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Biomedical subjects

John C Wingfield

Publications and source records attributed to John C Wingfield.

At least 37 records · Page 2Linked to original sources

Seasonal gonadal recrudescence in song sparrows: response to temperature cues.

Day length predicts changing of seasons at mid-latitudes, but additional environmental cues (e.g., temperature, rainfall) give more precise information about timing of food peaks critical for offspring survival. We tested the effects of temperature on seasonal reproductive development of male song sparrows (Melospiza melodia morphna) from two populations: the Western Washington coast (3 m) and Cascade Mountains (500-1220 m). Previous work has shown that the timing of gonadal recrudescence can differ between the two sites in the field by as much as two months. However, in the laboratory under identical controlled conditions, testes grow at the same rate. To test whether temperature alone could account for a portion of the variation we measured in the field, we captured birds from each site and held them in temperature controlled environmental chambers that mimicked temperatures experienced either in the mountains or on the coast. We increased day length on a natural schedule, and measured testis volume, levels of circulating androgens and prolactin, and song rates. Increasing day length stimulated gonadal growth in all groups. We found only modest effects of temperature on reproductive development. In the mountain birds colder, montane temperatures slowed rates of growth, delaying the onset of growth by one month. Since temperature changes more markedly during the early winter months in the mountains than on the coast, increasing temperature may be a more relevant cue in timing of reproduction in the mountain population. These data suggest that while temperature helps to explain some of the variation in reproductive timing of free living sparrows, another as yet untested cue in the field may play a more important role. Furthermore, our data suggest that individuals within the same species may rely on different proximate cues for reproductive timing depending on the specific habitat in which they live.

Analysis of Variance↗

Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain.

We recently identified a novel hypothalamic neuropeptide inhibiting gonadotropin release in quail and termed it gonadotropin-inhibitory hormone (GnIH). Cell bodies and terminals containing the dodecapeptide GnIH are localized in the paraventricular nucleus (PVN) and median eminence, respectively. To understand the physiological role of GnIH, we investigated the mechanisms that regulate GnIH expression. In this study, we show that melatonin originating from the pineal gland and eyes induces GnIH expression in the quail brain. Pinealectomy (Px) combined with orbital enucleation (Ex) (Px plus Ex) decreased the expression of GnIH precursor mRNA and content of mature GnIH peptide in the diencephalon, which includes the PVN and median eminence. Melatonin administration to Px plus Ex birds caused a dose-dependent increase in expression of GnIH precursor mRNA and production of mature peptide. The expression of GnIH was photoperiodically controlled and increased under short-day photoperiods, when the duration of melatonin secretion increases. To identify the mode of melatonin action on GnIH induction, we investigated the expression of Mel(1c), a melatonin receptor subtype, in GnIH neurons. In situ hybridization of Mel(1c) mRNA combined with immunocytochemistry for GnIH revealed that Mel(1c) mRNA was expressed in GnIH-immunoreactive neurons in the PVN. Melatonin receptor autoradiography further revealed specific binding of melatonin in the PVN. These results indicate that melatonin is a key factor for GnIH induction. Melatonin appears to act directly on GnIH neurons through its receptor to induce GnIH expression. This is the first demonstration, to our knowledge, of a direct action of melatonin on neuropeptide induction in any vertebrate class.

Animals↗

Increased sensitivity of the serotonergic system during the breeding season in free-living American tree sparrows.

In order to understand the physiological role of serotonin in regulating aggressive behaviour it is important to understand how this neuromodulator acts within the context of a naturally fluctuating social and physical environment. To accomplish this, we examined the effect of the selective serotonin reuptake inhibitor fluoxetine during the breeding season in free-living male American tree sparrows (Spizella arborea) in Northern Alaska. During this time period males are maximally aggressive towards territorial intruders. Male, territorial sparrows were injected with either vehicle or a 10 mg/kg dose of fluoxetine. One hour later, aggression was measured using a simulated territorial intrusion. Depending upon when birds were sampled, the aggression scores for vehicle and fluoxetine treatments were grouped according to the number of days after territorial behaviour was initiated. The three groups were: early, days 1-5; middle, days 6-10; and late, days 11-15. There was a significant overall difference between groups (F(5,36)=5.18, P<0.0015). Post hoc analysis demonstrated that the level of aggression did not differ between the three groups of saline injected birds. However, fluoxetine injected birds showed a time dependent decrease in aggression. When compared to control birds the middle and late fluoxetine groups had significantly less aggression. Furthermore, the late group of fluoxetine treated birds were significantly less aggressive than the early group of fluoxetine birds. This demonstrates that free-living male ATSPs show a rapid change in their behavioural response to fluoxetine across the first 2 weeks of the breeding season. The rapidity of the change in responsiveness suggests a dynamic sensitivity of the serotonergic system.

Aggression↗

Metabolic profile of long-distance migratory flight and stopover in a shorebird.

Migrating birds often complete long non-stop flights during which body energy stores exclusively support energetic demands. The metabolic correlates of such long-distance travel in free-living migrants are as yet poorly studied. Bar-tailed godwits, Limosa lapponica taymyrensis, undertake a 4500 km flight to their single spring stopover site and thus provide an excellent model in which to determine the energy fuels associated with endurance travel. To this end, we evaluated plasma concentrations of six key metabolites in arriving godwits caught immediately upon landing near their stopover site. Initial metabolite levels were compared with levels after 5 h of inactive rest to determine how flight per se affects energy metabolism. Birds refuelling on the stopover site were also examined. Arriving godwits displayed elevated plasma free fatty acids, glycerol and butyrate, confirming the importance of lipid fuel in the support of extended migratory activity. Further-more, elevated plasma triglycerides in these birds suggest that fatty acid provisioning is facilitated through hepatic synthesis and release of neutral lipids, as previously hypothesized for small migrants with high mass-specific metabolic rates. Finally, elevations in plasma uric acid suggest that protein breakdown contributes to the support of long-distance movement, to possibly maintain citric acid cycle intermediates, gluconeogenesis and/or water balance.

Africa↗

Corticosterone inhibits feather growth: potential mechanism explaining seasonal down regulation of corticosterone during molt.

Corticosterone (CORT) is seasonally modulated in many passerines, with plasma CORT concentrations lowest during the prebasic molt when all feathers are replaced. To explain why, we proposed that the birds downregulate natural CORT release during molt in order to avoid CORT's degradative effects on proteins and its inhibition of protein synthesis. If CORT exerted these effects during molt, it could slow protein deposition during feather production and potentially result in a longer period of degraded flight performance. To test this hypothesis, either empty or CORT-filled silastic implants were inserted into captive European starlings (Sturnus vulgaris) and white-crowned sparrows (Zonotrichia leucophrys) undergoing induced (feather replacement after plucking) and natural molts. We then measured the rate of feather re-growth by regularly measuring the length of primary, secondary, and tail feathers. CORT implanted birds showed a significantly decreased rate of feather growth compared to control animals. Basal CORT concentrations of induced molt and non-molting birds were also compared but no difference was noted. The results suggest a tradeoff; a complete set of new feathers may be more important to the survival of a bird than the ability of CORT to respond maximally to a stressor.

Animals↗

Testosterone and group size in cliff swallows: testing the "challenge hypothesis" in a colonial bird.

The "challenge hypothesis" states that increases in testosterone levels of male animals during the breeding season are directly related to the extent of intrasexual competition for resources or mates that they experience. Although often tested in territorial species, the challenge hypothesis has not been evaluated for colonial animals that live in groups of different sizes and that thus experience different intensities of intrasexual competition. We measured circulating testosterone levels of male and female cliff swallows (Petrochelidon pyrrhonota) in southwestern Nebraska, where these birds nest in colonies of widely different sizes. Males had significantly higher testosterone levels than females, as expected. For males especially, there was a seasonal rise in testosterone levels early in the nesting cycle, corresponding to the period when birds were establishing nest ownership and egg laying, and then a fall as they switched to parental duties. Testosterone levels varied significantly with colony size; for both sexes, birds in larger colonies had higher levels of testosterone than those in smaller colonies when controlling for date. Age and body mass were not related to testosterone levels. Higher levels of testosterone for birds of both sexes in larger colonies probably reflect greater competition for matings, often extra pair, in the more social nesting situations. The results support the predictions of the challenge hypothesis.

Analysis of Variance↗

The adrenocortical response of tufted puffin chicks to nutritional deficits.

In several seabirds, nutritional state of a nest-bound chick is negatively correlated with the activity of its hypothalamus-pituitary-adrenal (HPA) axis. Increased corticosterone (cort) secretion has been shown to facilitate changes in behavior that allow hungry chicks to obtain more food from parents. However, if parents are not willing/able to buffer their young from temporary food shortages, increased cort secretion could be detrimental to undernourished chicks. In a system where parents are insensitive to chick demands, low benefits and high costs of activation of the HPA-axis in hungry chicks should lead to a disassociation of the nutritional state of the young and the activity of its HPA-axis. We tested this novel hypothesis for the tufted puffin (Fratercula cirrhata), a seabird with intermittent provisioning of a nest-bound semi-precocial chick. We examined the HPA-axis activity of captive chicks exposed to the following: (1) a short-term (24 h) food deprivation; and (2) an array of prolonged (3 weeks) restrictions in feeding regimens. We found that in response to a short-term food deprivation chicks decreased baseline levels of cort and thyroid hormones. In response to prolonged restrictions, food-limited chicks exhibited signs of nutritional deficit: they had lower body mass, endogenous lipid reserves, and thyroid hormone titers compared to chicks fed ad libitum. However, baseline and maximum acute stress-induced levels of cort were also lower in food-restricted chicks compared to those of chicks fed ad libitum. These results support a major prediction of the study hypothesis that puffin chicks suppress HPA-axis activity in response to short- and long-term nutritional deficits. This physiological adaptation may allow a chick to extend its development in the nest, while eluding detrimental effects of chronic cort elevation.

Adrenal Cortex↗

Steroids in allantoic waste: an integrated measure of steroid exposure in ovo.

Recent studies examining patterns and consequences of variation in maternally deposited steroids in avian egg yolk have demonstrated that these maternal hormones can have dramatic effects on chick phenotypes. However, maternal steroids are not the only source for avian embryos, which activate endocrine axes relatively early in development and are capable of producing substantial amounts of endogenous steroids. Although organizational effects of steroids have been demonstrated, the interactions between steroids from yolk and endogenous production have not been addressed. Steroids in the yolk are likely to alter development of the embryo's endocrine axes. The ability to assess total steroid exposure in ovo in a nonlethal fashion would improve our understanding of these interactions and help elucidate the mechanisms by which maternal steroids alter chick phenotype. Steroid levels in allantoic waste provide a cumulative measure of steroids excreted in ovo and may prove to be a useful tool. We present data from semiprecocial seabirds, common murres, demonstrating the presence of detectable steroids in allantoic waste and suggesting that some reflect differences in timing of hatching and may provide information about aspects of chick phenotype.

Allantois↗

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.

Androgens↗

The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease.

Why do we get the stress-related diseases we do? Why do some people have flare ups of autoimmune disease, whereas others suffer from melancholic depression during a stressful period in their life? In the present review possible explanations will be given by using different levels of analysis. First, we explain in evolutionary terms why different organisms adopt different behavioral strategies to cope with stress. It has become clear that natural selection maintains a balance of different traits preserving genes for high aggression (Hawks) and low aggression (Doves) within a population. The existence of these personality types (Hawks-Doves) is widespread in the animal kingdom, not only between males and females but also within the same gender across species. Second, proximate (causal) explanations are given for the different stress responses and how they work. Hawks and Doves differ in underlying physiology and these differences are associated with their respective behavioral strategies; for example, bold Hawks preferentially adopt the fight-flight response when establishing a new territory or defending an existing territory, while cautious Doves show the freeze-hide response to adapt to threats in their environment. Thus, adaptive processes that actively maintain stability through change (allostasis) depend on the personality type and the associated stress responses. Third, we describe how the expression of the various stress responses can result in specific benefits to the organism. Fourth, we discuss how the benefits of allostasis and the costs of adaptation (allostatic load) lead to different trade-offs in health and disease, thereby reinforcing a Darwinian concept of stress. Collectively, this provides some explanation of why individuals may differ in their vulnerability to different stress-related diseases and how this relates to the range of personality types, especially aggressive Hawks and non-aggressive Doves in a population. A conceptual framework is presented showing that Hawks, due to inefficient management of mediators of allostasis, are more likely to be violent, to develop impulse control disorders, hypertension, cardiac arrhythmias, sudden death, atypical depression, chronic fatigue states and inflammation. In contrast, Doves, due to the greater release of mediators of allostasis (surplus), are more susceptible to anxiety disorders, metabolic syndromes, melancholic depression, psychotic states and infection.

Adaptation, Physiological↗

Balancing food and predator pressure induces chronic stress in songbirds.

The never-ending tension between finding food and avoiding predators may be the most universal natural stressor wild animals experience. The 'chronic stress' hypothesis predicts: (i) an animal's stress profile will be a simultaneous function of food and predator pressures given the aforesaid tension; and (ii) these inseparable effects on physiology will produce inseparable effects on demography because of the resulting adverse health effects. This hypothesis was originally proposed to explain synergistic (inseparable) food and predator effects on demography in snowshoe hares (Lepus americanus). We conducted a 2 x 2, manipulative food addition plus natural predator reduction experiment on song sparrows (Melospiza melodia) that was, to our knowledge, the first to demonstrate comparable synergistic effects in a bird: added food and lower predator pressure in combination produced an increase in annual reproductive success almost double that expected from an additive model. Here we report the predicted simultaneous food and predator effects on measures of chronic stress in the context of the same experiment: birds at unfed, high predator pressure (HPP) sites had the highest stress levels; those at either unfed or HPP sites showed intermediate levels; and fed birds at low predator pressure sites had the lowest stress levels.

Analysis of Variance↗

Plasticity of the avian song control system in response to localized environmental cues in an equatorial songbird.

A striking feature of the vertebrate brain is its plasticity. In high-latitude vertebrates, seasonal plasticity of the brain is driven by ubiquitous photoperiod cues and therefore is highly predictable and synchronous across extensive geographic ranges. A pronounced example of seasonal brain plasticity occurs in the nuclei that regulate song behavior in songbirds. These nuclei are larger in breeding than in nonbreeding birds. In the tropics, photoperiod varies little annually, and other environmental cues important for breeding can show considerable local geographic variability. We investigated whether localized patterns of seasonal breeding in tropical birds are associated with brain plasticity. We studied two populations of rufous-collared sparrows (Zonotrichia capensis) that breed, only 25 km apart, on the equator but out of phase with each other. We measured gonadal activity and the size of song nuclei (high vocal center, robust nucleus of the arcopallium, and area X) during each population's breeding and nonbreeding periods. Breeding males had larger song nuclei and greater gonadal activity than did nonbreeding birds. This plasticity was associated with local environmental cues, such that the two populations exhibit asynchronous changes in brain structure. These results demonstrate the sensitivity of the brain and its ability to use a variety of environmental cues to coordinate seasonal plasticity and reproduction.

Animals↗

Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows.

The immunocompetence handicap hypothesis proposes that testosterone (T)-dependent sexual signals are honest indicators of male health or genetic quality because only high-quality males are able to withstand the obligate effects of T-induced immunosuppression. In birds, the basic assumption that T suppresses immune function is equivocal, and the physiological mechanisms underlying T-induced immunosuppression remain to be investigated. We explored the proximate pathways of T-induced immunosuppression in song sparrows (Melospiza melodia) by treating captive nonbreeding males with different androgens and measuring several components of acquired immune function. Males implanted with T suppressed cell-mediated and humoral immune responses compared to males implanted with 5alpha-dihydrotestosterone (DHT), dehydroepiandrosterone, or control (empty) implants. Furthermore, T treatment increased plasma levels of corticosterone and decreased body mass and fat stores in relation to other treatments. The failure of DHT to depress immune function suggests that T-induced immunosuppression does not occur through a direct pathway because both T and DHT bind to androgen receptors on target cells. Instead, we outline indirect pathways that are likely responsible for suppression of the avian immune system that include stress-induced immunosuppression, aromatization to estrogen, and alterations in energy allocation that constrain expenditures toward immune system activation.

Androgens↗

Testosterone in tropical birds: effects of environmental and social factors.

Previous investigations suggest that male tropical birds have lower plasma testosterone concentrations than northern latitude species. To test whether this generalization is valid, we analyzed all currently available plasma testosterone data of tropical birds. We focused on peak breeding testosterone levels using phylogenetic and conventional statistics. Explanatory variables considered were social mating system, type of territoriality, breeding season length, and altitude. On average, tropical birds had lower mean peak testosterone levels than northern temperate birds. However, in several tropical species, testosterone levels were well within the range of northern latitude birds. Without controlling for phylogeny, breeding season length, type of territoriality, and altitude explained a significant proportion of the variance in testosterone levels. The shorter the breeding season, the higher the testosterone levels. Tropical birds that defend a breeding season territory had higher testosterone levels than birds that were year-round territorial or colonial, and testosterone levels were positively correlated with altitude. When controlling for phylogeny, only breeding season length predicted testosterone levels. In conclusion, we propose to refine previous notions of low plasma testosterone levels in tropical birds: short breeding seasons and perhaps environmental conditions at high altitudes precipitate conditions under which high testosterone levels are beneficial in the tropics.

Animals↗

Reproductive development according to elevation in a seasonally breeding male songbird.

Seasonal temperate zone breeders respond to increasing day length to anticipate the approach of spring breeding conditions. Other (supplementary) environmental cues, such as temperature and precipitation, were historically thought to play unimportant roles in reproductive timing. We demonstrate variation in reproductive timing across small geographic distances by examining the vernal testicular recrudescence of adult song sparrows (Melospiza melodia morphna) breeding in coastal (0-10 m elevation) and montane (280-1220 m elevation) habitats. Each year, these birds experienced the same photoperiod, but were exposed to different supplementary cues that varied with altitude. Coastal birds experienced warmer and more stable temperatures during late winter and early spring than did montane birds. We measured bud opening, emergence of new green shoots, and arthropod biomass to monitor the pace of spring's approach. New spring shoots emerged 2 months earlier on the coast than in the mountains and buds on flowering trees and shrubs also tended to open earlier at the coast. Arthropod biomass was similar in both the mountains and the coast during early spring, and began to increase in early summer. Reproductive morphology (i.e. testis volume and cloacal protuberance length) developed up to 2 months earlier on the coast than in the mountains. Testicular recrudescence occurred earlier on the coast in most years and proceeded at a faster rate in 1 year. Circulating levels of luteinizing hormone, follicle stimulating hormone and prolactin increased through the season, but did not correlate with differences between sites. Both populations responded similarly when exposed to identical photoperiodic cues in the laboratory. Therefore, we suggest that an integrated response to cues characteristic of location and elevation account for differences in patterns measured in the field.

Altitude↗

The effects of combined aromatase inhibitor and anti-androgen on male territorial aggression in a tropical population of rufous-collared sparrows, Zonotrichia capensis.

Territorial aggression, exhibited by male vertebrates in a reproductive context, is generally thought to be mediated by elevated levels of the gonadal steroid hormone testosterone. Rufous-collared sparrows from Papallacta, Ecuador are only aggressive during the breeding season when plasma testosterone concentrations are elevated. However, previous experiments have determined that during the breeding season testosterone does not increase in response to territorial challenges and testosterone implants do not make males more aggressive. This relationship between testosterone and aggression is different from closely related northern latitude species. We conducted another experiment investigating the role of testosterone in mediating territorial aggression, during the breeding season, in male rufous-collared sparrows. We predicted that blocking the actions of the testosterone would suppress aggression in response to territorial challenges. During the early breeding season males were captured using a simulated territorial intrusion and there was no relationship between time to capture and plasma testosterone, dihydrotestosterone, and corticosterone concentrations. Individual males were then implanted with both the aromatase inhibitor ATD and the anti-androgen Flutamide or empty implants as a control. After one week, birds were challenged with a simulated territorial intrusion and the aggressive responses measured. There were no differences in individual behavioral responses (number of songs, flights, closest approach, or time within 5 m) or overall aggression between the two groups. Androgen levels were elevated, post-implant, in the experimental group suggesting that the treatment was successful by blocking the negative feedback system. We conclude that pharmacologically inhibiting testosterone during the breeding season does not affect territorial aggression in these birds.

Aggression↗

Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype.

Many environmental perturbations may elevate plasma corticosterone in laying birds, including disease, poor body condition, high predator density, anthropogenic disturbance, and/or food scarcity. When adverse conditions are not dire enough to dictate foregoing reproduction, maternal corticosterone in egg yolk may phenotypically engineer offspring so as to maximize success under the constraints of the local environment. We tested the hypotheses that corticosterone in avian egg yolk should correlate with corticosterone in maternal circulation at the time of laying, and that high corticosterone in yolk should then influence offspring development and adult phenotype. We implanted female Japanese quail (Coturnix coturnix japonica) with corticosterone-filled or empty implants and measured concentrations of corticosterone in the yolk of their eggs. Then we incubated the eggs and raised the chicks to test for effects on growth and hypothalamo-pituitary-adrenal response to capture and restraint in adult offspring. We found that corticosterone implants significantly increased corticosterone in yolk. Furthermore, chicks of corticosterone-implanted mothers grew more slowly than controls and showed higher activity of the hypothalamo-adrenal axis in response to capture and restraint as adults. These results suggest that stress experienced by a laying bird has significant effects on offspring development and adult phenotype, possibly mediated by the transfer of maternal corticosterone to yolk.

Animals↗