[Show abstract][Hide abstract] ABSTRACT: Testosterone is a key hormone for the development of secondary sexual characters and dimorphisms in behavior and morphology of male vertebrates. Because females often express detectable levels of testosterone, testosterone has been suggested to also play a role in the modulation of secondary sexual traits in females. Previous comparative analyses in birds and fish demonstrated a relationship between male-to-female testosterone ratios and the degree of sexual dimorphism. Furthermore, female maximum testosterone was related to mating system and coloniality. Here, we reevaluate these previous ideas using phylogenetic analyses and effect size measures for the relationship between birds’ male-to-female maximum testosterone levels. Further, we investigate the seasonal androgen response of female birds (the difference from baseline to maximum testosterone), which in males is strongly related to mating system. We could not confirm a relationship between male-to-female testosterone, maximum female testosterone, or the seasonal androgen response of females with any life-history parameter. We conclude that the expectation that testosterone regulates traits in females in a similar manner as in males should be reconsidered. This expectation may be partially due to hormone manipulation studies using pharmacological doses of testosterone that had similar effects in females than in males but may be of limited importance for the physiological range of testosterone concentrations occurring within ecological and evolutionary contexts. Thus, the assumption that circulating testosterone should covary with ecologically relevant secondary sexual traits in females may be misleading: selection pressures on females differ from those on males and females may regulate behavior differently.
[Show abstract][Hide abstract] ABSTRACT: Emberizid sparrows (emberizidae) have played a prominent role in the study of avian vocal communication and social behavior. We present here brain transcriptomes for three emberizid model systems, song sparrow Melospiza melodia, white-throated sparrow Zonotrichia albicollis, and Gambel's white-crowned sparrow Zonotrichia leucophrys gambelii. Each of the assemblies covered fully or in part, over 89% of the previously annotated protein coding genes in the zebra finch Taeniopygia guttata, with 16,846, 15,805, and 16,646 unique BLAST hits in song, white-throated and white-crowned sparrows, respectively. As in previous studies, we find tissue of origin (auditory forebrain versus hypothalamus and whole brain) as an important determinant of overall expression profile. We also demonstrate the successful isolation of RNA and RNA-sequencing from post-mortem samples from building strikes and suggest that such an approach could be useful when traditional sampling opportunities are limited. These transcriptomes will be an important resource for the study of social behavior in birds and for data driven annotation of forthcoming whole genome sequences for these and other bird species.
[Show abstract][Hide abstract] ABSTRACT: The aim of this study was to determine circulating patterns of the three major adrenal steroids in blood in response to stress during acute restraint handling in two subspecies of white-crowned sparrow (Zonotrichia leucophrys). Gambel’s white-crowned sparrows (Z.l. gambelii) are long distance migrants that breed at high latitudes and Nuttall’s white-crowned sparrows (Z.l. nuttalli) are residents of coastal California. Column partition chromatography was developed to separate progesterone, dehydroepiandrosterone (DHEA), and corticosterone from a small plasma sample. Each of these steroids has the capability to modulate the stress response through various mechanisms. For example, progesterone is bound to corticosterone binding globulin (CBG) with a higher affinity than corticosterone. If plasma levels of progesterone rise during acute stress, then this could displace corticosterone from CBG and increase the amount of biologically active, free, corticosterone in blood. Dehydroepiandrosterone (DHEA) has been implicated to have many anti-stress properties with the potential to mitigate some of the actions of corticosterone. Results indicate that progesterone levels in both subspecies are elevated in response to acute stress handling. DHEA levels declined in Gambel’s but did not change in Nuttall’s. Thus DHEA does not follow the same secretory pattern as in mammals. Corticosterone levels were elevated in response to acute stress handling in both subspecies. This study provides new insight into an integrated stress response among three steroids.
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 01/2014;
[Show abstract][Hide abstract] ABSTRACT: Across vertebrates, the hypothalamic-pituitary-adrenal axis is a conserved neuroendocrine network that responds to changing environments and involves the release of glucocorticoids into the blood. Few studies have been carried out concerning mammalian adrenal regulation in wild species either in the laboratory or field, and even fewer have been able to determine true glucocorticoid baselines. We studied the South-American caviomorph rodent Octodon degus, a diurnal and social mammal that has become an important species in the biological research. First, we determined the plasma cortisol baseline and the acute stress concentrations during the non-reproductive and mating seasons in free-living individuals. Second, using the same protocol we assessed the impact of long-term captivity on the adrenal function in wild-caught degus and degus born in laboratory. Third, we examined laboratory groups formed with degus taken from two distant natural populations; one of them originally occurs at the Andes Mountains in high altitude conditions. The data revealed seasonal modulation of basal cortisol in the wild associated with mating. In laboratory, degus presented higher cortisol stress responses, with greater magnitudes shown in degus born and reared in captivity. No differences between populations were found. The results suggest differential regulatory mechanisms between basal and stress-induced cortisol levels, and context dependence of cortisol modulation in a mammalian species.
General and Comparative Endocrinology 12/2013; · 2.82 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Background/Aim: Sickness behaviors are the behavioral alterations animals exhibit during the course of an infection, often accompanied by reduced reproductive activity. Adopting sickness behaviors may aid in overcoming the infection, by diverting energy from routine activities towards enhancement of the immune system. Nonetheless, sickness behaviors are plastic, being influenced by specific environmental and social circumstances. Here, we tested whether the presentation of a novel female to males suffering from a simulated infection could impact the behavioral effects of sickness, the reproductive axis, or both. Methods: Male zebra finches were housed in isolation and injected intramuscularly with lipopolysaccharide or saline. Behaviors were recorded before (3 h before injection) and after (3.5 h after injection) addition of a novel female to the cage for 30 min. Four hours after injection, we collected the brain and testis for the analysis of important reproductive axis modulators, gonadotropin-releasing hormone, and gonadotropin-inhibitory hormone, and to quantify gene expression of a proinflammatory cytokine involved in the regulation of sickness behaviors [interleukin (IL)-1β]. Testosterone was quantified in the plasma. Results: The presence of a novel female diminished sickness behaviors and induced alterations in the reproductive axis within 30 min, with no associated changes in brain gene expression of IL-1β. Social environment itself altered brain gene expression of IL-1β. Conclusions: Male zebra finches prioritize the opportunity to mate versus investment in recovery from an infection, as determined by reduced expression of sickness behaviors when a potential mate was present. The behavioral effects of IL-1β appear to be context dependent in this species.
[Show abstract][Hide abstract] ABSTRACT: In this perspective paper, we emphasize the importance that integrative mechanisms, and especially the GC (glucocorticoid) stress response, can play in the ability of vertebrates to cope with ongoing global change. The GC stress response is an essential mediator of allostasis (i.e. the responses of an organism to a perturbation) that aims at maintaining stability (homeostasis) despite changing conditions. The GC stress response is a complex mechanism that depends on several physiological components and aims at promoting immediate survival at the expense of other life-history components (e.g. reproduction) when a labile perturbation factor (LPF) occurs. Importantly, this mechanism is somewhat flexible and its degree of activation can be adjusted to the fitness costs and benefits that result from the GC stress response. Therefore, this GC stress response mediates life-history decisions and is involved in the regulation of important life-history trade-offs. By inducing abrupt and rapid changes in the regime of LPFs, we believe that global change can affect the efficiency of the GC stress response to maintain homeostasis and to appropriately regulate these trade-offs. This dysfunction may result in an important mismatch between new LPFs and the associated GC stress response and, thus, in the inability of vertebrates to cope with a changing world. In that context, it is essential to better understand how the GC stress response can be adjusted to new LPFs through micro-evolution, phenotypic plasticity and phenotypic flexibility (habituation and sensitization). This paper sets up a theoretical framework, hypotheses and new perspectives that will allow testing and better understanding how the GC stress response can help or constrain individuals, populations and species to adjust to ongoing global change.
General and Comparative Endocrinology 06/2013; · 2.82 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: In seasonally breeding birds, the annual cycle of photoperiod is a principal environmental cue for temporal arrangement of different life-history stages, such as migration and breeding. In the past, most research has focused on the mechanisms of photoperiodic control of breeding with less attention paid to migration. In Gambel’s white-crowned sparrow Zonotrichia leucophrys gambelii (GWCS), photoreceptors for induction of breeding are known to reside in the basal hypothalamus. However, it is unknown whether the sites of photoperiodic reception for vernal migration are the same as those for breeding. Therefore, we hypothesized that they may be controlled separately. In this study, we exposed photosensitive GWCSs to low-penetration green light (wavelength at 510 nm) under a regime of 1 lux during the day and <0.1 lux at night, and switched the photoperiodic conditions from short day (10 h daytime) to long day (18 h daytime). The results showed that the experimental birds developed traits associated with vernal migration including mass increase, fat deposition and migratory restlessness behavior when transferred from short day to long day green light cycles, while control birds maintained continuously on short day green light conditions did not express any migration related characteristics. Neither experimental nor control groups showed gonadal recrudescence under either green light cycles. In support of our hypothesis, we were able to apparently dissociate the photoperiodic responses regulating vernal migration and breeding, which suggests separate mechanisms of photoperiodic time measurement. Such distinct photoperiodic mechanisms may drive the fine-tuned temporal arrangement of the two life history stages.
Current Zoology 06/2013; 59(3):349-359. · 1.39 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Previous studies show that most birds inhabiting temperate regions have well defined life history stages, and they modulate the production of testosterone (T) and corticosterone (CORT) in response to changes in seasonality. In this study we aimed to examine baseline and stress-induced levels of CORT and circulating T in relation with life history stages in the rufous-collared sparrow, Zonotrichia capensis. We carried out this study for a year in a population inhabiting riparian habitats in the Atacama Desert in Chile, one of the most climatically stable and driest places in the world. This environment shows minimal yearly change in average temperature and precipitation is virtually zero. We found individuals breeding, molting and overlapping breeding and molt year round, although most individuals were molting during March and in breeding condition during October. T levels were not related to individual breeding condition, and at population level they were not significantly different across sampling months. Baseline levels of CORT did not vary across the year. Stress-induced levels of CORT were suppressed during March when most of the birds were molting. This phenomenon was also observed in birds not molting during this period suggesting a mechanism other than molt in determining the stress-response suppression. Our results strongly suggest that in this study site, long-term extremely stable conditions could have relaxed the selective pressures over the timing of life history stages which was evidenced by the breeding and molt schedules, its overlap and endocrine profiles.
General and Comparative Endocrinology 05/2013; · 2.82 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Highlights
► Perturbations of the environment can be labile or permanent, with consequences for how animals respond. ► The exposome is the sum of environmental factors affecting an individual from conception to death. ► Allostasis and reactive scope concepts combine costs of daily routines and stress. ► The adrenocortical response to stress includes hormone secretion, transport and response. ► Stress responses involve modulation of robustness (resistance), responsiveness (flexibility) and resilience (recovery).
[Show abstract][Hide abstract] ABSTRACT: Glucocorticoids are essential for life and their secretion is regulated by the hypothalamic-pituitary-adrenal axis (HPA). The HPA axis is often divided into two components: baseline glucocorticoids levels and stress response glucocorticoids levels, which are affected by changes in ambient temperature and productivity among others factors. An approximation to evaluate how a species copes with these changes is to evaluate differences of this hormone amongst populations of the same species that inhabit places ideally presenting all the possible combinations of temperature and productivity. We aimed to evaluate whether environmental temperature or productivity, represent challenges in terms of stress in the Thorn-tailed Rayadito (Aphrastura spinicauda). We examined circulating baseline levels of CORT and stress responses from three populations, covering the whole geographic distribution of the species across large gradients in weather conditions. If low temperature influences baseline CORT levels, we expect higher levels of this hormone in the southernmost population (higher latitude). However, if productivity is the factor that influences baseline CORT levels, we expect the contrary pattern, that is, lower values of this hormone in the southernmost population (more productive environment). We observed that baseline CORT levels presented lower values in the southernmost population, supporting the environmental productivity hypothesis. Secondly, we tested the hypothesis that individuals breeding at higher latitudes should have a lower stress response than individuals breeding at lower latitudes. Contrary to our expectations, we found that stress response did not vary among populations in any of the three years. We concluded that low environmental temperatures did not represent a stress situation for the Thorn-tailed Rayadito if food abundance was sufficient to support energetic demands.
General and Comparative Endocrinology 01/2013; · 2.82 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 1. Rapid, effective and enduring responses of physiology and behaviour to perturbations of the environment are key to robustness of an organism (ability to resist perturbations) and resilience (ability to resist and recover quickly from perturbations) so that the normal life cycle can be resumed quickly. 2. Perturbations of the environment can be labile (i.e. eventually subside) or permanent such as when human activity changes the environment in the long term, for example, deforestation, urbanization, etc. 3. Hormonal responses to labile perturbation factors (LPFs) allow organisms to cope during the perturbation and then return to the normal life cycle. These hormonal responses are called stress responses especially in cases when major changes in physiology and behaviour occur (emergency life-history stage). 4. Permanent perturbations require more than just temporary acclimation resulting in changes in range, adaptation or in some cases local extinction. Perturbations can be abiotic, biotic and social, but these are not mutually exclusive. 5. Here I focus on the effects of abiotic perturbation factors and their effects on the hypothalamo-pituitary—adrenal/interrenal axis in vertebrates. There is a great need for more field investigations of responses of free-living populations to perturbations of the environment, especially now that it appears the frequency and intensity of these events is increasing. However, such studies will require a high degree of opportunism on the part of the investigators to take advantage of unpredictable events when they occur.
[Show abstract][Hide abstract] ABSTRACT: Abstract The roles of testosterone (T) during reproduction are often complex and vary among and within vertebrate taxa and locations, making general hypotheses relating T to breeding behavior and success difficult to integrate. In birds, T is thought to influence degrees of territoriality and associated aggression in males to maximize breeding success. Importantly, most work supporting these ideas has been conducted in the Northern Hemisphere. However, accumulating work on tropical species has shown divergent patterns of T in association with breeding behavior. The compilation of work from northern temperate and tropical species suggests that the function of T in relation to breeding behavior varies across latitude and environmental conditions. We investigate the patterns of T in relation to breeding behavior in a subspecies of the rufous-collared sparrow Zonotrichia capensis australis breeding at high latitude in the Southern Hemisphere (55°S). We then compare the T profiles and breeding behaviors of male Z. c. australis to conspecifics breeding in the tropics and congeners in North America to test the hypothesis that environments with breeding seasons of similar lengths will drive similar patterns of T in relation to breeding behavior. We found that Z. c. australis have high levels of T during the early-breeding periods when territories are being established and low levels of T during the parental phase of breeding, similar to temperate and Arctic birds in the Northern Hemisphere but unlike tropical Zonotrichia capensis costaricensis. In contrast, we found that Z. c. australis also exhibit similar aggressive behaviors in early breeding and midbreeding, unlike many birds in the Northern Hemisphere.
Physiological and Biochemical Zoology 01/2013; 86(6):782-90. · 2.46 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Abstract Organisms that breed multiple times must trade off resources between current and future reproduction. In many species, sexual selection can lead to reduced levels of immune function in males because they invest heavily in current reproduction at the expense of self-maintenance. Much less is known about whether the same trend is seen in species such as the brood-parasitic brown-headed cowbird Molothrus ater (hereafter "cowbird"), in which females invest heavily in current reproduction. We examined two measures of immune function (bactericidal capacity of the plasma and the phytohemagglutinin swelling response) and baseline levels of corticosterone in both sexes of the cowbird and its nonparasitic relative the red-winged blackbird Agelaius phoeniceus (hereafter "redwing") during the breeding and subsequent nonbreeding seasons. We found that female cowbirds exhibited significantly lower levels of both measures of immune function than did male cowbirds and female redwings during the breeding season but had comparable levels during the nonbreeding season. Female redwings, in contrast, exhibited higher or comparable levels of immune function when compared with male redwings during the breeding season. In conjunction with published accounts documenting significantly higher rates of mortality for female cowbirds compared with male cowbirds and the fact that female cowbirds produce very high numbers of eggs (25-65) in a single breeding season, our results suggest that female cowbirds invest heavily in current reproduction at the expense of self-maintenance.
Physiological and Biochemical Zoology 01/2013; 86(1):61-72. · 2.46 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Changes in hormones can affect many types of learning in vertebrates. Adults experience fluctuations in a multitude of hormones over a temporal scale, from local, rapid action to more long-term, seasonal changes. Endocrine changes during development can affect behavioral outcomes in adulthood, but how learning is affected in adults by hormone fluctuations experienced during adulthood is less understood. Previous reports have implicated the sex steroid hormone estradiol (E2) in both male and female vertebrate cognitive functioning. Here, we examined the effects of E2 on auditory recognition and learning in male European starlings (Sturnus vulgaris). European starlings are photoperiodic, seasonally breeding songbirds that undergo different periods of reproductive activity according to annual changes in day length. We simulated these reproductive periods, specifically 1. photosensitivity, 2. photostimulation, and 3. photorefractoriness in captive birds by altering day length. During each period, we manipulated circulating E2 and examined multiple measures of learning. To manipulate circulating E2, we used subcutaneous implants containing either 17-β E2 and/or fadrozole (FAD), a highly specific aromatase inhibitor that suppresses E2 production in the body and the brain, and measured the latency for birds to learn and respond to short, male conspecific song segments (motifs). We report that photostimulated birds given E2 had higher response rates and responded with better accuracy than those given saline controls or FAD. Conversely, photosensitive, animals treated with E2 responded with less accuracy than those given FAD. These results demonstrate how circulating E2 and photoperiod can interact to shape auditory recognition and learning in adults, driving it in opposite directions in different states.
[Show abstract][Hide abstract] ABSTRACT: We examined two measures of immune function (bactericidal capacity of the blood plasma and a pro-inflammatory response to an injection of phytohemagglutinin) and baseline levels of corticosterone in wild adult male Brown-headed Cowbirds (Molothrus ater) to determine whether the size of the song repertoire, a fixed or “static” signal, can be linked to current condition. We hypothesized that static signals and immune function are positively correlated with males' quality because high-quality males should exhibit relatively large sexual signals and also maintain high levels of immune function. In contrast to our primary prediction, we found that song-repertoire size and bactericidal capacity were negatively correlated. We also found that repertoire size and corticosterone levels were positively correlated and that there was no relationship between corticosterone level and either measure of immunity. The positive correlation between corticosterone level and repertoire size suggests that males with larger repertoires expend more energy than do males with smaller repertoires and that the negative correlation between repertoire size and bactericidal capacity is mediated via activity levels, because corticosterone does not appear to suppress immune function directly. If repertoire size indicates a male's quality, these results imply that the level of immune function of high-quality males is not high at all times and that increased energy expenditure related to breeding may draw resources away from immune function.
Examinamos dos medidas de la función inmunológica (capacidad bactericida del plasma sanguíneo y una respuesta pro inflamatoria a una inyección de fitohemaglutinina) y los niveles basales de corticoesterona en machos adultos libres de Molothrus ater para determinar si el tamaño del repertorio de canciones, una señal fija o “estática,” puede estar vinculado a la condición actual. Sugerimos que las señales estáticas y la función inmune se correlacionan positivamente con la calidad del macho, porque los machos de alta calidad deben exhibir grandes señales sexuales y también mantener altos niveles de función inmunológica. En contraste con nuestra predicción inicial, encontramos que el tamaño del repertorio de canciones y la capacidad bactericida se correlacionaron negativamente. También encontramos que el tamaño del repertorio y corticoesterona se correlacionaron positivamente, y que no existe relación entre corticoesterona y cualquier medida de inmunidad. La correlación positiva entre el nivel de corticoesterona y el tamañno del repertorio sugiere que los machos con repertorios más amplios tienen mayor gasto energético que los machos con repertorios más pequeños, y que la correlación negativa entre el tamaño del repertorio y la capacidad bactericida es mediada a través de los niveles de actividad, ya que corticoesterona no parece suprimir directamente la función inmune. Si el tamaño del repertorio indica la calidad del macho, estos resultados implican que el nivel de la función inmune de los machos de alta calidad no es alto en todos los momentos y que el mayor gasto de energía relacionado con la reproducción puede tomar recursos de la función inmune.
The Condor 01/2013; 115(2):434-441. · 1.37 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Over the last decades, the corticosterone stress response has been suggested as a major physiological tool to understand what strategy an individual might adopt in response to environmental perturbations. More recently, another hormone related to parental care - prolactin - has been suggested as a complementary tool to investigate this question. Indeed, both of these hormones are affected by stressors and are involved in parental decisions, such as deserting the nest. Because of these similarities, it remains unclear what the functional distinction between the prolactin and corticosterone stress responses is. Here, we investigated whether natural variations of the corticosterone and prolactin stress responses are functionally linked in free-living Cape petrel (Daption capense) parents. If prolactin and corticosterone mediate the same functional response to a stressor and are the proxies of the same response, we predict that corticosterone and prolactin stress responses (1) will be modulated according to the same factors; (2) will affect reproductive performances in the same way; and, (3) of course, will be correlated. Contrary to these predictions, we found that the corticosterone and prolactin stress responses were respectively modulated according to body condition and breeding status. Moreover, prolactin levels, but not corticosterone levels, were related to hatching success in this species. Finally, we did not find any significant correlation between these two stress responses under any circumstances (failed breeders, incubating or chick rearing birds) and this result was overall supported by a review of the existing literature. Therefore, these two stress responses do not seem to be tightly linked and we believe that they may provide complementary pieces of information on parental investment in birds.
General and Comparative Endocrinology 11/2012; · 2.82 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Songbirds provide rich natural models for studying the relationships between brain anatomy, behavior, environmental signals,
and gene expression. Under the Songbird Neurogenomics Initiative, investigators from 11 laboratories collected brain samples
from six species of songbird under a range of experimental conditions, and 488 of these samples were analyzed systematically
for gene expression by microarray. ANOVA was used to test 32 planned contrasts in the data, revealing the relative impact
of different factors. The brain region from which tissue was taken had the greatest influence on gene expression profile,
affecting the majority of signals measured by 18,848 cDNA spots on the microarray. Social and environmental manipulations
had a highly variable impact, interpreted here as a manifestation of paradoxical “constitutive plasticity” (fewer inducible
genes) during periods of enhanced behavioral responsiveness. Several specific genes were identified that may be important
in the evolution of linkages between environmental signals and behavior. The data were also analyzed using weighted gene coexpression
network analysis, followed by gene ontology analysis. This revealed modules of coexpressed genes that are also enriched for
specific functional annotations, such as “ribosome” (expressed more highly in juvenile brain) and “dopamine metabolic process”
(expressed more highly in striatal song control nucleus area X). These results underscore the complexity of influences on
neural gene expression and provide a resource for studying how these influences are integrated during natural experience.
Proceedings of the National Academy of Sciences 10/2012; 109(Supplement 2):17245-17252. · 9.81 Impact Factor