little is known about the physiological and behavioral changes that expectant fathers undergo prior to the birth of their babies. We measured hormone concentrations and responses to infant stimuli in expectant and new fathers living with their partners to determine whether men can experience changes that parallel the dramatic shifts seen in pregnant women. We obtained two blood samples from couples at one of four times before or after the birth of their babies. After the first sample, the couples were exposed to auditory, visual, and olfactory cues from newborn infants (test of situational reactivity). Men and women had similar stage-specific differences in hormone levels, including higher concentrations of prolactin and cortisol in the period just before the births and lower postnatal concentrations of sex steroids (testosterone or estradiol). Men with more pregnancy (couvade) symptoms and men who were most affected by the infant reactivity test had higher prolactin levels and greater post-test reduction in testosterone. Hormone concentrations were correlated between partners. This pattern of hormonal change in men and other paternal mammals, and its absence in nonpaternal species, suggests that hormones may play a role in priming males to provide care for young.

Stress Hormones: A Link between Maternal Condition and Sex-Biased Reproductive Investment

In species where offspring fitness is sex‐specifically influenced by maternal reproductive condition, sex allocation theory predicts that poor‐quality mothers should invest in the evolutionarily less expensive sex. Despite an accumulation of evidence that mothers can sex‐specifically modulate investment in offspring in relation to maternal quality, few mechanisms have been proposed as to how this is achieved. We explored a hormonal mechanism for sex‐biased maternal investment by measuring and experimentally manipulating baseline levels of the stress hormone corticosterone in laying wild female European starlings (Sturnus vulgaris) and examining effects on sex ratio and sex‐specific offspring phenotype adjustment. Here we show that baseline plasma corticosterone is negatively correlated with energetic body condition in laying starlings, and subsequent experimental elevation of maternal baseline plasma corticosterone increased yolk corticosterone without altering maternal condition or egg quality per se. Hormonal elevation resulted in the following: female‐biased hatching sex ratios (caused by elevated male embryonic mortality), lighter male offspring at hatching (which subsequently grew more slowly during postnatal development), and lower cell‐mediated immune (phytohemagglutinin) responses in males compared with control‐born males; female offspring were unaffected by the manipulation in both years of the study. Elevated maternal corticosterone therefore resulted in a sex‐biased adjustment of offspring quality favorable to female offspring via both a sex ratio bias and a modulation of male phenotype at hatching. In birds, deposition of yolk corticosterone may benefit mothers by acting as a bet‐hedging strategy in stochastic environments where the correlation between environmental cues at laying (and therefore potentially maternal condition) and conditions during chick‐rearing might be low and unpredictable. Together with recent studies in other vertebrate taxa, these results suggest that maternal stress hormones provide a mechanistic link between maternal quality and sex‐biased maternal investment in offspring.

Hormonal changes in males of a naturally biparental and a uniparental mammal

Blood samples from male hamsters (Phodopus) during their mates gestation and early lactation show that key hormones important in maternal behavior are also changing in males and differ for two closely related species with different levels of paternal care. Results of study 1 were consistent with a relationship between higher prolactin, lower testosterone and paternal behavior during early lactation in P. campbelli and provided no evidence for similar hormonal changes in P. sungorus. Study 2 sampled males before or after the birth. Prolactin did not increase until at least one day after the birth in P. campbelli but was high at the end of the pregnancy in P. sungorus. Increasing testosterone concentrations in P. campbelli as the birth approached were consistent with mate guarding, high testosterone concentrations on L5 were consistent with paternal aggression in defense of the litter, and the drop in testosterone after the birth was consistent with reduced aggression toward the new pups. Results confirmed that cortisol concentrations were reduced following the establishment of a pair-bond and found that P. campbelli males had elevated cortisol before the birth. Results support the hypothesis that mammalian paternal behavior has a hormonal basis which is analogous to maternal behavior.

Hormonal Changes in Mammalian Fathers

Known and hypothesized relationships between steroid (estradiol, testosterone, and cortisol) and peptide (oxytocin, vasopressin, and prolactin) hormones and the expression of mammalian paternal behavior are reviewed. Emphasis is placed on newly emerging animal models, including nonhuman primates and men, with elaborate paternal behavior repertoires. Currently available data are broadly consistent with a working hypothesis that the expression of parental behavior will involve homologous neuroendocrine circuits in male and females. Understanding the neuroendocrinology of paternal behavior is an emerging research opportunity in behavioral neuroscience.

Paternal care in rodents: weakening support for hormonal regulation of the transition to behavioral fatherhood in rodent animal models of biparental care.

Male rodents that are naturally paternal, like all females, must inhibit infanticide and activate direct parental behavior as they become parents. Males, however, alter their behavior in the absence of parturition, postpartum ovulation and lactation, and therefore do not experience the hormone dynamics associated with such conditions. Paternal males might nevertheless use the same hormones to activate pre-existing maternal behavior pathways in the brain. Positive and inverse associations between prolactin, sex steroids (estradiol, testosterone, progesterone), glucocorticoids, oxytocin and vasopressin and paternal behavior are reviewed. Across biparental rodents (Phodopus campbelli, Peromyscus californicus, Microtus ochrogaster, and Meriones unguiculatus), as well as non-human primates and men, hormone-behavior associations are broadly supported. However, experimental manipulations (largely restricted to P. campbelli) suggest that the co-variation of hormones and paternal behavior is not causal in paternal behavior. Perhaps the hormone-behavior associations shared by P. campbelli and other paternal males are important for other challenges at the same time as fatherhood (e.g., mating during the postpartum estrus). On the other hand, each paternal species might, instead, have unique neuroendocrine pathways to parental behavior. In the latter case, future comparisons might reveal extraordinary plasticity in how the brain forms social bonds and alters behavior in family groups.

Cortisol reactivity to social stress in adolescents: Role of depression severity and child maltreatment

This study examined the hypothesis that depressed adolescents with a history of childhood maltreatment will show greater cortisol reactivity to psychological stress challenge than those without, and this relation will be moderated by level of depression severity. Seventy-one adolescents were exposed to the Trier Social Stress Test. Salivary cortisol was assessed at baseline, immediately before the challenge, after the challenge, and during an extended recovery period. Childhood maltreatment was assessed with a rigorous contextual interview and rating system. Adolescents with a history of maltreatment produced higher and more prolonged levels of cortisol in response to the challenge than did adolescents with no maltreatment, but only among those with a mild/moderate level of depression severity. Those with moderate/severe depression exhibited a blunted cortisol response regardless of child maltreatment history. These findings indicate that depression is a heterogeneous syndrome, and that both depression severity and child maltreatment history should be considered in studies examining biological stress reactivity.

Biparental care in Djungarian but not Siberian dwarf hamsters (Phodopus)

Parental behaviour was directly observed during two 30-min bouts on each of the first 18 days after birth for both Djungarian, P. campbelli, and Siberian, P. sungorus, dwarf hamster litters. Results were consistent with predictions based on earlier studies that demonstrated a positive impact of paternal presence on pup survival in P. campbelli, but not P. sungorus. The presence of the father or an aunt significantly decreased, by about half, the proportion of time that pups were alone in P. campbelli. Because brief parental absences were unlikely to result in pup cooling, analyses also considered only those absences that were 3 min or longer. By those criteria, P. campbelli pups housed with a second adult were rarely alone. In contrast, the father had little impact on the parental care received by pups in P. sungorus. Phodopus sungorus males were rarely alone in the nest with the pups, whereas both fathers and aunts in P. campbelli were alone with the pups significantly more often than the mother from mid-lactation until weaning. This behaviour reflected temporal coordination between the behaviour of the adults. Pups were left alone less often than expected based on the independent behaviour of each adult. Because there was no reason to expect alloparental care by aunts in the wild, the presence of a second adult, rather than specific parental behaviour by that adult, may be the essential component of increased pup survival. Limited observations of male parental care in the wild demonstrated that significant paternal care could occur in P. campbelli. Both field and laboratory data, however, suggest that biparental care would be facultative and adaptive under certain environmental conditions (e.g. extreme temperatures) but not all.

Behavioral endocrinology of mammalian fatherhood

Mammalian fatherhood involves a muted version of the maternal experience. In spite of previous assumptions to the contrary, hormones influence mammalian paternal behavior. Naturally paternal males experience dynamic changes in the same hormones involved in maternal behavior and these hormones have access to the same brain pathways. Men becoming fathers for the first time are similar to their female partners too. These recent studies are still correlational, but promise to illuminate maternal behavior and to biologically validate the experiences of involved fathers.

Repeated exposure to stress across the childhood-adolescent period alters rats' anxiety- and depression-like behaviors in adulthood: The importance of stressor type and gender.

This research tests the hypothesis that specific forms of adversity in early life map onto behavioral signs analogous to depression versus anxiety in later life. Male and female rats were exposed to either severe sporadic stress or chronic mild stress during the childhood-adolescent period, and their behavior was tested in adulthood. Males in the severe sporadic stress group showed exaggerated anxiety-related behaviors, as indicated by increases in shock-probe burying and escape-like responses (jumps) from the open arms of the elevated plus-maze. Females exposed to severe sporadic stress displayed no change in burying behavior but did display increases in escape behavior. These same females also exhibited behaviors analogous to depression that manifested as decreased sucrose consumption. The chronic mild stress regime produced effects only in females, including reduced burying, decreased sucrose consumption, and an exaggerated corticosterone response to cold-water immersion stress. Findings reiterate the importance of early life experience to the development of adult psychopathologies and emphasize the need to consider both the type of early experience and gender differences in these analyses.

Progesterone receptors mediate male aggression toward infants

Neuroendocrine mechanisms that mediate male aggression toward infants are poorly understood. Although testosterone is known to enhance aggression in other social contexts, evidence that it modulates aggression toward infants is equivocal. We have found that male progesterone receptor knockout (PRKO) mice exhibit no infanticidal behavior and little aggression toward young. Male PRKO mice also display significantly enhanced parental behaviors. In wild-type mice, blockade of PR induces a behavioral phenotype similar to that of the PRKO males, whereas progesterone exacerbates aggressive tendencies toward infants. Aggressive behaviors directed toward adult males, by contrast, are unaffected by progesterone, PR antagonism, or PR gene deletion. Previously thought to be of diminished importance in male animals, PRs play a critical and specific role in modulating infant-directed behaviors in male mice.