Intracellular glucocorticoid receptors in spleen,but not skin,vary seasonally in wild house sparrows (Passer domesticus)

Over the short-term and at physiological doses, acute increases in corticosterone (CORT) titres can enhance immune function. There are predictable seasonal patterns in both circulating CORT and immune function across many animal species, but whether CORT receptor density in immune tissues varies seasonally is currently unknown. Using radioligand binding assays, we examined changes in concentrations of glucocorticoid receptors (GR) and mineralocorticoid receptors (MR) in spleen and skin in wild-caught house sparrows in Massachusetts during six different life-history stages: moult, early winter, late winter, pre-egg-laying, breeding and late breeding. Splenic GR and MR binding were highest during the pre-laying period. This may help animals respond to immune threats through increased lymphocyte proliferation and/or an increase in delayed-type hypersensitivity reactions, both of which CORT can stimulate and in which spleen is involved. A decrease in splenic GR and MR during the late breeding period coincides with low baseline and stress-induced CORT, suggesting immune function in spleen may be relatively CORT-independent during this period. We saw no seasonal patterns in GR or MR in skin, suggesting skin''s response to CORT is modulated primarily via changes in circulating CORT titres and/or via local production of CORT in response to wounding and other noxious stimuli.     

Immune and Stress Responses Covary with Melanin-Based Coloration in the Barn Swallow

Eumelanin and pheomelanin are the main endogenous pigments in animals and melanin-based coloration has multiple functions. Melanization is associated with major life-history traits, including immune and stress response, possibly because of pleiotropic effects of genes that control melanogenesis. The net effects on pheo- versus eumelanization and other life-history traits may depend on the antagonistic effects of the genes that trigger the biosynthesis of either melanin form. Covariation between melanin-based pigmentation and fitness traits enforced by pleiotropic genes has major evolutionary implications particularly for socio-sexual communication. However, evidence from non-model organisms in the wild is limited to very few species. Here, we tested the hypothesis that melanin-based coloration of barn swallow (Hirundo rustica) throat and belly feathers covaries with acquired immunity and activation of the hypothalamic–pituitary–adrenal (HPA) axis, as gauged by corticosterone plasma levels. Individuals of both sexes with darker brownish belly feathers had weaker humoral immune response, while darker males had higher circulating corticosterone levels only when parental workload was experimentally reduced. Because color of belly feathers depends on both eu- and pheomelanin, and its darkness decreases with an increase in the concentration of eu- relative to pheomelanin, these results are consistent with our expectation that relatively more eu- than pheomelanized individuals have better immune response and smaller activation of the HPA-axis. Covariation of immune and stress response arose for belly but not throat feather color, suggesting that any function of color as a signal of individual quality or of alternative life-history strategies depends on plumage region.     

Signaling stress? An analysis of phaeomelanin-based plumage color and individual corticosterone levels at two temporal scales in North American barn swallows, Hirundo rustica erythrogaster

Sexually selected traits confer greater reproductive benefits to individuals with more elaborate forms of the signal. However, whether these signals convey reliable information about the physiology underlying trait development remains unknown in many species. The steroid hormone corticosterone (CORT) mediates important physiological and behavioral processes during the vertebrate stress response, and CORT secretion itself can be modulated by melanocortins. Thus, sexually selected melanin-based plumage coloration could function as an honest signal of an individual's ability to respond to stressors. This hypothesis was tested in North American barn swallows, Hirundo rustica erythrogaster, where males with darker ventral plumage color exhibit higher phaeomelanin content and are more successful at reproduction. Because reproductive behavior occurs months after plumage signals are developed, we also addressed the potential temporal disconnect of physiological state during trait development and trait advertisement by analyzing three different measurements of CORT levels in adult males during the breeding season (trait advertisement) and in nestling males while they were growing their feathers (trait development). Variation in adult plumage color did not predict baseline or stress-induced CORT, or stress responsiveness. Likewise, there was no relationship between nestling plumage color and any of the CORT measurements, but heavier nestlings had significantly lower baseline CORT. Our finding that a predominantly phaeomelanin-based trait is unrelated to circulating CORT suggests that phaeomelanin and eumelanin signals may convey different physiological information, and highlights the need for further study on the biochemical links between the hypothalamic–pituitary–adrenal (HPA) axis and the production of different melanin-based pigments.     

Low-quality birds do not display high-quality signals: The cysteine-pheomelanin mechanism of honesty

The mechanisms that make that the costs of producing high-quality signals are unaffordable to low-quality signalers are a current issue in animal communication. The size of the melanin-based bib of male house sparrows Passer domesticus honestly signals quality. We induced the development of new bibs while treating males with buthionine-sulfoximine (BSO), a substance that depletes the levels of the antioxidant glutathione (GSH) and the amino acid cysteine, two elements that switch melanogenesis from eumelanin to pheomelanin. Final bib size is negatively related to pheomelanin levels in the bib feathers. BSO reduced cysteine and GSH levels in all birds, but improved phenotypes (bibs larger than controls) were only expressed by high-quality birds (BSO birds with largest bibs initially). Negative associations between final bib size and cysteine levels in erythrocytes, and between pheomelanin and cysteine levels, were observed in high-quality birds only. These findings suggest that a mechanism uncoupling pheomelanin and cysteine levels may have evolved in low-quality birds to avoid producing bibs of size not corresponding to their quality and greater relative costs. Indeed, greater oxidative stress in cells was not observed in low-quality birds. This may represent the first mechanism maintaining signal honesty without producing greater relative costs on low-quality signalers.     

Contrasting patterns of selection on the size and coloration of a female plumage ornament in common yellowthroats

Females often possess ornaments that appear smaller and duller than homologous traits in males. These ornaments may arise as nonfunctional by‐products of sexual selection in males and cause negative viability or fecundity selection in females in proportion to the cost of their production and maintenance. Alternatively, female ornaments may function as signals of quality that are maintained by sexual or social selection. In a 4‐year study of 83 female common yellowthroats (Geothlypis trichas) and their 222 young, we found strong viability and fecundity selection on the yellow bib, a carotenoid‐based plumage ornament that is a target of sexual selection in males. Females with larger bibs were older, larger and more fecund than females with smaller bibs. However, bib size positively covaried with bib total brightness and carotenoid chroma, aspects of bib coloration that were under negative viability and fecundity selection. Females with more colourful bibs laid fewer eggs in their first clutch, were more likely to suffer total brood loss due to predation and were less likely to return to the study area. Selection against bib coloration limits the value of bib size as a quality indicator in females and may constrain the elaboration of bib attributes in males.     

Dual functions of a melanin-based ornament in the common yellowthroat

Melanin-based ornaments often function as signals in male-male competition, whereas carotenoid-based ornaments appear to be important in female mate choice. This difference in function is thought to occur because carotenoid pigments are more costly to produce than melanins and are thus more reliable indicators of male quality. We examined the role of melanin- and carotenoid-based ornaments in male-male competition and female choice in the common yellowthroat Geothlypis trichas, a sexually dichromatic passerine. Males display a black facial mask produced by melanin pigmentation and a bright yellow bib (throat, breast and belly) produced by carotenoid pigmentation. In controlled aviary experiments, mask size was the best predictor of both male-male competition and female mate choice, and, therefore, mask size may be regarded as an ornament of dual function. These dual functions may help to maintain the reliability of mask size as an indicator of male quality, despite the potentially low cost of production. The size of the bib was unrelated to male-male competition or female choice, but there was a tendency for females to prefer males with more colourful bibs. We propose that the black mask is important in competition for territories with other males and for attracting females. Our results highlight the need for more studies of the mechanisms of sexual selection in species with ornaments composed of different pigment types.     

Corticosteroids and the brain

Mineralocorticoid (MR) and glucocorticoid receptors (GR) are expressed in the central nervous system. Radioligand binding studies, autoradiography, immunocytochemistry and in situ hybridization have shown that MR and GR are found in abundance in neurons of the limbic system (hippocampus), a structure involved in mood, affect and subtle control of the hypothalamic-pituitary-adrenal (HPA) axis. In the hippocampus MR binds corticosterone (CORT) as well as aldosterone (ALDO) with high affinity. MR seems mainly occupied by CORT in the face of its 2-3 order higher circulating concentration. GR binds CORT with a 6-10-fold lower affinity. MR and GR gene expression, as well as the native receptor proteins, seem to be controlled in a coordinative manner. When GR is down-regulated by excess homologous steroid, MR appears to be increased. Down regulation of MR reduces GR as well. MR and GR display a differential ontogenetic pattern. Ontogeny, particularly that of GR, can be permanently influenced when animals are exposed during the first post-natal week of maternal deprivation, handling, CORT or ACTH1-24 injections. These MR and GR changes persist into senescence and have been proposed to result in altered CORT responsiveness, stress regulation, behavioural adaptation and brain aging.     

Anatomical resolution of two types of corticosterone receptor sites in rat brain with in vitro autoradiography and computerized image analysis

The rat brain contains two receptor systems for corticosterone (CORT): the glucocorticoid (GR) and corticosterone or mineralocorticoid-like (CR) receptor sites. We have studied the localization of these receptors by in vitro autoradiography and by in vitro cytosol binding assays in microdissected brain areas. In vitro autoradiography revealed that CR receptor sites are almost entirely restricted to the septal-hippocampal complex, whereas the presence of GR extends throughout the brain. Highest levels of GR are present in the lateral septum, hippocampal, cortical and thalamic regions and the paraventricular nucleus. In vitro determination of binding of 3H-labelled steroids to CR and GR in cytosol of "punched out" brain tissue revealed a similar neuroanatomical distribution as observed with the autoradiographic analysis. In addition, it was found that CORT binds to CR (KD approximately 0.5 nM) with 5-10-fold higher affinity than to GR (KD approximately 2.5-5 nM).     

Geographic variation in the function of ornaments in the common yellowthroat Geothlypis trichas

We used controlled aviary experiments to study the role of male ornaments in male-male competition and female choice in the common yellowthroat Geothlypis trichas , a sexually dichromatic warbler. Previous aviary studies in Wisconsin, USA, indicated that males with larger black facial masks were dominant over males with smaller masks and preferred by females in mate choice experiments. In this study, we replicated those experiments in a population in New York, USA, where male mating success was related more consistently to the size of the yellow bib (throat, breast, and belly) than to the size of the mask. Similar to the study in Wisconsin, we found that males with larger masks were more likely to be dominant in New York, however, we found that males with larger bibs were preferred by females in New York, and there was no significant preference for males with larger masks. These results are consistent with the hypothesis that carotenoid-based ornaments are selected by female choice and melanin-based ornaments are selected by male-male competition. However, the pattern of female choice appears to vary between New York and Wisconsin. This geographic difference could be related to a variety of environmental factors (habitat, carotenoid and parasite abundance) that affect the costs and benefits of choosing males with particular ornaments in each location.     

Age-specific cost of first reproduction in female southern elephant seals

When to commence breeding is a crucial life-history decision that may be the most important determinant of an individual''s lifetime reproductive output and can have major consequences on population dynamics. The age at which individuals first reproduce is an important factor influencing the intensity of potential costs (e.g. reduced survival) involved in the first breeding event. However, quantifying age-related variation in the cost of first reproduction in wild animals remains challenging because of the difficulty in reliably recording the first breeding event. Here, using a multi-event capture–recapture model that accounts for both imperfect detection and uncertainty in the breeding status on an 18-year dataset involving 6637 individuals, we estimated age and state-specific survival of female elephant seals (Mirounga leonina) in the declining Macquarie Island population. We detected a clear cost of first reproduction on survival. This cost was higher for both younger first-time breeders and older first-time breeders compared with females recruiting at age four, the overall mean age at first reproduction. Neither earlier primiparity nor delaying primiparity appear to confer any evolutionary advantage, rather the optimal strategy seems to be to start breeding at a single age, 4 years.     

Breeding phenology and winter activity predict subsequent breeding success in a trans-global migratory seabird

Inter-seasonal events are believed to connect and affect reproductive performance (RP) in animals. However, much remains unknown about such carry-over effects (COEs), in particular how behaviour patterns during highly mobile life-history stages, such as migration, affect RP. To address this question, we measured at-sea behaviour in a long-lived migratory seabird, the Manx shearwater (Puffinus puffinus) and obtained data for individual migration cycles over 5 years, by tracking with geolocator/immersion loggers, along with 6 years of RP data. We found that individual breeding and non-breeding phenology correlated with subsequent RP, with birds hyperactive during winter more likely to fail to reproduce. Furthermore, parental investment during one year influenced breeding success during the next, a COE reflecting the trade-off between current and future RP. Our results suggest that different life-history stages interact to influence RP in the next breeding season, so that behaviour patterns during winter may be important determinants of variation in subsequent fitness among individuals.     

Prenatal exposure to dexamethasone alters hippocampal drive on hypothalamic-pituitary-adrenal axis activity in adult male rats

Glucocorticoids are essential for normal hypothalamic-pituitary-adrenal (HPA) axis activity; however, recent studies warn that exposure to excess endogenous or synthetic glucocorticoid during a specific period of prenatal development adversely affects HPA axis stability. We administered dexamethasone (DEX) to pregnant rats during the last week of gestation and investigated subsequent HPA axis regulation in adult male offspring in unrestrained and restraint-stressed conditions. With the use of real-time PCR and RIA, we examined the expression of regulatory genes in the hippocampus, hypothalamus, and pituitary, including corticotropin-releasing hormone (CRH), arginine vasopressin (AVP), glucocorticoid receptors (GR), mineralcorticoid receptors (MR), and 11-beta-hydroxysteroid dehydrogenase-1 (11beta-HSD-1), as well as the main HPA axis hormones, adrenal corticotropic hormone (ACTH) and corticosterone (CORT). Our results demonstrate that the DEX-exposed group exhibited an overall change in the pattern of gene expression and hormone levels in the unrestrained animals. These changes included an upregulation of CRH in the hypothalamus, a downregulation of MR with a concomitant upregulation of 11beta-HSD-1 in the hippocampus, and an increase in circulating levels of both ACTH and CORT relative to unrestrained control animals. Interestingly, both DEX-exposed and control rats exhibited an increase in pituitary GR mRNA levels following a 1-h recovery from restraint stress; however, the increased expression in DEX-exposed rats was significantly less and was associated with a slower return to baseline CORT compared with controls. In addition, circulating levels of ACTH and CORT as well as hypothalamic CRH and hippocampal 11beta-HSD-1 expression levels were significantly higher in the DEX-exposed group compared with controls following restraint stress. Taken together, these data demonstrate that late-gestation DEX exposure in rats is associated with persistent changes in both the modulation of HPA axis activity and the HPA axis-mediated response to stress.     

Sex of opponent influences response to a potential status signal in house sparrows

We evaluated the possible use of a sexually dimorphic plumage trait as a status signal in inter- and intrasexual social interactions in free-living house sparrows, Passer domesticus. Males with larger black throat patches (bibs) tended to be dominant regardless of the opponent's sex. This relationship was maintained after controlling for body size and age in multivariate analyses. However, the nature of social interactions varied according to the sex of the opponent and a male's bib size. Males with larger bibs tended to be less aggressive to male opponents, and received significantly less aggression from those birds, a key predicted benefit of a status signal. However, when the opponent was a female, males with large bibs displayed significantly more aggression than males with small bibs, and this relationship persisted even after controlling for the dominance status of the participants. Females were significantly more aggressive towards male opponents than towards female opponents, and females interacting with two males of known bib size were more aggressive to the one with the larger bib. These results suggest that the bib of male house sparrows may be a signal of status, but that in interactions with females, the bib may also have other functions. Frequent testing by females of the underlying quality being signalled by the bib may be linked to later mate choice, and might be adaptive if the information value of the bib varies among years. Such testing may also contribute to mechanisms for maintaining the bib as a reliable signal of status. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Individual behaviour in firebugs (Pyrrhocoris apterus)

The concept of animal personalities has recently become of major interest as researchers began to wonder why animals within a given population show consistent behaviour across situations and contexts, what led to the evolution of such behavioural inflexibility and what mechanisms might underlie the phenomenon. A recent model explains individual differences in a population as the result of trade-off between present and future reproduction. We tested this model on the two wing morphs, i.e. short-winged (brachypterous) and long-winged (macropterous) specimens of the firebug (Pyrrhocoris apterus). Since it has been already demonstrated that the two wing morphs differ in their life-history strategies, this species is an ideal subject to test whether the specimens with different life-history strategies have different personalities as well. The results show that individuals behave consistently over time and across contexts, meaning observed bugs do have personalities. We also have found that in females, the two wing morphs have different personalities supporting the theoretical predictions, i.e. winged ones, which are supposed to have lower future reproductive value, are braver and more exploratory. We found no difference between the morphs in males. Differences in reproductive investment might explain this discrepancy between the sexes.     

Multiple behavioral contexts of a melanized tail display in a desert lizard

Conspicuous color displays in animals are often studied in the context of how they communicate an individual's reproductive value, ability to escape capture, or overall health. The study of sexual dichromatism often focuses on the evolution of male display traits balanced between detectability and mate acquisition, representing constraints stemming from both natural and sexual selection. Melanistic coloration and melanin color patterns play important roles in both intraspecific and interspecific signaling in animals; as melanin serves multiple purposes in organismal biology, the evolution of melanin-based visual displays might not be restricted to a single behavioral or ecological context. Here, we examine the behavioral contexts of the conspicuous melanin-based tail display in the greater earless lizard (Cophosaurus texanus), asking if this melanized tail pattern is associated with (a) female association preference of males varying in the concentration of melanin, (b) individual locomotor performance capacity, and (c) thermal ecology. We found the amount of tail melanin is linked with both locomotor performance and female association preference, with greater concentrations of melanin predicting the evolution of faster performance capacities and females preferring males with more discrete melanin bars. We found limited support that differences in melanin are linked with thermoregulation or thermal ecology. Overall, we find that multiple behavioral contexts shape the evolution of this melanized display trait. We conclude that behavioral constraints stemming from both natural and sexual selection can interact synergistically to favor the evolution and expression of a melanistic visual display, even in potentially costly ecological contexts.     

Female Choice for Male Morphological Traits in House Sparrows,Passer domesticus

Female mate choice for male morphological traits was examined in captive house sparrows in New Mexico, USA. A study of house sparrows in Denmark indicated that male bib size is important in female choice (Moller 1988, 1989). To examine this issue further, and to compare the selective pressures on male morphological traits between the two populations, bibs of males were manipulated to one of four standard sizes and females were allowed to choose from four males, one of each bib size. The amount of time the female spent with each male was recorded for 40 trials. Males were then ranked in each trial, with a rank of 4 given to the male the female spent the most time with. The ranks a male obtained were then averaged to provide an indication of a male's attractiveness to females. Data from 23 different males indicated that bib size was not correlated with a male's average rank, even when the effects of other traits were controlled statistically. In addition, the size of the original (unaltered) bib was not correlated with male average rank. Bill depth was the only trait significantly correlated with a male's average rank. Differences in the populations studied or the methodologies used may have led to differences between the results obtained in this study and that of Moller (1988).     

Mediation of a corticosterone-induced reproductive conflict

Current research in birds suggests that a conflict should exist during reproduction for the role of the glucocorticoid corticosterone (CORT). While elevated levels have been correlated with the increased energetic demand of raising offspring, elevated CORT levels have traditionally been implicated in reproductive abandonment. We examined the relationship between CORT and nest desertion in breeding wild female European starlings (Sturnus vulgaris) incorporating analyses of both total circulating levels and 'free', unbound CORT through analysis of corticosteroid-binding globulin (CBG). Free baseline CORT levels of nest-abandoning birds were significantly higher than nonabandoning birds within each stage, with chick-rearing birds exhibiting the highest free baseline CORT levels, while concurrently remaining the most resistant stage to nest desertion. Elevated free baseline CORT levels in chick-rearing birds were not due to increased total CORT secretion, but rather to a decrease in CBG levels. Overall, our results suggest that CORT and CBG interact to play a role in mediating the increased energetic demand of offspring, while minimizing the chances of nest desertion, thereby alleviating any potential behavioral conflict for CORT during reproduction. Furthermore, these results demonstrate that the traditional view of the role of CORT during reproduction is much more complex than previously appreciated. Together with mounting evidence, we suggest that elevated corticosteroid levels are an inherent and necessary part of reproduction in nonmammalian tetrapods.