Endocrine and neuroendocrine regulation of fathering behavior in birds.

YHBEH-03852; No. of pages: 12; 4C: Hormones and Behavior xxx (2015) xxx–xxx

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Review

Endocrine and neuroendocrine regulation of fathering behavior in birds Sharon E. Lynn ⁎ Department of Biology, The College of Wooster, 931 College Mall, Wooster, OH 44691, USA

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Available online xxxx Keywords: Paternal care Fathering behavior Birds Testosterone Progesterone Prolactin Corticosterone Social cues Neuropeptides

a b s t r a c t 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. © 2015 Elsevier Inc. All rights reserved.

Contents Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Testosterone and fathering behavior: does testosterone mediate a conflict between sexual/territorial and paternal behavior? Circulating testosterone during the parental phase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Testosterone as an inhibitor of paternal behavior: evidence and exceptions. . . . . . . . . . . . . . . . . . . . . Progesterone and fathering behavior: a need for further study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Prolactin and fathering behavior: the “hormone of paternity”? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pioneering work in ring doves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Relationship between prolactin and paternal care across avian species . . . . . . . . . . . . . . . . . . . . . . . A need for direct experimental studies in the wild . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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⁎ Corresponding author. Fax: +1 330 263 2378. E-mail address: [email protected].

http://dx.doi.org/10.1016/j.yhbeh.2015.04.005 0018-506X/© 2015 Elsevier Inc. All rights reserved.

Please cite this article as: Lynn, S.E., Endocrine and neuroendocrine regulation of fathering behavior in birds, Horm. Behav. (2015), http:// dx.doi.org/10.1016/j.yhbeh.2015.04.005

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S.E. Lynn / Hormones and Behavior xxx (2015) xxx–xxx

Corticosterone and fathering behavior: varying contexts, varying mechanisms, varying effects? . . . . . . . . . Baseline corticosterone and paternal care . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stress-induced corticosterone and paternal care . . . . . . . . . . . . . . . . . . . . . . . . . . . . Consideration of corticosteroid binding globulin in studies of stress-induced corticosterone and paternal care Interrelationships of corticosterone, prolactin, and fathering behavior in times of stress . . . . . . . . . . . . . Influence of neuropeptides on fathering behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The vasopressin–oxytocin nonapeptides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Gonadotropin inhibitory hormone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Influence of social cues and social feedback on fathering behavior . . . . . . . . . . . . . . . . . . . . . . . Previous reproductive experience . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Perception of cues from chicks and mates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Indirect manipulation of male care by females . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Proximate mechanisms mediating fathering behavior in birds: areas for further study. . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Introduction Paternal care, or care provided by males that is directed at eggs or young, is more common among birds than any other vertebrate class. Biparental care is exhibited in more than 80% of avian species (Cockburn, 2006; Kendeigh, 1952), and rearing of altricial young (which generally requires significant parental input in the form of warming, protection, and feeding before chicks the nest) occurs in more than 70% of avian species (Silver et al., 1985). Birds are strictly oviparous; thus, with the exception of egg-laying, male birds are generally capable of participating in the same range of parental behaviors as females. Such behaviors include indirect care such as nest building and feeding females during incubation, or more direct care including incubating eggs, assisting with hatching, brooding young, feeding young or escorting them to feeding sites, guarding eggs and chicks, and tidying the nest (Ketterson and Nolan, 1994; Silver et al., 1985; Vleck and Vleck, 2011). The extent to which males contribute to care of eggs and young also varies widely across avian species. Some males provide no care of eggs or young, some share parental care duties with females, and far fewer provide exclusive care of young (reviewed in Cockburn, 2006; Ketterson and Nolan, 1994; Silver et al., 1985). Thus, collectively, birds represent an excellent taxon for not only investigating the evolution of paternal care in vertebrates, but also for investigating proximate mechanisms underpinning diverse aspects of male care of young across a variety of contexts (e.g., Ball, 1991; Ketterson and Nolan, 1994). Existing studies of the endocrine bases of paternal care have focused largely on circulating hormones (especially testosterone and prolactin), with a strong early emphasis on captive males in a laboratory setting (e.g., Buntin, 1996). This work has been instrumental in guiding our investigation of the proximate mechanisms of paternal behavior. As studies of paternal care have been extended to free-living birds, we have begun to develop a clearer understanding of how ecology and life history might shape the relationships between endocrine and neuroendocrine secretions and fathering behavior. Even so, much of what we know is rooted in correlational studies. Thus, despite paternal behavior being so common among birds, surprisingly little is known about the diversity of endocrine and neuroendocrine mechanisms governing fathering behavior in this vertebrate group. Importantly, though male care is widespread in birds, it is not always essential for survival of young—females of many biparental species appear able to compensate for reduced or absent care by males, at least in the short term (e.g., Dunn and Hannon, 1992; Freeman-Gallant, 1998; Gowaty, 1983; Smith et al., 1982; Whillans and Falls, 1990). This suggests that endocrine and neuroendocrine mechanisms of paternal behavior may be shaped by considerably different selective pressures than mechanisms of maternal behavior. Even so, a large number of studies of paternal care have been conducted in biparental species, where shared care of eggs and young includes expression of common

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behaviors by males and females. Thus, one may be tempted to assume that mechanisms governing “parental behavior” in birds are also common between the sexes. However, emerging work indicates that mechanisms of male and female parenting behavior are not always the same (possibly due to sexual dimorphisms in neural substrates, receptor distributions, and circulating hormone profiles). Thus, a need exists for a clearer understanding of how fathering and mothering behavior are differentially regulated in birds, even when behavioral expression seems very similar. Here, I review much of what is currently known about proximate mechanisms of paternal care in birds. Though this review does not provide an exhaustive treatment of the subject, I emphasize specific hormones that vary predictably and/or unpredictably during the parental phase in both captive and wild birds, and that thus are likely candidates for regulating fathering behavior. Some of these hormones (i.e., prolactin and progesterone) are generally assumed to enhance paternal care and others (i.e., testosterone and corticosterone) are commonly—though not always correctly—assumed to inhibit paternal care. I also highlight studies in which investigators have considered the dynamics of multiple hormones simultaneously (e.g., the interrelationships of corticosterone, prolactin, and fathering behavior in times of stress), and summarize key findings that suggest a potential role for specific neuropeptides in promoting paternal care in birds. In particular, I focus on the vasopressin–oxytocin nonapeptides, which are known to promote aspects of parental care in mammals, and gonadotropin inhibitory hormone, which interacts in key ways with hormones known to affect fathering behavior, such as testosterone and corticosterone. In addition, because endocrine secretions are not the sole mechanistic influence on paternal behavior, I touch on how certain experiential factors such as prior experience and feedback from offspring and mates might influence fathering behavior in birds. Throughout this review, I not only distill what is currently known about selected endocrine and neuroendocrine mechanisms governing fathering behavior in birds, but I also highlight areas that are ripe for future study. Testosterone and fathering behavior: does testosterone mediate a conflict between sexual/territorial and paternal behavior? Circulating testosterone during the parental phase Seasonal activation of the hypothalamo-pituitary-gonadal (HPG) axis leads to elevations in testosterone in anticipation of breeding in seasonally breeding birds. In males, this elevation is important for seasonal development of some secondary sex characters, spermatogenesis, sexual behavior, mate attraction and territory defense during breeding (Balthazart, 1983; Wingfield et al., 2000; Wingfield and Farner, 1993). Testosterone is also commonly considered to be a potent inhibitor of paternal care, at least in certain contexts (Ketterson et al., 1992; Lynn, 2008; Wingfield et al., 1990).



This assumption is, in part, tied to the seasonal testosterone profile that is typically exhibited by paternal males: in species in which males show paternal care, testosterone levels are elevated early in the breeding season when males form pair bonds and establish territories, and then decline to a low breeding baseline as nests are initiated (Wingfield and Farner, 1978a, 1978b, 1993; Wingfield and Moore, 1987). Thus, circulating testosterone tends to be low during the parental phase. This pattern of secretion is predicted by Wingfield et al.'s (1990) Challenge Hypothesis, which relates both seasonal and short-term patterns of testosterone secretion to mating system, levels of male–male aggression, and degree of paternal care (see also Hirschenhauser et al., 2003). The Challenge Hypothesis also predicts that certain social cues can result in androgen secretion above the breeding baseline level. Thus, in many avian species in which males exhibit parental care, despite the low baseline testosterone levels that males exhibit during the parental phase, the possibility exists that males may still experience transient elevations in plasma testosterone at this time, for example, in response to territorial challenges by other males or cues from receptive females (Feder et al., 1977; Moore, 1983, 1982; Wingfield et al., 1990). If males remain responsive to these transitory peaks in circulating testosterone during the parental phase, this creates an opportunity for testosterone to influence expression of paternal care in certain social and ecological contexts. Testosterone as an inhibitor of paternal behavior: evidence and exceptions A large number of field studies have employed long-release testosterone implants that elevate normally low testosterone levels in paternal males to investigate (1) whether males remain responsive to elevated testosterone during the parental phase, and if so, (2) how elevated testosterone impacts expression of male behavior at this time. The results of such studies have demonstrated that, across a variety of species, elevated testosterone during the parental phase tends to increase sexual and aggressive behaviors in male birds at the expense of care of young (reviewed in Lynn, 2008). Though the majority of these studies focus on chick provisioning by males, experimentally elevated testosterone has also been shown to inhibit incubation in males that incubate alone (Oring et al., 1989) and males that assist females with incubation of eggs (Alonso-Alvarez, 2001; De Ridder et al., 2000; McDonald et al., 2001; Van Roo, 2004). Further supporting the notion that androgens inhibit paternal care, experimental treatment of parental males with anti-androgens such as flutamide and cyproterone acetate has generally been shown to enhance paternal behavior (Hegner and Wingfield, 1987; Moreno et al., 1999; but see also Van Roo, 2004). These experimental findings, in combination with the typical decline in plasma testosterone that is seen in parental males, have led to general acceptance of the notion that a male's circulating testosterone levels during the parental phase mediate a tradeoff between sexual and/or aggressive and paternal behavior. That is, elevated testosterone is thought to favor sexual and aggressive behavior at the expense of paternal care (Ketterson and Nolan, 1994; Lynn, 2008). However, at least two lines of evidence suggest that this explanation may not be as broadly applicable as is often assumed. First, though the majority of testosterone implant studies suggest that elevated testosterone interferes with expression of paternal care (see above), males of some species do not reduce paternal care in response to high testosterone, a phenomenon that has been referred to as “behavioral insensitivity” to testosterone during the parental phase (Lynn, 2008; Lynn et al., 2002). That males of some species exhibit behavioral insensitivity to the potentially disruptive effects of testosterone on parenting implies that under certain circumstances, males may stand to benefit more from caring for their young than from enhancing sexual and/or territorial behavior, even when testosterone levels are elevated (Hunt et al., 1999; Lynn et al., 2002). Thus, in these species, uninterrupted care of young may be enabled by (1) a decoupling of

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testosterone secretion from social challenges, which could reduce the incidence of transient elevations in testosterone once breeding is underway, and (2) a reduced behavioral sensitivity to any elevations in testosterone that do occur (e.g., in the presence of fertile females) (Goymann et al., 2007; Lynn, 2008; Lynn and Wingfield, 2008). In terms of underlying mechanisms, some evidence suggests that changes in androgen receptor levels and/or rapid changes in expression or activity of the androgen-metabolizing enzyme aromatase in the brain may mediate at least some aspects of changing sensitivity to testosterone during breeding (Foidart et al., 1998; Lea et al., 2001; Pintér et al., 2011; Riters et al., 2001; Silverin et al., 2004; Silverin and Deviche, 1991; Soma et al., 1999). However, mechanisms of behavioral insensitivity to testosterone during the parental phase specifically remain understudied. A second line of evidence supporting a complex relationship of androgens and fathering behavior derives from studies investigating how individual variation in circulating testosterone relates to expression of paternal care. Such studies are few, and have produced mixed results. Many have not demonstrated the expected negative relationship of circulating androgens and care of young predicted by a tradeoff between testosterone and paternal care. For example, naturally occurring variation in plasma testosterone did not predict male provisioning rates in a variety of songbirds (European starling, Sturnus vulgaris, Pinxten et al., 2007; dark-eyed junco, Junco hyemalis, McGlothlin et al., 2007; barn swallow, Hirundo rustica, Eikenaar et al., 2011; northern cardinal, Cardinalis cardinalis, DeVries and Jawor, 2013; black redstart, Phoenicurus ochruros, Villavicencio et al., 2014), and surprisingly, despite an overall decline in testosterone during the parental phase relative to the sexual phase, male tawny owls (Strix aluco) with higher testosterone fed their chicks more frequently than males with lower testosterone, though this effect appeared to be largely mediated by male experience (see below; Sasvari et al., 2009). In addition, studies investigating individual variation in testosterone secretion in response to a gonadotropin-releasing hormone (GnRH) challenge have also produced equivocal results: GnRH-induced testosterone secretion correlated negatively with feeding rates in male dark-eyed juncos (McGlothlin et al., 2007), but not in cardinals or redstarts (DeVries and Jawor, 2013; Villavicencio et al., 2014). Studies of species in which males exhibit discrete morphological and behavioral phenotypes that differ in rates of nestling provisioning have also been valuable in exploring the nuanced relationship of individual variation in testosterone and its influence on paternal care in birds. For example, in red-backed fairy wrens (Malarus melanocephalus), males express three phenotypes that differ in morphology, nestling provisioning behavior, and circulating baseline androgen levels: red/ black-plumaged breeders exhibit low nestling feeding rates and high baseline testosterone levels, brown-plumaged breeders exhibit high nestling feeding rates and intermediate baseline testosterone levels, and brown-plumaged helpers exhibit intermediate nestling feeding rates and low baseline testosterone levels (Barron et al., 2015; Lindsay et al., 2009). Interestingly, however, males of these three phenotypes did not differ in their androgen responsiveness to GnRH challenge, and when males of each phenotype were grouped, neither baseline nor GnRH-induced androgen concentrations were related to nestling provisioning behavior (Barron et al., 2015). Thus, these data demonstrate that even within a species that exhibits marked phenotypic variation in expression of paternal behavior, individual variation in fathering behavior does not relate to individual variation in testosterone secretion. The relationship of individual variation in testosterone to fathering behavior during incubation is also not clear-cut. In European starlings, male testosterone levels correlated negatively with incubation behavior (Pinxten et al., 2007), but male black-tailed gulls (Larus crassirostris) with higher circulating testosterone during incubation were more likely to defend their nests against model predators than males with lower levels (Kazama et al., 2011). Collectively, these data suggest that the assumption that testosterone mediates a trade-off between sexual/


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aggressive and paternal behavior is not universally applicable among birds. Because individual variation is the substrate upon which natural selection acts, a clear need exists for more systematic exploration of such variation in the context of androgens and fathering behavior in birds (see also Williams, 2008; Cockrem, 2013 for excellent discussions of the importance of considering individual variation in endocrine measures). Ultimately, emerging studies suggest that the interrelationship of testosterone and fathering behavior in birds may be considerably more complex than is often assumed. This area deserves further study, with a particular focus on the importance of both ecological and evolutionary history of avian species, the neural underpinnings of behavioral effects, and additional attention to individual variation in both circulating androgens and androgen responsiveness to social and GnRH challenge. Furthermore, though studies have examined the relationship of testosterone with a variety of fathering behaviors in males, including incubation, nestling provisioning, and nest defense (see above), the vast majority of work in this area has focused on provisioning behavior in songbirds. Given the broad array of fathering behaviors males exhibit across a variety of avian taxa, a clear need exists for expanding research on testosterone and paternal care, both taxonomically and behaviorally. Progesterone and fathering behavior: a need for further study Progesterone is generally considered to be a reproductive hormone, though it tends to be studied more in females than in males. In birds, throughout the breeding cycle, progesterone circulates at generally lower levels in males than in females. Some studies clearly indicate that progesterone is a key mediator of paternal behavior in birds. For example, in ring doves, treatment of breeding pairs with progesterone has extremely rapid effects on onset of incubation by males—even more rapid effects than prolactin treatment—but these effects of progesterone were only seen in doves that had prior experience with nesting activity (Buntin, 2010; Lehrman and Wortis, 1960; Michel, 1977; Michel and Moore, 1985). Furthermore, during the ring dove brooding period, when circulating levels of prolactin are generally low, central synthesis of progesterone (and associated steroids including pregnenolone and pregnenolone sulfate) appears to be involved in expression of brooding behavior by males (Lea et al., 2001). Progesterone's role in expression of paternal care across avian taxa, however, has not been extensively studied. Among free-living birds, progesterone has received relatively little attention with regard to promoting or otherwise influencing paternal behavior. A recent correlational study demonstrates a seasonal peak in circulating progesterone in male black kites (Milvus migrans) during the post-brooding period—a period in which males provide significant care of fledglings (Blas et al., 2010). Though this temporal overlap of elevated progesterone and elevated paternal care may tempt one to assume that elevated circulating progesterone may be in some way associated with expression of male care in kites, studies of progesterone dynamics in other species suggest that male progesterone profiles during breeding appear to relate more to pairing status than to paternal care (graylag geese, Anser anser; Hirschenhauser et al., 1999). Ultimately, studies that employ experimental manipulation of progesterone action in a physiologically and ecologically relevant manner across a broad range of taxa are needed to more fully explore how, if at all, progesterone affects avian fathering behavior. Prolactin and fathering behavior: the “hormone of paternity”? Prolactin, a protein hormone secreted by the anterior pituitary, affects myriad aspects of physiology in vertebrates. It is also well known for influencing parental care across vertebrate taxa (e.g., Buntin, 1996; Schradin and Anzenberger, 1999; Ziegler, 2000). Prolactin's influence on maternal behavior has been extensively studied; however, a broad array of correlational and experimental studies across taxa also strongly implicates prolactin in expression of fathering behavior (Bridges et al., 1990; Buntin, 1996; Goldsmith, 1991; Larsen and

Grattan, 2012; Schradin and Anzenberger, 1999; Vleck and Vleck, 2011; Ziegler, 2000). In fact, prolactin has been suggested to be the “hormone of paternity” in fish, birds and mammals (Schradin and Anzenberger, 1999). In birds specifically, prolactin has been shown to exhibit some relationship with paternal care in 25 avian species, ranging across 9 orders (reviewed in Schradin and Anzenberger, 1999), with elevations in this hormone most commonly associated with the transition from sexual to paternal activity (Sharp et al., 1998). Pioneering work in ring doves Much experimental work focusing on prolactin's role in mediating paternal behavior has been conducted in ring doves, and this work has been reviewed extensively elsewhere (Buntin, 1996). In general, elevated prolactin does not appear necessary for the onset of incubation behavior in ring doves, but does appear to be important for maintenance of incubation. Prolactin is clearly also important in promoting male feeding behavior, as peripheral and central prolactin injections increased feeding of foster young in males and females compared with control treatment (Buntin, 1996). Though much excellent work on ring doves has provided a solid basis for understanding prolactin's influences on fathering behavior, columbiform birds such as doves are unusual in that they feed their young with crop milk, a form of food whose production requires elevated prolactin. Thus, understanding whether the interrelationship of prolactin and paternal behavior in ring doves belies a more common pattern among birds requires studies of other, non-columbiform species as well. Relationship between prolactin and paternal care across avian species Since the early ring dove work mentioned above, studies in noncolumbiforms have also revealed a broad association of prolactin with fathering behavior. Most commonly, circulating prolactin tends to peak in males during the period of incubation, followed by either a sustained elevation during the brooding period or a gradual decline after hatching (reviewed in Schradin and Anzenberger, 1999). In some species, pre-breeding prolactin levels have been shown to correlate positively with the number of fledglings produced (e.g., Ouyang et al., 2011). Thus, temporal elevations in prolactin tend to precede or coincide with parental behavior in male birds, suggesting that this hormone plays an important role in facilitation of paternal behavior broadly within the class Aves. Interestingly, findings in cooperatively breeding birds demonstrate that prolactin levels are elevated on a similar timeframe in alloparental “helpers” as they are in parental birds in some species (Khan et al., 2001; Schoech et al., 1996) and may in fact be higher than those of parental birds at stages when helpers provide more care of young than parents (Vleck et al., 1991). These findings further suggest strong selection for elevated prolactin coincident with the presence of eggs and young in need of care. Does the extent to which males participate in parental care relate to prolactin profiles during breeding? Such a relationship does appear to be borne out to some degree, especially when males participate in incubation. For example, in species in which males incubate the eggs and care for the young predominantly or exclusively, male prolactin titers exceed those of their mates (e.g., Wilson's phalarope, Phalaropus tricolor, Oring et al., 1988; red-necked phalarope, Phalaropus lobatus, Gratto-Trevor et al., 1990; spotted sandpiper, Actitus macularius, Oring et al., 1986). In addition, in the socially monogamous blue-headed vireo (Vireo solitarius), a species in which males share incubation duties with females, plasma prolactin levels were higher at all stages of breeding than they were in congeneric red-eyed vireo (Vireo olivaceus), a species in which males do not incubate eggs (Van Roo, 2003). Although incubation is commonly associated with high circulating levels of prolactin, however, the relationship between prolactin and incubation is not always straightforward. For example, prolactin levels were elevated in male red-eyed vireos during incubation relative to



other stages of breeding, despite males not participating in incubation duties (Van Roo, 2003). This pattern of elevated prolactin titers in fathers prior to the hatching of eggs, even when males do not participate in incubation, has been described in other biparental passerines as well (e.g., Campbell et al., 1981; Dawson and Goldsmith, 1982; Goldsmith, 1982; Hiatt et al., 1987; Schoech et al., 1996; Silverin and Goldsmith, 1983; Wingfield and Goldsmith, 1990). Existing data support at least two possible explanations for why prolactin would be elevated prior to hatching of eggs in species in which males do not contribute to incubation. One is that prolactin plays a preparatory role in priming males for care of young, and that it later facilitates expression of paternal care in the presence of young (e.g., see Dawson and Goldsmith, 1982; Silverin and Goldsmith, 1983). Another is that prolactin is not heavily involved in paternal behavior, but is important for other aspects of physiology associated with breeding. This second explanation is borne out by findings that in some species, seasonal rises in prolactin secretion appear to be photoperiodically driven (e.g., European starlings, Dawson and Goldsmith, 1983; White-crowned sparrow, Zonotrichia leucophrys, Hiatt et al., 1987; song sparrow, Melospiza melodia, Wingfield and Goldsmith, 1990), and can occur even in species that show no paternal care whatsoever (e.g., Brown-headed cowbird, Molothrus ater, Dufty et al., 1987). This seasonal pattern of prolactin secretion may be associated not with reproductive development or parental care, but rather with the onset of photorefractoriness (Dawson and Goldsmith, 1983; Dufty et al., 1987; Goldsmith and Nicholls, 1984). Changes in central nervous system sensitivity to hormones, rather than changes in the profile of circulating hormones themselves, may also explain why strictly non-paternal birds such as cowbirds still exhibit high prolactin titers during breeding. The preoptic area (POA) of the hypothalamus is known to be the central site mediating the onset of parental care in mammals and birds (e.g., Buntin, 1996; Buntin et al., 2006; Slawski and Buntin, 1995). Differences in sensitivity of the POA to prolactin have been hypothesized to underlie the lack of association with prolactin and paternal behavior in cowbirds (Dufty et al., 1987), with cowbirds showing quantitatively lower levels of prolactin binding than parental species at this site (Ball, 1991). Whether such differences in tissue sensitivity exist across species showing a diversity of paternal care strategies, however, is poorly understood. Thus, in some species, such as brown-headed cowbirds, plasma prolactin titers appear to be regulated on a seasonal cycle and divorced from expression of any aspect of paternal care. However, in others, prolactin levels can be regulated on a seasonal cycle (i.e., with the onset of secretion being independent of cues from eggs and/or chicks), yet still be important for expression of paternal care. For example, in penguins (in which males and females alternate bouts of incubating a single egg over an extended period of time,) prolactin secretion appears to be endogenously timed, allowing prolactin to be elevated in both sexes throughout the entire period of parental care, including when individuals are away from the egg/chick for extended periods (Garcia et al., 1996; Lormée et al., 2000; Vleck et al., 2000). Despite this, disrupted prolactin secretion has been reported in response to nest desertion relating to naturally depleted energy stores, suggesting that secretion is also responsive to some extent to changing environmental and/or physiological cues (Cherel et al., 1994; Groscolas et al., 2008). A growing body of research has demonstrated that prolactin secretion is indeed responsive to changing cues, especially in the face of unpredictability. That is, during times of both acute and chronic stress, prolactin secretion is often reduced, in concert with elevations in the main avian glucocorticoid, corticosterone. Such hormonal changes are generally disruptive to parental care, which is thought to promote adult survival in the face of adversity in certain contexts. The interrelationships of parental behavior, stress, and prolactin have been reviewed elsewhere (e.g., Angelier and Chastel, 2009; Storey et al., 2006), and are discussed in relation to fathering behavior specifically later in this review.

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A need for direct experimental studies in the wild Collectively, studies of prolactin and paternal care in birds suggest a relatively broad association of this hormone with expression of fathering behavior (including incubation, brooding, and feeding of young) across a variety of species. Correlational work has done much to enhance our understanding of the interrelationship of prolactin and paternal care, but direct experimental studies are comparatively lacking, perhaps owing to the relative difficulty of manipulating prolactin, especially in free-living birds (e.g., manipulating prolactin requires use of osmotic pumps, repeated injection, or indirect manipulation by use of pharmacological agents). The few experimental studies that have been conducted suggest that prolactin does play a direct role in expression of paternal behavior in freeliving birds. For example, experimental decrease of prolactin secretion in male Adélie penguins (Pygoscelis adeliae) modified their incubation behavior such that hatching success was reduced compared to that of unmanipulated penguins (Thierry et al., 2013). An experimental study of free-living house finches (Haemorhous mexicanus) also suggests a direct role of prolactin in feeding behavior by males (Badyaev and Duckworth, 2005). In this species, male plumage coloration is associated with both paternal provisioning behavior and prolactin levels: bright red males normally do not provision young at high rates and have low prolactin levels during nestling feeding, whereas dull males provision at higher rates and have higher prolactin levels (Duckworth et al., 2003). Treatment of bright males with vasoactive intestinal polypeptide (VIP, the primary stimulator of prolactin release) resulted in a significant increase in nestling provisioning, whereas blocking prolactin release with bromocriptine treatment decreased provisioning by males with duller plumage (Badyaev and Duckworth, 2005). These experimental findings are noteworthy, because although an abundance of studies demonstrate a clear correlation between prolactin secretion and paternal provisioning (Buntin, 2010; Buntin et al., 2006), fully parsing whether prolactin promotes provisioning behavior, or whether provisioning behavior promotes or sustains prolactin secretion is not possible without such experimental manipulations. Corticosterone and fathering behavior: varying contexts, varying mechanisms, varying effects? Thus far, I have focused on the relationship of paternal care and circulating hormones that fluctuate in a predictable manner during the parental phase. However, free-living animals are often faced with unpredictable environmental stimuli during breeding, producing changes in endocrine and neuroendocrine secretions that can in turn influence parental behavior (Wingfield et al., 1998). For example, activation of the hypothalamo-pituitary-adrenal (HPA) axis produces elevations in circulating corticosterone (a steroid hormone secreted by the adrenal cortex, and the primary glucocorticoid in birds), which broadly regulates physiology and behavior associated with energy intake and expenditure under both predictable and unpredictable circumstances (McEwen and Wingfield, 2003). Among the well-known changes in behavior orchestrated by stressinduced secretion of corticosterone in birds is disruption of both paternal and maternal behavior, often with the consequence of complete abandonment of the nest and young if glucocorticoid elevations are sustained (Wingfield et al., 1998). However, some studies show that moderate elevations in corticosterone actually enhance expression of paternal behavior (see below). How can these differences be reconciled? Baseline corticosterone levels are associated with maintenance of allostasis when energy demands are predictable, and act primarily through activation of type I mineralocorticoid receptors (MR) (McEwen and Wingfield, 2003; Romero, 2004). Corticosterone is also a wellknown mediator of stress physiology in the face of unpredictable circumstances, and its actions at stress-induced levels are primarily mediated through binding of type II glucocorticoid receptors (GR). Because activation of MR and GR have different consequences for physiology and


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behavior (Romero, 2004), baseline and stress-induced concentrations of corticosterone would be expected to exert different effects on paternal behavior. Below I explore the relationship of fathering behavior to both baseline and stress-induced corticosterone levels in turn. Baseline corticosterone and paternal care Bonier et al. (2009a) have proposed that a positive relationship of baseline corticosterone and fitness should exist when elevations in baseline corticosterone promote allocation of resources to reproduction (i.e., the “cort-adaptation hypothesis”). Thus, this hypothesis predicts that moderate elevations in baseline corticosterone should enhance paternal behavior. Such a relationship has been demonstrated in female passerines and seabirds, at least in relation to chick provisioning (e.g., Bonier et al., 2011, 2009a, 2009b; Crossin et al., 2012), suggesting that elevated corticosterone is important for allowing females to meet the increased demands of chick rearing. Whether such a relationship between moderate elevations in baseline corticosterone and male provisioning, however, is unclear, as far less is known of the relationship between elevations in baseline corticosterone and paternal behavior. In some species, males have been reported to exhibit higher baseline levels of corticosterone than females during certain substages of the parental phase in which males play a greater role in parenting than females (Logan and Wingfield, 1995; Riechert et al., 2014), and baseline corticosterone in breeding males has been shown to correlate positively with the number of fledglings produced (Ouyang et al., 2011). However, in these studies, no data were provided regarding how these elevated levels related (if at all) to specific aspects of paternal care. Studies that have directly examined natural variation in baseline corticosterone and paternal provisioning have provided equivocal results—in some species, a male's baseline corticosterone levels appear to correlate positively with chick provisioning under non-stressful conditions (e.g.,. mourning doves, Zenaida macroura, Miller et al., 2009; common murres, Uria aalge, Doody et al., 2008), but in others such a relationship was not apparent (e.g., house sparrows, Passer domesticus, Lendvai and Chastel, 2010; eastern bluebirds, Sialia sialis, Davis and Guinan, 2014; black redstarts, Villavicencio et al., 2014). Experimental studies investigating the relationship of elevated baseline corticosterone and fathering behavior are scarce. Silverin (1990) reported that biparental pied flycatchers (Ficedula hypoleuca) with experimentally enlarged broods exhibited slightly elevated baseline corticosterone as well as increased chick provisioning rates; however, a direct relationship between corticosterone levels and parental provisioning was not investigated. In fact, studies that have attempted to examine the effects of altering baseline corticosterone levels directly (i.e., without introducing other potentially confounding factors such as changes in brood size) on expression of paternal care are extremely uncommon. A recent study of great tits revealed that extended elevation of circulating corticosterone within a physiologically relevant baseline range increased the rates at which males fed their mates during incubation (Ouyang et al., 2013). Though this study did not investigate the effects of elevated baseline corticosterone during chick-rearing, when males would be caring for young directly, this effect of corticosterone on male behavior is consistent with the predictions of the cort-fitness hypothesis (Bonier et al., 2009a). In polymorphic whitethroated sparrows (Zonotrichia albicollis), a species in which paternal provisioning differs with male morphology (tan-striped males tend to provision young at higher rates than white-striped males), elevated corticosterone in tan-striped males decreased provisioning behavior, whereas administration of the GR blocker RU486 led to an increase in provisioning behavior in white-striped males (Horton and Holberton, 2009). However, despite the absolute hormone levels achieved in this study being below concentrations achieved by capture and handling, these data clearly point to GR activation as a mediator of corticosterone's actions on paternal behavior. Thus whether these manipulations were in

fact within the range of naturally occurring variation in baseline corticosterone is unclear. Overall, few studies have focused on the relationship between baseline corticosterone and parental behavior in birds, with only a handful of studies investigating this association in relation to male care directly. This is likely due, at least in part, to the difficulty of manipulating baseline corticosterone experimentally. However, because variation in baseline corticosterone is a likely target of natural selection (e.g., Ouyang et al., 2011), a strong need for such studies exists. Stress-induced corticosterone and paternal care The effects of stress-induced elevations of corticosterone on reproductive behavior, including paternal care, in birds have been well studied (Wingfield et al., 1998). Early work in free-living songbirds demonstrated that experimentally elevated corticosterone (achieved via subcutaneous implants) substantially disrupted paternal behavior in biparental songbirds (e.g., Silverin, 1990, 1986), though the physiological relevance of corticosterone elevations achieved by subcutaneous implants has recently been called into question (e.g., Bonier et al., 2009a). Surprisingly few studies have focused on the relationship of natural variation in corticosterone responses to stress and subsequent expression of paternal care in free-living birds, though existing studies support the idea that stress-induced elevations in corticosterone tend to correspond with reductions in paternal care. For example, corticosterone secretion by individual male house sparrows and mourning doves exposed to a standardized period of capture and restraint was negatively related to their chick provisioning behavior (Lendvai and Chastel, 2010; Miller et al., 2009; Ouyang et al., 2011). Recent work also suggests that the individual differences in HPA responses to more natural, unpredictably changing environmental conditions also relate to expression of paternal care: stress-induced corticosterone levels in male Great tits (Parus major) were a strong predictor of nest desertion under harsh environmental conditions (i.e., high rainfall, low ambient temperature, and diminished food availability; Ouyang et al., 2012). In addition, when environmental conditions were poor, stress-induced corticosterone levels in male great tits were negatively related to the likelihood of renesting, such that breeding pairs in which males had lower corticosterone were more likely to initiate a renesting attempt than those in which males had higher corticosterone (Ouyang et al., 2012). Collectively, the results of corticosterone implant studies and studies focusing on natural variation in individual males' corticosterone secretion in response to stressful stimuli point to a reciprocal relationship of stressinduced elevations of circulating corticosterone and expression of paternal care. The well-known disruptive actions of elevated glucocorticoids during periods of stress on aspects of reproduction and parenting have led to the hypothesis that an individual's response to acute stress reflects a trade-off between current and future reproduction. That is, an individual can respond to a stressor by either (1) increasing corticosterone secretion, thus activating emergency behavior including reducing care of young or abandoning the current reproductive effort, or (2) suppressing corticosterone secretion and attempting to continue the current reproductive effort at considerable personal risk (Wingfield et al., 1998). Thus, down regulation of corticosterone responsiveness to stressors is expected to reflect high investment in parental care (O'Reilly and Wingfield, 2001; Wingfield et al., 1995). In support of this hypothesis, research in birds suggests that corticosterone secretion in response to a stressor may be suppressed in the sex that provides most of the parental care. That is, experimental studies have reported greater down regulation of the corticosterone response to stress in males when paternal care is more common than maternal care, the reverse pattern when maternal care is more common, and equivalent corticosterone responses between the sexes when care is shared equally (Lynn et al., 2003; O'Reilly and Wingfield, 2001; Wingfield et al., 1995). These findings were to some



degree supported by a phylogenetic comparative analysis of corticosterone responsiveness to stress and parental care: Bókony et al. (2009) found that when parental care was female-biased, female corticosterone responses were lower; however, intriguingly, the opposite was true when care was male-biased. Corticosterone secretion in response to stress (controlled for baseline) was actually higher in species in which males provided more care than females (Bókony et al., 2009). This analysis suggests that, though a trade-off between stress-induced corticosterone and parenting apparently exists in birds, that tradeoff may be more applicable in the context of maternal care than paternal care, and raises interesting questions about the selective pressures shaping mechanisms of parental care between the sexes. Future experimental work in this area is warranted, and careful selection of species within a phylogenetic framework may be especially informative. Consideration of corticosteroid binding globulin in studies of stress-induced corticosterone and paternal care Investigations of avian glucocorticoid secretion during periods of stress may also be informed by consideration of corticosteroid binding globulin (CBG) levels (Breuner et al., 2013, but see also Schoech et al., 2013). CBG is a binding protein that binds corticosterone with high affinity in circulation. Plasma CBG may regulate not only the biological activity of corticosterone, but also the metabolic clearance rate, tissuespecific delivery to target cells, and/or binding of the corticosterone– CBG complex to binding globulin receptors on target cell membranes (reviewed in Breuner et al., 2013; Malisch and Breuner, 2010). CBG has also been shown to be a dynamic component of avian physiology: CBG binding capacity differs across breeding substages in some birds (e.g., Shultz and Kitaysky, 2008; Silverin, 1986), and it can also vary in response to acute and prolonged stressors in a subset of species (reviewed in Malisch and Breuner, 2010). Thus, it is possible that predictable or unpredictable changes in CBG might also play a role in modulation of the effects of stress-induced corticosterone secretion during the parental phase in male birds. Direct studies of CBG dynamics (and hence dynamics of the free vs. bound fractions of corticosterone) and fathering behavior in birds are completely lacking, however, and this remains an interesting area for future study. Interrelationships of corticosterone, prolactin, and fathering behavior in times of stress In recent years, a trade-off between stress-induced hormone secretion and parenting, like that proposed for corticosterone, has also been suggested for prolactin secretion during times of stress. However, whereas corticosterone levels tend to increase in response to noxious stimuli or energetic constraints (see above), prolactin levels in breeding birds tend to decrease (Angelier and Chastel, 2009; Chastel et al., 2005; Delehanty et al., 1997; Groscolas et al., 2008; Krause et al., 2015; Riou et al., 2010; Schmid et al., 2011). Given the strong associations of prolactin and paternal care (see above), this decrease in prolactin during periods of stress that coincide with breeding (often called the “prolactin response to stress”) is thought to at least partially underlie the disruptive effects of stressors on parental care (Angelier and Chastel, 2009; Chastel et al., 2005). In addition, the magnitude of an individual's prolactin response to stress (i.e., the extent to which prolactin levels are dampened) is thought to reflect that individual's level of parental investment (reviewed in Angelier and Chastel, 2009). Notably, studies of parental behavior and the prolactin response to stress have focused almost exclusively on species with biparental care, and thus have focused on the relationship of stress and prolactin on parental care collectively exhibited by males and females. At least one study, however, has demonstrated a differential prolactin response to stress between the sexes that may reflect differential parental investment between the sexes as chicks age (Schmid et al., 2011).

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Current data suggest that concomitant changes in circulating corticosterone and prolactin during times of acute stress likely mediate different aspects of the acute stress response (corticosterone mediating changes associated with energy balance, and prolactin mediating changes associated with parental effort; reviewed in Angelier and Chastel, 2009). However, when corticosterone levels are elevated in a prolonged manner, or when energetic constraints are sustained, changes in circulating prolactin and corticosterone are thought to be linked both mechanistically and functionally. For example, corticosterone implants that elevated circulating corticosterone for a 2-day period in biparental black-legged kittiwakes (Rissa tridactyla) resulted in a gradual but prolonged depression of circulating prolactin (a 30% decrease from baseline) that was accompanied by a decrease in parental activity by both sexes and, ultimately, a reduction in breeding success. Interestingly, these behavioral effects persisted well beyond the period in which corticosterone was actually elevated, but corresponded with the decline in circulating prolactin (Angelier et al., 2009). In addition to experimental manipulations such as this one, sustained unfavorable environmental conditions leading to egg and chick abandonment were also linked with elevated corticosterone and dampened prolactin secretion in male king penguins (Aptenodytes patagonicus, Groscolas et al., 2008). Whether the reduction in prolactin and associated parental behaviors seen in these studies occurred via direct actions of elevated corticosterone on prolactin secretion, or whether it resulted from corticosterone's effects to reduce behaviors which normally stimulate prolactin secretion (such as nest attendance) is not fully clear. Future work aimed at identifying the mechanistic links between prolactin and corticosterone during periods of stress in relation to parenting in birds is warranted. Furthermore, with some exceptions (Krause et al., 2015; Schmid et al., 2011), the majority of work focusing on both corticosterone and prolactin responses to stress in relation to care of young by males has been conducted in seabirds (reviewed in Angelier and Chastel, 2009). Considerable work is still needed to determine whether the interrelationships of prolactin, corticosterone, and parental behavior that have been described in seabirds are broadly applicable across a broad taxonomic range of avian species, and whether these interrelationships differ in meaningful ways between the sexes. Influence of neuropeptides on fathering behavior Though the vast majority of work on mechanisms of paternal care in birds has focused on circulating hormones, comprehensive study of the neuroendocrine control of fathering behavior in birds also requires a more systematic look at neuropeptide function and neural mechanisms of behavior. Here I focus on a potential role for two classes of neuropeptides to affect paternal behavior in birds—the vasopressin–oxytocin nonapeptides and gonadotropin inhibitory hormone. Though, clearly, a broad suite of neuropeptides may affect parental care in birds, I highlight these two classes here because emerging work raises intriguing questions about their involvement in fathering behavior specifically. The vasopressin–oxytocin nonapeptides The vertebrate nonapeptides are an ancient and strongly conserved family of peptides derived from arginine vasotocin (VT). The wellknown mammalian peptides vasopressin and oxytocin, as well as the homologues vasotocin and mesotocin, which are found in birds and many other vertebrates, partially comprise this family of peptides, which is often referred to as the “vasopressin–oxytocin nonapeptides” (reviewed in Goodson, 2013). Among vertebrates, the nonapeptide system plays important roles in nonsocial and physiological functions, but nonapeptide circuits and functions also have strong associations with bonding and affiliative behavior across a variety of taxa (Goodson, 2013; Kelly and Goodson, 2014). For example, the vasopressin–oxytocin nonapeptides are important mediators of parental behavior in mammals, though the relationship is


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more clear-cut for females than it is for males (Bosch and Neumann, 2008; Saltzman and Ziegler, 2014). Nonetheless, this presents the possibility that these neuroendocrine secretions may also play such a role in birds. Among birds studied to date (as in other tetrapod vertebrates), a male-biased dimorphism exists in the vasotocin circuitry in the brain (specifically the medial bed nucleus of the stria terminalis; Goodson, 2013; Kelly and Goodson, 2014). In addition, the circuit diminishes during non-breeding periods in seasonally breeding birds (De Vries and Panzica, 2006; Goodson and Bass, 2001). The evolution of the sexual dimorphism (and seasonal expression) of this circuit has been hypothesized to have been favored due to the circuit's role in reducing male aggression during the breeding season, particularly in contexts in which heightened affiliative behavior would be beneficial (such as interactions with potential mates and/or young; Goodson, 2013). Thus, the possibility exists that the vasopressin–oxytocin peptide system functions a mediator of paternal care in males. Importantly, the vasopressin–oxytocin peptides are to some extent promiscuous—for example, the V1a receptor (V1aR) and the OT receptor (OTR) mediate the effects of both vasopressin and oxytocin in mammals. Evidence suggests that avian nonapeptide receptors are similarly promiscuous with regard to vasotocin and mesotocin binding (which is perhaps unsurprising, given the highly conserved nature of peptides in this family; Klatt and Goodson, 2013; Leung et al., 2009). A recent study used OTR and V1aR antagonists to explore whether the avian forms of oxytocin and vasopressin (mesotocin and vasotocin) play a role in nest building behavior in zebra finches, a species in which both males and females normally contribute to construction of the nest (Klatt and Goodson, 2013). Whereas peripheral treatment with an OTR antagonist reduced female nesting behavior, it had no such effect on male nesting behavior. However, peripheral treatment with a V1aR antagonist significantly reduced nesting behavior in both sexes. Central treatment with the same antagonist had no such effect. Thus, these data clearly implicate peripheral V1a receptors (but surprisingly, not central ones) to at least some degree in mediation of nesting behavior in males. Such peripheral effects on nesting behavior are thought to manifest indirectly via influences of the vasopressin–oxytocin peptides on other functions associated with homeostasis (e.g., such as thermoregulation, see Klatt and Goodson, 2013). Gonadotropin inhibitory hormone The hypothalamic neuropeptide gonadotropin inhibitory hormone (GnIH), which appears to be a key player in the fine-tuning of reproductive timing, may also play a role in mediating transitions to the parental phase in birds. Hypothalamic GnIH can oppose gonadotropin synthesis and release in birds and mammals (Bentley et al., 2006; Johnson et al., 2007; Kriegsfeld et al., 2006; Osugi et al., 2004; Sari et al., 2009; Ubuka et al., 2006), and may also regulate gonadotropin releasing hormone directly (Tsutsui et al., 2012). In addition, gonadally produced GnIH may exert local control of gonadal function. Both hypothalamic and gonadal GnIH also appear to be enhanced by glucocorticoid elevation (Calisi et al., 2008; Davies and Deviche, 2014; McGuire et al., 2013; Lynn et al. 2015). Thus, via these interactions with both the HPG and HPA axes, the GnIH system has the potential to influence endocrine secretions relevant to paternal behavior. Furthermore, recent work in European starlings demonstrated that hypothalamic GnIH peptide expression changed both with the onset of paternal care and with simulated nest failure during incubation (Calisi et al., 2013), potentially implicating this neuropeptide in mediating transitions between sexual and paternal behavior. Influence of social cues and social feedback on fathering behavior Thus far, I have focused this review on the interrelationships of endocrine and neuroendocrine secretions and care of eggs and young by males. However, experiential and social factors may have strong

influences on paternal care that can either interact with or potentially override a male's neuroendocrine status in relation to expression of paternal care, and thus these deserve at least brief mention here. Though a variety of social and experiential factors are likely to be important in influencing expression of fathering behavior in males, here I focus on three such factors: previous reproductive (and hence paternal) experience, perception of cues from chicks and mates, and indirect manipulation of paternal care by females. Previous reproductive experience Previous parental experience is known to play a large role in expression of maternal care across taxa, and also appears to be an important influence on paternal behavior in birds. Such influences may override or complement the influences of circulating hormones on male behavior. For example, in the common tern, previous parental experience did not influence feeding rates by males and females, but it did increase the energetic content of prey items brought to chicks, which was a positive predictor of breeding success (Limmer and Becker, 2009). Likewise, provisioning of chicks and mates by male Florida scrub jays (Aphelocoma coerulescens) and the probability of fledging a successful chick in snow petrels (Pagadroma nivea) have been shown to increase with paternal age, suggesting that experience may also be an important mediator of paternal care (Angelier et al., 2007; Wilcoxen et al., 2010). The effects of prior reproductive and paternal experience may also interact in important ways with endocrine mediators of paternal care. For example, in a study of testosterone levels, reproductive performance, and paternal care in tawny owls, breeding experience was positively related to plasma testosterone, territory quality, and mate fidelity (Sasvari et al., 2009). Taken together, these data suggest that studies focused on endocrine and neuroendocrine mediation of paternal behavior would also benefit from considering the potential modulatory impacts of male breeding experience on male care of eggs and young. Perception of cues from chicks and mates Regardless of a male's prior breeding experience, cues from the chicks themselves appear critical in some species for matching paternal care with chick demands in a fluctuating environment. Captive studies of ring doves demonstrate the importance of cues from chicks in stimulating appropriate levels of paternal care. For example, deafened males (that were hence unable to hear the begging calls of their chicks) paired with deafened females significantly reduced chick provisioning behavior and abandoned chicks too early to ensure chick survival (Nottebohm and Nottebohm, 1971). In free-living house wrens (Troglodytes aedon, a species in which males don't incubate eggs but do feed the young) visual/tactile contact with chicks appears necessary for males to begin feeding chicks after hatching (Johnson et al., 2008). Few studies have directly explored how exposure to chicks interacts with neuroendocrine mediators of paternal behavior. However, in parental male and female ring doves, fos immunoreactivity in the POA and lateral hypothalamus was greater in parents exposed to their chicks than in parents that were deprived of chicks for a 16–18 h period. In addition, the amount of fos immunoreactivity in the POA varied depending on whether parents were allowed direct physical contact with their young after a similar separation, or whether they were only allowed exposure to chicks across a mesh partition (Buntin et al., 2006). Thus, particular cues associated with chicks appeared to differentially stimulate a cascade of gene expression important for triggering parental behavior. In free-living birds, begging by chicks has been shown to be a sensitive indicator of chick physiological state that may reflect environmental conditions. For example, in black-legged kittiwakes (R. tridactyla), artificially elevated corticosterone levels in chicks, mimicking those secreted during years of poor food availability, stimulated an increase in chick begging, and a concomitant increase in chick provisioning rates by both parents (Kitaysky et al., 2001). Interestingly, experimental



elevation of corticosterone in the parents themselves had no effect on chick provisioning (Kitaysky et al., 2001). Relatedly, in eastern bluebirds, though male provisioning of young was unrelated to male baseline corticosterone levels (see above), it was positively related to baseline corticosterone levels of their mates and their chicks (Davis and Guinan, 2014). Taken together, these studies suggest that, at least in some species, a male's expression of paternal behavior may be influenced more heavily by the physiological state of members of his family unit than by his own physiological state. Thus, taking these social influences into account when investigating interactions of hormones and fathering behavior may be essential for understanding the complex underpinnings of male behavior during the parental phase. Indirect manipulation of male care by females Sexual conflict promotes manipulation of breeding partners into increasing parental investment (Chapman et al., 2003; Houston et al., 2005; Lessells, 2006; Parker et al., 2002), and such manipulation may occur through a variety of mechanisms. Variation in the maternal allocation of hormones to egg yolk has been hypothesized to be a physiological mechanism by which females might indirectly manipulate male care. That is, because differential allocation of hormones to yolk can influence chick growth rates and begging behavior, females may capitalize on male responsiveness to signals produced by chicks (Groothuis et al., 2005; Moreno-Rueda, 2007; Müller et al., 2007). Few studies, however, have directly tested this intriguing hypothesis. For example, maternal deposition of androgens into yolk was associated with specific components of chick begging that had a strong influence on male provisioning behavior in yellow-legged gulls (Larus michaellis). Paternal feeding rate was also strongly associated with nestling body mass in this study, suggesting that paternal investment in chick provisioning accelerated chick development (Noguera et al., 2013). A study that experimentally manipulated yolk androgens and investigated subsequent male provisioning behavior in great tits, however, did not find such an association (Tschirren and Richner, 2008). Future work, both correlational and experimental, that is aimed at untangling how maternal physiology at the time of egg laying interacts with expression of male care in species with different ecological (and phylogenetic) constraints would be of considerable interest. Such work would be of value not only for identifying potential mechanisms mediating sexual conflict, but also for understanding the complex mechanisms, both behavioral and physiological, that influence paternal care in birds. Proximate mechanisms mediating fathering behavior in birds: areas for further study Clearly, a wide array of endocrine and neuroendocrine secretions interact to shape the expression of fathering behavior in birds in both predictable and unpredictable contexts. However, significant gaps remain in our understanding of the proximate regulation of paternal behavior, and of how physiological mechanisms governing male care are shaped by selective forces. Taking a deliberate approach to future research on fathering behavior in male birds can help to narrow these gaps in a number of important ways. First, a strong need exists for continued 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. Second, because individual variation is the substrate for natural selection, studies that focus on individual variation in both hormone secretion and expression of fathering behavior will inform questions about the evolution of proximate mechanisms of paternal care. Third, studies that focus not only on collective “parental care” exhibited by biparental species, but that also investigate mechanisms of both maternal and paternal care independently may reveal important insights into how fathering and mothering behavior are differentially regulated in birds, even when behavioral expression of

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care seems very similar. Fourth, more deliberate selection of focal species and specific paternal behaviors for study is also needed. For example, investigations of particular hormone–paternal behavior interactions currently tend to be biased toward certain taxonomic groups (e.g., studies of interactions of testosterone and paternal care largely focus on songbirds, whereas studies of interactions of corticosterone, prolactin, and paternal care in times of stress focus primarily on seabirds). In addition, the vast majority of studies of hormones and paternal care emphasize provisioning behavior, despite the wide array of paternal behaviors that males express. Thus, expanding future investigations to account for a larger array of species and orders, and a broader sampling of behavioral expression, will be of considerable value in determining whether current hypotheses about the interactions of endocrine and neuroendocrine secretions and paternal behavior are broadly applicable. Fifth, investigations that continue to identify, and more fully investigate, exceptions to the commonly held notions of hormone–paternal behavior interactions that currently dominate the literature (such as the prevailing assumptions that elevations in androgens and glucocorticoids are universally disruptive to paternal care) will be of considerable importance in furthering our understanding of not only how paternal care is regulated physiologically, but also the social, ecological, and evolutionary contexts within which it has evolved. Finally, as the integrative study of complex biological systems continues to provide important insights, investigators that attempt in an intentional way to integrate behavior, circulating hormones, social and experiential cues, and underlying neural and molecular mechanisms will make tremendous strides toward refining our understanding of the complex nature by which paternal behavior in birds is regulated. Acknowledgments I am extremely grateful to Z. M. Benowitz-Fredericks for discussion of and comments on an earlier draft of this manuscript. I also appreciate the constructive suggestions of two anonymous reviewers. References Alonso-Alvarez, C., 2001. Effects of testosterone implants on pair behaviour during incubation in the Yellow-legged Gull Larus cachinnans. J. Avian Biol. 32, 326. Angelier, F., Chastel, O., 2009. Stress, prolactin and parental investment in birds: a review. Gen. Comp. Endocrinol. 163, 142–148. http://dx.doi.org/10.1016/j.ygcen.2009.03.028. Angelier, F., Moe, B., Weimerskirch, H., Chastel, O., 2007. Age-specific reproductive success in a long-lived bird: do older parents resist stress better? J. Anim. Ecol. 76, 1181–1191. http://dx.doi.org/10.1111/j.1365-2656.2007.01295.x. Angelier, F., Clément-Chastel, C., Welcker, J., Gabrielsen, G.W., Chastel, O., 2009. How does corticosterone affect parental behaviour and reproductive success? A study of prolactin in black-legged kittiwakes. Funct. Ecol. 23, 784–793. http://dx.doi.org/10.1111/j. 1365-2435.2009.01545.x. Badyaev, A.V., Duckworth, R.A., 2005. Evolution of plasticity in hormonally integrated parental tactics. Functional Avian Endocrinology. Narosa Publishing House, New Delhi, pp. 375–386. Ball, G.F., 1991. Endocrine mechanisms and the evolution of avian parental care. Proc. XXth Int. Ornithol. Congr. 984–991. Balthazart, J., 1983. Hormonal correlates of behavior. In: Farner, D.S., King, J.R., Parkes, K.C. (Eds.), Avian Biology. Academic Press, New York, pp. 221–365. Barron, D.G., Webster, M.S., Schwabl, H., 2015. Do androgens link morphology and behaviour to produce phenotype-specific behavioural strategies? Anim. Behav. 100, 116–124. http://dx.doi.org/10.1016/j.anbehav.2014.11.016. Bentley, G.E., Kriegsfeld, L.J., Osugi, T., Ukena, K., O'Brien, S., Perfito, N., Moore, I.T., Tsutsui, K., Wingfield, J.C., 2006. Interactions of gonadotropin-releasing hormone (GnRH) and gonadotropin-inhibitory hormone (GnIH) in birds and mammals. J. Exp. Zool. A Comp. Exp. Biol. 305, 807–814. http://dx.doi.org/10.1002/jez.a.306. Blas, J., López, L., Tanferna, A., Sergio, F., Hiraldo, F., 2010. Reproductive endocrinology of wild, long-lived raptors. Gen. Comp. Endocrinol. 168, 22–28. http://dx.doi.org/10. 1016/j.ygcen.2010.03.020. Bókony, V., Lendvai, Á.Z., Liker, A., Angelier, F., Wingfield, J.C., Chastel, O., 2009. Stress response and the value of reproduction: are birds prudent parents? Am. Nat. 173, 589–598. http://dx.doi.org/10.1086/597610. Bonier, F., Martin, P.R., Moore, I.T., Wingfield, J.C., 2009a. Do baseline glucocorticoids predict fitness? Trends Ecol. Evol. 24, 634–642. http://dx.doi.org/10.1016/j.tree. 2009.04.013. Bonier, F., Moore, I.T., Martin, P.R., Robertson, R.J., 2009b. The relationship between fitness and baseline glucocorticoids in a passerine bird. Gen. Comp. Endocrinol. Endocrinology 163, 208–213. http://dx.doi.org/10.1016/j.ygcen.2008.12.013.


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Neuroendocrine Regulation of Metabolism.

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Neuroendocrine Regulation of Hydromineral Homeostasis.

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Reproductive Neuroendocrine Pathways of Social Behavior.

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Hijacking of Endocrine and Metabolic Regulation in Cancer and Diabetes.

Photoperiodic regulation of neuroendocrine-gonadal activity.

Endocrine functions of the hypothalamus and alterations in neuroendocrine function--focus on thyrotropin and growth hormone.

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Including illness behavior in the assessment of endocrine patients.

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Microbial endocrinology: Host-microbiota neuroendocrine interactions influencing brain and behavior.

Editorial: Hormonal and Neuroendocrine Regulation of Energy Balance.