Sharon E. Lynn

Behavioral insensitivity to testosterone: Why and how does testosterone alter paternal and aggressive behavior in some avian species but not others?

Considerable research has been conducted on the interrelationships of the steroid hormone testosterone and reproductive behavior in seasonally breeding birds. In species in which males provide paternal care, males experience a peak in testosterone secretion that coincides with territory establishment and pair bonding, and then drops to a breeding baseline as nests are initiated. A large body of evidence suggests that a males seasonal profile of testosterone reflects a trade-off between expression of sexual and territorial behavior and expression of paternal behavior. For example, studies utilizing testosterone implants to extend the early season peak in plasma testosterone have demonstrated that testosterone tends to increase sexual behavior as well as intensity and persistence of male-male aggression, but also decreases paternal care of offspring. However, recent studies demonstrate that in some species, males do not respond to experimentally elevated testosterone with alterations in aggression and/or paternal care. This phenomenon of behavioral insensitivity to testosterone may relate to a variety of environmental factors, particularly those that necessitate high levels of paternal investment. This review explores both ultimate and proximate explanations for behavioral insensitivity to testosterone, and explores hypotheses to explain how this phenomenon may relate to androgen responses to social interactions during breeding. Further research into behavioral insensitivity to testosterone in a variety of vertebrates may provide additional insights into the complex patterns of sex steroid secretion and its behavioral consequences.

Food, stress, and reproduction: Short-term fasting alters endocrine physiology and reproductive behavior in the zebra finch

Stress is thought to be a potent suppressor of reproduction. However, the vast majority of studies focus on the relationship between chronic stress and reproductive suppression, despite the fact that chronic stress is rare in the wild. We investigated the role of fasting in altering acute stress physiology, reproductive physiology, and reproductive behavior of male zebra finches (Taeniopygia guttata) with several goals in mind. First, we wanted to determine if acute fasting could stimulate an increase in plasma corticosterone and a decrease in corticosteroid binding globulin (CBG) and testosterone. We then investigated whether fasting could alter expression of undirected song and courtship behavior. After subjecting males to fasting periods ranging from 1 to 10h, we collected plasma to measure corticosterone, CBG, and testosterone. We found that plasma corticosterone was elevated, and testosterone was decreased after 4, 6, and 10h of fasting periods compared with samples collected from the same males during nonfasted (control) periods. CBG was lower than control levels only after 10h of fasting. We also found that, coincident with these endocrine changes, males sang less and courted females less vigorously following short-term fasting relative to control conditions. Our data demonstrate that acute fasting resulted in rapid changes in endocrine physiology consistent with hypothalamo-pituitary-adrenal axis activation and hypothalamo-pituitary-gonadal axis deactivation. Fasting also inhibited reproductive behavior. We suggest that zebra finches exhibit physiological and behavioral flexibility that makes them an excellent model system for studying interactions of acute stress and reproduction.

A phylogenetically controlled test of hypotheses for behavioral insensitivity to testosterone in birds.

In most male birds that exhibit paternal care, extending the spring testosterone (T) peak throughout the breeding season reduces nestling provisioning. However, in some species, this trade-off between high T and expression of paternal care is absent. For example, during some or all of the nestling period, T did not affect paternal behavior in Male Lapland longspurs (Calcarius lapponicus), chestnut-collared longspurs (Calcarius ornatus), and great tits (Parus major). Two ecological constraints have been hypothesized to drive insensitivity to T after eggs hatch: (1) a short breeding season that limits breeding opportunities, and (2) a need for paternal care to ensure reproductive success. However, because two of the three species that exhibit T insensitivity are closely related, potential phylogenetic confounds limit determination of which, if either, factor constrains some males to T insensitivity. We examined the effects of supplementary T on paternal behavior in the Snow Bunting (Plectrophenax nivalis), a member of the monophyletic Calcarius/Plectrophenax clade. Male Snow Buntings are constrained to a short breeding season, but paternal care is not essential for survival of nestlings. We administered exogenous T during the parental phase to mimic the early spring T peak. T treatment increased song rates and interfered with paternal behavior such that nestlings of T-implanted males grew more slowly than controls. Our data suggest that T insensitivity in this clade is related to relatively recent constraints of the breeding environment (i.e., not simply common ancestry) and that the necessity of paternal care in some species may be a strong selective factor driving behavioral insensitivity to T during the parental phase.

A single exposure to an acute stressor has lasting consequences for the hypothalamo-pituitary-adrenal response to stress in free-living birds

In vertebrates, activation of the hypothalamo-pituitary-adrenal (HPA) axis in response to unpredictable events results in elevated glucocorticoid secretion. Repeated exposure to stressors alters subsequent glucocorticoid secretion, either by inducing chronic stress or as a result of habituation. However, most studies of repeated stress focus on the impacts of multiple and frequent exposures to acute stressors, and few have been carried out in free-living animals. We investigated whether a single exposure to a novel stressor was sufficient to produce long-lasting alterations in HPA function in free-living eastern bluebirds (Sialia sialis). We subjected adult females to a capture/restraint protocol in which we collected serial blood samples over an hour of restraint to be analyzed for corticosterone. We administered this protocol to three groups of females during the nestling phase of their first and/or second brood of the season: Repeaters (sampled during brood 1 and brood 2), Naïve-Brood 1 (sampled only during brood 1), and Naïve-Brood 2 (sampled only during brood 2). Repeaters had attenuated corticosterone responses to the second restraint bout compared to the first, and in brood 2, Repeaters had lower responses than Naïve-Brood 2 females. However, Naïve-Brood 1 and Naïve-Brood 2 birds did not differ in their responses to restraint. Thus, as little as one prior experience with an acute stressor was sufficient to alter subsequent HPA responsiveness, and this effect was not due to a natural change in HPA responsiveness as the breeding season progressed. These data may have important implications for understanding how acute stressors can alter a free-living animals ability to cope in the face of subsequent stressors, and for longitudinal field studies in which individuals are repeatedly sampled for glucocorticoid responsiveness.

Free-Living Male Mountain White-Crowned Sparrows Exhibit Territorial Aggression Without Modulating Total or Free Plasma Testosterone

Abstract ABSTRACT In some species, expression of territorial aggression is accompanied by a rise in testosterone secretion, but in others aggressive behavior is expressed while testosterone levels remain unchanged. Corticosteroid binding globulin (CBG) binds both corticosterone and testosterone in avian plasma. Thus, increasing corticosterone may result in fluctuations in unbound (“free”) testosterone; this could result in greater biological activity of testosterone without an increase in testosterone secretion. We investigated whether such plasma interactions of testosterone, corticosterone, and CBG might result in alterations of free testosterone in male Mountain White-crowned Sparrows (Zonotrichia leucophrys oriantha). We conducted simulated territorial intrusions during incubation and compared total and free testosterone of males captured immediately following a simulated territorial intrusion with that of males captured passively. All experimental males showed aggressive behavior, but apparently did not modulate total or free testosterone relative to controls.

Food, stress, and circulating testosterone: Cue integration by the testes, not the brain, in male zebra finches (Taeniopygia guttata).

Food abundance is closely associated with reproductive readiness in vertebrates. Food scarcity can activate the hypothalamo-pituitary-adrenal axis, decrease sex steroid secretion, and dampen reproductive behavior. However, the mechanisms underlying these transient effects are unclear. Gonadotropin inhibitory hormone (GnIH), a neuropeptide present in the brain and gonads, is also influenced by glucocorticoids and fasting in some species. We investigated whether fasting stress activated the GnIH system in zebra finches (Taeniopygia guttata), with the potential for downstream effects on reproductive physiology and behavior. We fasted or fed males ad libitum for 10h. Fasting increased corticosterone and decreased testosterone in circulation. To assess whether the decrease in testosterone was mediated by changes in the hypothalamus and/or the gonads, we (1) quantified GnRH- and GnIH-positive neurons in the hypothalamus, (2) assessed hypothalamic gene expression for GnRH and GnIH, and (3) examined gene expression for proteins involved in testosterone synthesis in fasted and control birds. No measure of hypothalamic neuropeptides was related to treatment or circulating steroids. However, birds with higher corticosterone had higher testicular GnIH expression and lower testosterone. StAR and LHR expression were lower in the testes of fasted birds than controls. Thus, the decrease in testosterone was not likely mediated by hypothalamic GnIH, but rather by direct actions of fasting and/or corticosterone on the testes, indicating that the testes can integrate and respond to cues of stress directly. Such local inhibition of testosterone synthesis may allow for rapid and reversible changes in physiology and behavior when conditions are inappropriate for breeding.

Organism-environment interactions in a changing world: a mechanistic approach

Understanding the interactions of an organism and its environment is essential for us to integrate ultimate and proximate causation on a global scale. Organism–environment interaction includes all organisms including animals, plants, and non-eukaryotes, etc. because all of them are responsive to environmental change including those that are human-induced. A mechanistic approach is important for us to understand why some organisms can cope with change and others cannot. Here, we present three examples of environments (“the three poles”) that are changing rapidly and how avian species typical of these ecosystems are responding. These examples include apparently adaptive responses to change in climate (i.e. the predictable environment) in one species in which a lengthened breeding season now allows multiple breeding attempts. Why other species are unable to respond in a similar way remains unclear. A second example describes how changing weather (i.e. the unpredictable) may have disastrous results for breeding success in a species adapted to an extreme cold environment. Implications for climate change in which weather extremes will become more common again suggest a mechanistic approach will be important to understand how organisms may respond. The third example outlines a scenario in which multiple human-induced rapid changes (a combination of predictable and unpredictable such as development, habitat change, introduction of invasive species and climate change) may influence indigenous species in different ways. Organism–environment interaction is a fundamental concept that may unify ultimate and proximate causation and point the way for future investigations striving to understand coping mechanisms in a world where both predictable and unpredictable components of the environment are changing.

Supplementary Testosterone Inhibits Paternal Care in a Tropically Breeding Sparrow, Zonotrichia capensis

In most male birds that exhibit paternal care, elevation in testosterone above the breeding baseline reduces nestling provisioning, which can be detrimental to offspring survival. Mechanisms that may allow some males to avoid this detrimental effect of elevated testosterone include (1) decreased sensitivity to testosterone’s effects on behavior and (2) uncoupling of testosterone secretion from territorial challenges (thus reducing the number of transient elevations in testosterone above the breeding baseline). Both of these “cost‐avoidance” mechanisms have been documented, but whether selection for these mechanisms is correlated or independent is unknown. We investigated the relationship between elevated testosterone and paternal care in a tropical bird, the rufous‐collared sparrow (Zonotrichia capensis). Zonotrichia capensis males exhibit an uncoupling of testosterone secretion from territorial aggression, and this species has a flexible breeding season and a clutch size smaller than those of temperate congeners. We implanted males with testosterone or empty implants and observed paternal behavior 2–3 and 6–7 d posthatch. During both observation periods, 100% of control males fed chicks, whereas 22% and 0% of testosterone‐implanted males fed chicks on days 2–3 and 6–7, respectively. Chicks of testosterone‐implanted males weighed less than control chicks, but tarsus growth, wing growth, and fledging success did not differ. Thus, we demonstrate a robust negative effect of testosterone on nestling provisioning that may not ultimately affect reproductive success. We suggest that these results relate to extreme flexibility in breeding schedule and the small clutch size in this tropical species. Our data also suggest that selection for the two mechanisms to avoid deleterious effects of elevations in testosterone above the breeding baseline likely occurs independently.

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.

Ecological Factors Affecting the Adrenocortical Response to Stress in Chestnut‐Collared and McCown’s Longspurs (Calcarius ornatus, Calcarius mccownii)

Secretion of the steroid hormone corticosterone (CORT) in response to perturbations results in behavior patterns that can maximize survival. Three commonly cited hypotheses suggest that during breeding, there are advantages associated with suppressed (CORT) secretion in (1) the sex that is most important for parental care, (2) individuals in good body condition, and (3) species with a short breeding season and limited renesting opportunities. We addressed these hypotheses in two midlatitude breeders, chestnut‐collared and McCown’s longspurs, by assessing CORT secretion over a 1‐h period of handling. These species have congeners that are exclusively arctic breeders, and this provides a unique opportunity to assess adrenocortical responsiveness both within a phylogenetic framework and across environmental variables. In both species, males and females showed similar CORT secretion patterns in response to handling, and body condition was unrelated to CORT secretion. Additionally, although these midlatitude breeders have more opportunities to attempt a renest than their arctic congeners, their hormonal response to stress was similar to that reported for their arctic congeners. We suggest that an attenuated stress response may relate to the severity of the breeding environment and a low likelihood of successful renesting, since these variables are common to both arctic and grassland habitats.