Dads: Progress in understanding the neuroendocrine basis of human fathering behavior.

We outline the progress on the hormonal basis of human paternal behavior during the past twenty years. Advances in understanding the roles of testosterone, prolactin, oxytocin and vasopressin in fathering behavior are described, along with recent research on hormonal interactions, such as those between testosterone and cortisol, and testosterone and the peptide hormones. In addition, we briefly describe the recent leaps forward in elucidating the neurobiological and neuroendocrine basis of fatherhood, made possible by fMRI technology. Emerging from this literature is a developing and complicated story about fatherhood, highlighting the need to further understand the interplay between behavior, physiology, social context, and individual genetic variation. Given the changing roles of parents in many societies, the continued growth of this research area will provide a strong empirical knowledge base about paternal behavior on which to create policies promoting fathers' involvement in their infants' lives.

Primate paternal care: Interactions between biology and social experience.

This article is part of a Special Issue "Parental Care".We review recent research on the roles of hormones and social experiences on the development of paternal care in humans and non-human primates. Generally, lower concentrations of testosterone and higher concentrations of oxytocin are associated with greater paternal responsiveness. Hormonal changes prior to the birth appear to be important in preparation for fatherhood and changes after the birth are related to how much time fathers spend with offspring and whether they provide effective care. Prolactin may facilitate approach and the initiation of infant care, and in some biparental non-human primates, it affects body mass regulation. Glucocorticoids may be involved in coordinating reproductive and parental behavior between mates. New research involving intranasal oxytocin and neuropeptide receptor polymorphisms may help us understand individual variation in paternal responsiveness. This area of research, integrating both biological factors and the role of early and adult experience, has the potential to suggest individually designed interventions that can strengthen relationships between fathers and their partners and offspring.

The effects of social context on the hormonal and behavioral responsiveness of human fathers.

We tested first-time fathers with their 22-month old toddlers to determine whether social context variables such as pre-test absence from the child and presence of the mother affected physiological measures associated with paternal responsiveness. Heart rate and blood pressure readings as well as blood samples to determine prolactin, testosterone and cortisol levels were taken before and after the 30-min father-toddler interactions. Fathers were tested on a day when they were away from their child for several hours before testing ('without-child' day) and on another day where they remained with their child throughout the day ('with-child' day). Most measures decreased over the 30-min test period but relative decreases were context-dependent. Men maintained higher prolactin levels when they were away from their children longer before testing on the 'without-child' day. Cortisol levels decreased during both tests and they decreased more on the 'with-child' day for men who had spent more time alone with their toddler before the test. Heart-rate and diastolic (but not systolic) blood pressure decreased more on the 'with-child' day than on the 'without-child' day. Fathers' testosterone levels decreased when their partners were less involved in the interactions. Compared to men with high responsiveness ratings on both days, men whose responsiveness increased after being away from their child on the 'without-child' day maintained higher systolic blood pressure and had a greater decrease in testosterone levels. We conclude that context may be more important in determining fathers' physiological responses to child contact than has previously been appreciated, particularly for some individuals.

Physiological Indicators of Attachment in Domestic Dogs (Canis familiaris) and Their Owners in the Strange Situation Test.

Behaviorally, attachment is demonstrated when one individual maintains close proximity to another individual and shows distress upon separation. For 29 owner-dog dyads, we employed a modified Ainsworth's Strange Situation Test (SST) to investigate whether both members would show a physiological reaction to separation. Dogs experienced a series of separation from and reuniting events with their owners and were introduced to a stranger. Before and after the SST, saliva samples were taken from each dyad to measure stress-related analytes: cortisol (CORT) and chromogranin A (CgA). Dogs exhibited attachment behaviors toward owners as evidenced by more time spent in close proximity, more contact initiated and less time spent near the door, compared to episodes with the stranger. Dogs that initiated more contact with their owners in re-uniting episodes had lower CgA than dogs that initiated less contact, but their owners had higher CgA levels. Also during re-uniting episodes, dogs and owners spent more time near each other when owner CgA levels were low, owner CORT levels were high, and the dog had owner-reported separation anxiety. During the episodes alone with the stranger, dogs with higher CORT spent more time with the stranger. Finally, dogs' initial CgA levels were correlated with their owner's initial CORT levels, and dog final CORT levels were correlated with their owners' final CORT levels, suggesting some hormonal synchrony within the dyad. As all owner-dog dyads were assessed as securely attached, attachment style differences could not explain variation in hormonal or behavioral results. These results suggest that dogs may respond to owner hormonal state and/or behavior and demonstrate that individual differences in responses to a behavioral challenge reflect the stress physiology of both dogs and their owners.

Balancing personal maintenance with parental investment in a chick-rearing seabird: physiological indicators change with foraging conditions.

Seabird parents use a conservative breeding strategy that favours long-term survival over intensive parental investment, particularly under harsh conditions. Here, we examine whether variation in several physiological indicators reflects the balance between parental investment and survival in common murres (Uria aalge) under a wide range of foraging conditions. Blood samples were taken from adults during mid-chick rearing from 2007 to 2014 and analysed for corticosterone (CORT, stress hormone), beta-hydroxybutyrate (BUTY, lipid metabolism reflecting ongoing mass loss), and haematocrit (reflecting blood oxygen capacity). These measures, plus body mass, were related to three levels of food availability (good, intermediate, and poor years) for capelin, the main forage fish for murres in this colony. Adult body mass and chick-feeding rates were higher in good years than in poor years and heavier murres were more likely to fledge a chick than lighter birds. Contrary to prediction, BUTY levels were higher in good years than in intermediate and poor years. Murres lose body mass just after their chicks hatch and these results for BUTY suggest that mass loss may be delayed in good years. CORT levels were higher in intermediate years than in good or poor years. Higher CORT levels in intermediate years may reflect the necessity of increasing foraging effort, whereas extra effort is not needed in good years and it is unlikely to increase foraging success in poor years. Haematocrit levels were higher in poor years than in good years, a difference that may reflect either their poorer condition or increased diving requirements when food is less available. Our long-term data set provided insight into how decisions about resource allocation under different foraging conditions are relating to physiological indicators, a relationship that is relevant to understanding how seabirds may respond to changes in marine ecosystems as ocean temperatures continue to rise.

Social and hormonal bases of individual differences in the parental behaviour of birds and mammals.

We present an overview of research on how social experiences and hormonal responses affect individual variation in parental care of birds and mammals. The parental roles of prolactin and glucorticoids (corticosterone or cortisol) have many similarities in birds and in mammals. Prolactin may be involved in the initiation of parental interactions, with prolactin variation possibly explaining individual differences in parental decision-making. Glucocorticoid levels increase when parents have to work harder, with some individuals showing greater hormonal and behavioural responses than others. Testosterone interferes with paternal behaviour in birds, but its role is more complex and species-specific in male mammals. We examine these differences in an adaptive framework, where retaining flexibility of response has allowed individuals to respond differentially to social opportunities and environmental change.

Constraints on nest site selection: a comparison of predator and flood avoidance in four species of marsh-nesting birds (genera: Catoptrophorus, Larus, Rallus, and Sterna).

Nest site characteristics associated with flood and predator avoidance were compared for four nonpasserine species of marsh-nesting birds: clapper rails, willets, laughing gulls, and common terns. Species with short nests, willets and terns, minimized flood damage by nesting on higher ground than did gulls and rails that build tall nests. Species with dispersed, cryptic nests had taller surrounding grass than did open-nesting colonial species. Total nest height was similar for species with tall nests and for terns whose short nests were elevated by placement on mats of dead Spartina grass. Willets had lower nest heights than the other species, probably because the inverse relation between grass height and ground height in the salt marsh makes it difficult for willets to find sites with high enough ground for flood avoidance while still retaining high enough grass for nest crypticity. Ground height for common terns and grass height for gulls and rails appear to be cues used in nest site selection. Nests of each species in which these characteristics were maximized were more successful in a major tidal flood. Laughing gulls and clapper rails appear to be more specialized salt marsh nesters than the other two species.

Nest-site safety predicts the relative investment made in first and replacement eggs by two long-lived seabirds.

Comparative studies of birds suggest that differences in nest-site characteristics, such as between open-nesting and cavity-nesting species, might ultimately underlie much interspecific variation in clutch size and renesting capacity. The "renesting hypothesis" holds that in species that typically enjoy high breeding success because they nest in safe sites, individuals maximize fitness by laying large first clutches early in the season while withholding few resources for renesting attempts. We tested whether differences in nesting habits would be associated with differences in egg size and renesting capacity in razorbills (Alca torda) and Brünnich's guillemots (Uria lomvia), long-lived marine birds of the tribe Alcini (family Alcidae) that lay single-egg clutches. Razorbills nest in a dispersed fashion, often building nests of small stones and other matter in enclosed crevices where their eggs and chicks are safe from avian predators. Brünnich's guillemots nest very densely on exposed cliff ledges and do not build nests. Due to these differences in nesting habits, razorbills experience higher hatching success than Brünnich's guillemots. As predicted by the renesting hypothesis, razorbills laid larger eggs than guillemots, after accounting for differences in adult body mass. Associated with this larger investment in first eggs, razorbills were less likely than guillemots to replace lost eggs, and they took longer to do so. As these results were obtained by experimentally removing eggs from early-laying females, they presumably assessed the tendencies of more capable birds in both species. Data from other colonies and years were consistent with these results. We conclude that differences in nesting habits have led to evolutionary divergence in the investment made in first and replacement eggs by these two closely related species.

Will the early bird get the mate? Egg lay order influences neural development in European Starling chicks.

We investigated the role of egg lay order on growth and neural development in pre-fledgling European Starlings, Sturnus vulgaris. Chicks hatched from early-laid eggs had larger relative RA volumes than chicks hatched from later-laid eggs. There were no relationships between lay order and the volume of other brain regions, or chick growth metrics. In adult birds, RA volume is related to song repertoire size, and may affect mate attraction ability. Lay order effects on adult song nuclei should be examined further.

The effects of variable foraging conditions on common murre (Uria aalge) corticosterone concentrations and parental provisioning.

This study investigated how total corticosterone concentrations, chick-feeding rates, and adult body mass changed with food availability from 1998 to 2000 in the same individually marked common murres (Uria aalge). Capelin, the main prey species, arrived inshore by the onset of murre chick hatching in 1998 and 1999 (prey match years); whereas in 2000, hatching began approximately 1 week before the capelin arrived inshore to spawn (prey mismatch year). Serum corticosterone concentrations were higher in the same individuals in the prey mismatch year than they were in either of the match years. Birds sampled before peak capelin spawning in the mismatch year had higher corticosterone levels than murres sampled after peak spawning. Murres with higher corticosterone levels had higher chick-feeding rates and less mass loss in the mismatch year (compared to the match year 1999) than birds with lower levels. Corticosterone levels did not differ between birds that had not foraged for at least 12 h (brooded chick overnight) and those that had, suggesting that short-term food deprivation did not affect corticosterone concentrations. Taken together, these findings suggest that the difference between years reflects a baseline shift in corticosterone levels, particularly in the high-quality birds that were able to increase both corticosterone concentrations and foraging effort.

Prolactin responses to infant cues in men and women: effects of parental experience and recent infant contact.

We used a longitudinal design to test whether parental experience differentially affects the development of prolactin responses to infant cues in men and women. Couples provided two blood samples at three tests, one test just before their babies were born, and two tests during the early postnatal period (n=21). Nine couples repeated the tests near the birth of their second babies. In the 30 min between the two samples, couples listened to recorded infant cries at the prenatal test and held their baby (fathers) or a doll (mothers) at the postnatal tests. Blood samples were analyzed for prolactin concentrations. Prolactin values were then related to sex and parity differences as well as to questionnaire data concerning emotional responses to infant cries and previous infant contact. We found that (1) prior to the birth of both the first and second babies, women's prolactin concentrations increased after exposure to infant stimuli, whereas men's prolactin concentrations decreased; postnatal sex differences varied with parity; (2) women's prolactin reactivity did not change significantly with parental experience; (3) the same men's prolactin concentrations decreased after holding their first newborns but increased after holding their second newborns; this change was not gradual or permanent; (4) men reporting concern after hearing recorded infant cries showed a different postnatal pattern of prolactin change after holding their babies than men not reporting concern; and (5) men who had little contact with their babies just prior to testing had a more positive prolactin response than men who had recently held their babies for longer periods. Although parental experience appears to affect men's prolactin responses, differences in reactivity were also related to patterns of recent infant contact and individual differences in responses to infant cues.