Hormones associated with non-maternal infant care: a review of mammalian and avian studies

Hormonal changes during non-maternal infant care have been demonstrated in many cooperatively breeding bird species, some monogamous rodents and two species of New World primates. Coevolution of hormones and social traits may have provided for the different breeding systems that occur today. Several hormones have been shown to covary with the breeding systems of vertebrates. Elevated levels of the hormone prolactin with male parenting behaviours are common to many birds, rodents and the callitrichid monkeys Callithrix jacchus and Saguinus oedipus. In birds, prolactin may be elevated in both male and female breeders during various stages of nest building, egg laying, incubating and feeding of young. Testosterone levels appear to have an inverse relationship to prolactin levels during infant care in birds and rodents, but this relationship has not been examined for primates. In cooperatively breeding birds, helpers who remain at the nest also have elevated levels of prolactin when displaying parental care behaviours. Prolactin levels are elevated in helper callitrichid monkeys during the postpartum period. Monogamous male rodents demonstrate elevated prolactin levels with parental care behaviour but, in contrast to the birds, the mechanisms mediating prolactin increase appear to differ for male and female rodents. Two factors may influence male parental behaviours and hormonal changes: stimuli from the pregnant female and stimuli from the newborn pups; whereas maternal behaviours are influenced by the maternal hormones of the female and the pup stimuli. An experiential factor may also influence male parental behaviours. Neuropeptides such as oxytocin and vasopressin appear to be involved in male rodent parental care and there may be an interaction between a series of hormones and neurosecretions and stimuli from mates and pups. Studies of Saguinus oedipus, the cotton-top tamarin, suggest that prolactin levels are responsive to stimuli from contact with infants and the level of infant care experience influences the levels of prolactin with male infant care. Father tamarins also have elevated levels of prolactin before the birth of infants suggesting that cues from the pregnant female are important. Prolactin's role in parental care may have evolved from prolactin's role in other reproductive functions. Hormonal regulation of non-maternal care may occur due to a complex interaction of many hormones and neurotransmitters. Studies described here should provide the impetus for further work on parental care hormones in a wide variety of primates.     

Endocrine and neuroendocrine regulation of fathering behavior in birds

This article is part of a Special Issue "Parental Care".Although paternal care is generally rare among vertebrates, care of eggs and young by male birds is extremely common and may take on a variety of forms across species. Thus, birds provide ample opportunities for investigating both the evolution of and the proximate mechanisms underpinning diverse aspects of fathering behavior. However, significant gaps remain in our understanding of the endocrine and neuroendocrine influences on paternal care in this vertebrate group. In this review, I focus on proximate mechanisms of paternal care in birds. I place an emphasis on specific hormones that vary predictably and/or unpredictably during the parental phase in both captive and wild birds: prolactin and progesterone are generally assumed to enhance paternal care, whereas testosterone and corticosterone are commonly—though not always correctly—assumed to inhibit paternal care. In addition, because endocrine secretions are not the sole mechanistic influence on paternal behavior, I also explore potential roles for certain neuropeptide systems (specifically the oxytocin–vasopressin nonapeptides and gonadotropin inhibitory hormone) and social and experiential factors in influencing paternal behavior in birds. Ultimately, mechanistic control of fathering behavior in birds is complex, and I suggest specific avenues for future research with the goal of narrowing gaps in our understanding of this complexity. Such avenues include (1) experimental studies that carefully consider not only endocrine and neuroendocrine mechanisms of paternal behavior, but also the ecology, phylogenetic history, and social context of focal species; (2) investigations that focus on individual variation in both hormonal and behavioral responses during the parental phase; (3) studies that investigate mechanisms of maternal and paternal care independently, rather than assuming that the mechanistic foundations of care are similar between the sexes; (4) expansion of work on interactions of the neuroendocrine system and fathering behavior to a wider array of paternal behaviors and taxa (e.g., currently, studies of the interactions of testosterone and paternal care largely focus on songbirds, whereas studies of the interactions of corticosterone, prolactin, and paternal care in times of stress focus primarily on seabirds); and (5) more deliberate study of exceptions to commonly held assumptions about hormone–paternal behavior interactions (such as the prevailing assumptions that elevations in androgens and glucocorticoids are universally disruptive to paternal care). Ultimately, investigations that take an intentionally integrative approach to understanding the social, evolutionary, and physiological influences on fathering behavior will make great strides toward refining our understanding of the complex nature by which paternal behavior in birds is regulated.     

Fathering in rodents: Neurobiological substrates and consequences for offspring

This article is part of a Special Issue “Parental Care”. Paternal care, though rare among mammals, is routinely displayed by several species of rodents. Here we review the neuroanatomical and hormonal bases of paternal behavior, as well as the behavioral and neuroendocrine consequences of paternal behavior for offspring. Fathering behavior is subserved by many of the same neural substrates which are also involved in maternal behavior (for example, the medial preoptic area of the hypothalamus). While gonadal hormones such as testosterone, estrogen, and progesterone, as well as hypothalamic neuropeptides such as oxytocin and vasopressin, and the pituitary hormone prolactin, are implicated in the activation of paternal behavior, there are significant gaps in our knowledge of their actions, as well as pronounced differences between species. Removal of the father in biparental species has long-lasting effects on behavior, as well as on these same neuroendocrine systems, in offspring. Finally, individual differences in paternal behavior can have similarly long-lasting, if more subtle, effects on offspring behavior. Future studies should examine similar outcome measures in multiple species, including both biparental species and closely related uniparental species. Careful phylogenetic analyses of the neuroendocrine systems presumably important to male parenting, as well as their patterns of gene expression, will also be important in establishing the next generation of hypotheses regarding the regulation of male parenting behavior.     

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

Blood samples from male hamsters (Phodopus) during their mate's 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.     

Estradiol and progesterone in paternal and non-paternal hamsters (Phodopus) becoming fathers: conflict with hypothesized roles

Phodopus campbelli has an extensive paternal behavior repertoire whereas the closely-related Phodopus sungorus is not paternally responsive to a displaced pup. For the first time in a naturally paternal mammal, male estradiol and progesterone were determined during two critical phases: (1) the transition from sexually naive male to paired, expectant father that occurs in the absence of stimuli from pups (sexually naive males, paired males on G8, G12, G15, or G17 of the 18-day gestation) and (2) after pup stimuli became available to the males (paired males on days L1, L3, L5, or L12 of pup development). Hormone concentrations in naive males and between G17 and L1 (as stimuli from the birth and the pups became available to males) were also compared. Paternal responsiveness was tested on L3-L5 and confirmed species differences. Hormone concentrations in naive males were similar in the two species and males of both species had estradiol concentrations as high as fertile adult females. However, in direct contrast to predictions, estradiol concentrations were stable in P. campbelli males but increased before the birth, fell across the birth, and increased over pup development in P. sungorus males. Progesterone concentrations in P. campbelli males increased from G17 to L1 whereas a decrease had been predicted. Testosterone dynamics were consistent with previous studies. Either hormonal facilitation of paternal behavior is a hyper-variable trait that has evolved differently in different species, or, more probably, peripheral hormone concentrations are inadequate to explain the role of sex steroid hormones in paternal behavior.     

Short-term changes in fathers' hormones during father-child play: impacts of paternal attitudes and experience

Hormonal differences between fathers and non-fathers may reflect an effect of paternal care on hormones. However, few studies have evaluated the hormonal responses of fathers after interacting with their offspring. Here we report results of a 30-minute in-home experiment in which Filipino fathers played with their toddlers and consider whether paternal experience and men's perceptions of themselves as fathers affect hormonal changes. Fathers provided saliva and dried blood spot samples at baseline (B) and 30 (P30) and 60 (P60, saliva only) minutes after the interaction. We tested whether testosterone (T), cortisol (CORT), and prolactin (PRL) shifted after the intervention. In the total sample, T did not vary over the study period, while CORT declined from B to P30 and P60, and PRL also declined from B to P30. Fathers who spent more time in daily caregiving and men who thought their spouses evaluated them positively as parental caregivers experienced a larger decline in PRL (B to P30) compared to other fathers. First-time fathers also had larger declines in PRL compared to experienced fathers. Experienced fathers also showed a greater decline in CORT (B to P60) compared to first-time fathers. These results suggest that males' paternal experience and age of offspring affect hormonal responses to father–child play and that there is a psychobiological connection between men's perceptions of themselves as fathers and their hormonal responsivity to childcare.     

Short-term changes in fathers' hormones during father–child play: Impacts of paternal attitudes and experience

Hormonal differences between fathers and non-fathers may reflect an effect of paternal care on hormones. However, few studies have evaluated the hormonal responses of fathers after interacting with their offspring. Here we report results of a 30-minute in-home experiment in which Filipino fathers played with their toddlers and consider whether paternal experience and men's perceptions of themselves as fathers affect hormonal changes. Fathers provided saliva and dried blood spot samples at baseline (B) and 30 (P30) and 60 (P60, saliva only) minutes after the interaction. We tested whether testosterone (T), cortisol (CORT), and prolactin (PRL) shifted after the intervention. In the total sample, T did not vary over the study period, while CORT declined from B to P30 and P60, and PRL also declined from B to P30. Fathers who spent more time in daily caregiving and men who thought their spouses evaluated them positively as parental caregivers experienced a larger decline in PRL (B to P30) compared to other fathers. First-time fathers also had larger declines in PRL compared to experienced fathers. Experienced fathers also showed a greater decline in CORT (B to P60) compared to first-time fathers. These results suggest that males' paternal experience and age of offspring affect hormonal responses to father–child play and that there is a psychobiological connection between men's perceptions of themselves as fathers and their hormonal responsivity to childcare.     

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.     

Endocrine mechanisms,behavioral phenotypes and plasticity: known relationships and open questions

Behavior of wild vertebrate individuals can vary in response to environmental or social factors. Such within-individual behavioral variation is often mediated by hormonal mechanisms. Hormones also serve as a basis for among-individual variations in behavior including animal personalities and the degree of responsiveness to environmental and social stimuli. How do relationships between hormones and behavioral traits evolve to produce such behavioral diversity within and among individuals? Answering questions about evolutionary processes generating among-individual variation requires characterizing how specific hormones are related to variation in specific behavioral traits, whether observed hormonal variation is related to individual fitness and, whether hormonal traits are consistent (repeatable) aspects of an individual's phenotype. With respect to within-individual variation, we need to improve our insight into the nature of the quantitative relationships between hormones and the traits they regulate, which in turn will determine how they may mediate behavioral plasticity of individuals. To address these questions, we review the actions of two steroid hormones, corticosterone and testosterone, in mediating changes in vertebrate behavior, focusing primarily on birds. In the first part, we concentrate on among-individual variation and present examples for how variation in corticosterone concentrations can relate to behaviors such as exploration of novel environments and parental care. We then review studies on correlations between corticosterone variation and fitness, and on the repeatability over time of corticosterone concentrations. At the end of this section, we suggest that further progress in our understanding of evolutionary patterns in the hormonal regulation of behavior may require, as one major tool, reaction norm approaches to characterize hormonal phenotypes as well as their responses to environments.In the second part, we discuss types of quantitative relationships between hormones and behavioral traits within individuals, using testosterone as an example. We review conceptual models for testosterone-behavior relationships and discuss the relevance of these models for within-individual plasticity in behavior. Next, we discuss approaches for testing the nature of quantitative relationships between testosterone and behavior, concluding that again reaction norm approaches might be a fruitful way forward.We propose that an integration of new tools, especially of reaction norm approaches into the field of behavioral endocrinology will allow us to make significant progress in our understanding of the mechanisms, the functional implications and the evolution of hormone–behavior relationships that mediate variation both within and among individuals. This knowledge will be crucial in light of already ongoing habitat alterations due to global change, as it will allow us to evaluate the mechanisms as well as the capacity of wild populations to adjust hormonally-mediated behaviors to altered environmental conditions.     

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.     

Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhlii)

We describe temporal patterns of change in paternal behaviour and urinary concentrations of the steroid hormones testosterone (T) and oestradiol (E(2)) in male black tufted-ear marmosets, Callithrix kuhlii, relative to the birth of their young, and test predictions of the hypotheses that (1) high levels of T are incompatible with paternal care and (2) levels of T and E(2)vary with a father's prior experience in his family group. After young were born, levels of urinary T and E(2)remained near prepartum concentrations and rates at which fathers carried infants were below peak levels until the approximate time that postpartum mating ordinarily occurs, suggesting a possible trade-off between readiness to mate and paternal behaviour in C. kuhlii. Infant-carrying behaviour of fathers occurred at its highest rate 3-4 weeks after parturition and coincided with significant declines in urinary levels of T and E(2), providing preliminary support for the hypothesis that these hormones are antagonistic to paternal behaviour. Urinary T and E(2)declined among fathers regardless of whether their young survived to weaning or died at birth, indicating that variation in these hormones after parturition occurs even in the absence of continued stimuli from infants. When adjusted for declines ordinarily associated with aging, urinary T tended to be lower among fathers with a great deal of prior experience caring for young compared with fathers having little or no experience, suggesting that either experience affects T levels of fathers, or that T levels influence fathers' chances of successfully rearing infants. Overall, our results suggest that in male C. kuhlii, T, and possibly E(2), play an important role in balancing the expression of paternal care with that of other reproductive behaviours. Copyright 2000 The Association for the Study of Animal Behaviour.     

Validation of endogenous controls for gene expression studies in human adipocytes and preadipocytes.

Quantitative gene expression protocols require adequate controls to monitor intersample variation. Quantitative approaches to describe relative changes in gene expression use endogenous controls--"housekeeping" genes. Given the low amounts of mRNA in fat cells, RT-PCR is the method of choice, and housekeeping genes are widely used as endogenous controls. However, literature reports suggest changes in gene expression of typical housekeeping genes (e. g. GAPDH, beta-actin, 18S rRNA) upon hormonal stimulation or during adipogenic differentiation. Thus, we tested the influence of 6 hormones and adipogenic differentiation on gene expression levels of 11 commonly used housekeeping genes in primary cultured mature human adipocytes and preadipocytes. Using the TaqMan RT-PCR technique and "Human Endogenous Control Assays" (PE Biosystems), we found several housekeeping genes with at least twice the difference in expression levels between stimulated and unstimulated cells (such as acidic ribosomal protein, beta-actin, beta(2)-microglobulin and beta-glucuronidase). Only GAPDH and transferrin receptor gene expression levels did not change under any of the stimuli tested, thus appeared best suited for gene expression studies in human adipose cells across a wide range of experimental settings.     

Patterns of paternal care in primates

An interspecific comparison was carried out to understand better the relationships among paternal care, paternal certainty, and reproductive burden in primates. Although monogamy is generally rare among mammals, a number of primate species are monogamous. Extensive paternal care is a related issue but is one that is not necessarily associated with monogamy or with paternal certainty. For example, despite paternal certainty, primate mothers in monogamous species with body weights over 2 kg still remain the primary infant caretakers, while males in the communally breeding tamarins carry infants more frequently than mothers do, even in the absence of paternal certainty. Several different tactics are used by small-bodied primates to cope with the energetic burden of raising proportionately large infants in an arboreal environment: (1) infant carrying by subadult and/or related nulliparous females (Saimiri, Lemur monogoz); (2) infant carrying by fathers and offspring (Aotus, Callicebus, Saguinus, Cebuella, Leontopithecus); (3) parking infants while family members forage (Tarsius, Galago, Microcebus, Cheirogaleus, Varecia); or (4) some combination of the above (Callithrix, Hapalemur, Loris). Lactation length and infant growth patterns appear to influence which of these tactics is employed by a given species. Moreover, although most small-bodied, mated, monogamous female primates spend no more than 9 months annually in gestation and lactation,Aotus andCallicebus mated females are either pregnant or lactating on a year-round basis. It is this heavy female reproductive burden that may be an important factor in selection for extensive paternal care in these monogamous cebids.     

Evolution of female colours in birds: The role of female cost of reproduction and paternal care

Female ornamentation is frequently observed in animal species and is sometimes found as more evolutionary labile than male ornamentation. A complex array of factors may explain its presence and variation. Here we assessed the role of female cost of reproduction and paternal care. Both factors have been pinpointed as important by theoretical studies but have not been investigated yet in details at the interspecific level. We worked on 133 species of North temperate Passeriformes bird species for which both the clutch volume – here taken as the proxy of female cost of reproduction – and amount of paternal care are relatively well known. Using spectrometry, we measured the whole-body coloured plumage patches and quantified three metrics corresponding to brightness (i.e. achromatic component), colour chromaticity (i.e. intensity) and colour volume (i.e. diversity). We found a strong association between male and female colour metrics. Controlling for this association, we found additional small but detectable effects of both cost of reproduction and paternal care. First, females of species with more paternal care were slightly brighter. Second, the interaction between the level of paternal care and egg volume was correlated with female colour intensity: females with more paternal care were more chromatic, with this association mostly present when their investment in reproduction was low. Together these results suggest that female cost of reproduction and paternal care are part of the multiple factors explaining variation of female coloration, besides the strong covariation between male and female coloration.     

X- and Y-chromosome linked paternal effects on a life-history trait

Males and females usually invest asymmetrically in offspring. In species lacking parental care, females influence offspring in many ways, while males only contribute genetic material via their sperm. For this reason, maternal effects have long been considered an important source of phenotypic variation, while paternal effects have been presumed to be absent or negligible. The recent surge of studies showing trans-generational epigenetic effects questions this assumption, and indicates that paternal effects may be far more important than previously appreciated. Here, we test for sex-linked paternal effects in Drosophila melanogaster on a life-history trait, and find substantial support for both X- and Y-linked effects.     

Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation

Male androgen responses to social challenges have been predicted to vary with mating system, male-male aggressiveness, and the degree of paternal investment in birds ("challenge hypothesis," Am. Nat. 136 (1990), 829). This study focused on the interspecific predictions of the challenge hypothesis. Comparative methods were used to control for effects of the phylogenetic relatedness among the sampled species. Male androgen data of 84 bird species were collected from literature records on seasonal androgen patterns. From these, the androgen responsiveness (AR) was calculated as described in the original challenge hypothesis (i.e., maximum physiological level/breeding baseline). Scatterplots of AR versus mating strategy, male-male aggressiveness, and the degree of paternal care confirmed the expected interspecific patterns. When phylogenetic analyses were performed among all of the sampled species, the effects of paternal investment disappeared while the AR remained covarying to a high degree with mating system and male-male aggressiveness. Although these mechanisms may be different at the intraspecific level, this suggests that interspecific differences of AR in male birds may have evolved in response to changes of mating strategies, rather than in response to altered paternal duties. However, control for phylogeny among the subsample of 32 passerine species revealed that if any paternal investment contributed to the observed variance in AR, then the change from "no male incubation" to "male shares incubation duties" represented the most effective, whereas the male's contribution to feeding offspring did not explain the observed variation of AR.     

Thyroid hormones, cytokines, physical training and metabolic control.

During the acute training response, peripheral cellular mechanisms are mainly metabolostatic to achieve energy supply. During prolonged training, glycogen deficiency occurs; this is associated with increased expression of local cytokines, and decreased insulin secretion and beta-adrenergic stimulation and lipolysis in adipose tissue which looses energy. This is indicated by decrease of adipocyte hormone leptin, which has inhibitory effects on excitatory hypothalamic neurons. Leptin, insulin, and cytokines such as interleukin 6 (IL-6) contribute to the metabolic error signal to the hypothalamus which result in decrease of hypothalamic release hormones and sympathoadrenergic stimulation. Thyroid stimulating hormone (TSH) is correlated to the metabolic hormones leptin and insulin, and may be used as indicator of metabolic control. Because the hypothalamus integrates various error signals (metabolic, hormonal, sensory afferents, and central stimuli), the pituitary's releasing hormones represent the functional status of an athlete. Long-term overtraining will lead to downregulation of hypothalamic hormonal and sympathoadrenergic responses, catabolism, and fatigue. These changes contribute to myopathy with predominant expression of slow muscle fiber type and inadequacy in performance. Thyroid hormones are closely involved in the training response and metabolic control.     

Hormones of youth?

Ageing is doubtless complicated, lifelong process regarding many body systems, including endocrine system. Human hormonal system changes with age. Although these changes concern secretion of many hormones, they are not unidirectional, there are hormones secretion of which is diminished, whereas secretion of the others is augmented or not changed with age. A possible role of hormones which are often termed "hormones of youth"(growth hormone, melatonin, and dehydroepiandrosterone) in the ageing process is discussed in the present article. Although some experimental and clinical data indicate that these hormones may play some role in the human ageing process, it appears from presented data that we are still far away from conclusion that, indeed, one (or more) of the discussed hormones could be considered as "hormone of youth", which may slow down ageing process. However, some symptoms of the quality of life improvement following administration of dehydroepiandrosterone, melatonin, and growth hormone may suggest that they may promote so called "successful aging".     

AVPR1b variation and the emergence of adaptive phenotypes in Platyrrhini primates

Platyrrhini (New World monkeys, NWm) are a group of primates characterized by behavioral and reproductive traits that are otherwise uncommon among primates, including social monogamy, direct paternal care, and twin births. As a consequence, the study of Platyrrhine primates is an invaluable tool for the discovery of the genetic repertoire underlying these taxon‐specific traits. Recently, high conservation of vasopressin (AVP) sequence, in contrast with high variability of oxytocin (OXT), has been described in NWm. AVP and OXT functions are possible due to interaction with their receptors: AVPR1a, AVPR1b, AVPR2, and OXTR; and the variability in this system is associated with the traits mentioned above. Understanding the variability in the receptors is thus fundamental to understand the function and evolution of the system as a whole. Here we describe the variability of AVPR1b coding region in 20 NWm species, which is well‐known to influence behavioral traits such as aggression, anxiety, and stress control in placental mammals. Our results indicate that 4% of AVPR1b sites may be under positive selection and a significant number of sites under relaxed selective constraint. Considering the known role of AVPR1b, we suggest that some of the changes described here for the Platyrrhini may be a part of the genetic repertoire connected with the complex network of neuroendocrine mechanisms of AVP–OXT system in the modulation of the HPA axis. Thus, these changes may have promoted the emergence of social behaviors such as direct paternal care in socially monogamous species that are also characterized by small body size and twin births.