Does corticosterone regulate the onset of breeding in free-living birds?: The CORT-Flexibility Hypothesis and six potential mechanisms for priming corticosteroid function

For many avian species, the decision to initiate breeding is based on information from a variety of environmental cues, including photoperiod, temperature, food availability, and social interactions. There is evidence that the hormone corticosterone may be involved in delaying the onset of breeding in cases where supplemental cues, such as low food availability and inclement weather, indicate that the environment is not suitable. However, not all studies have found the expected relationships between breeding delays and corticosterone titers. In this review, we present the hypothesis that corticosterone physiology mediates flexibility in breeding initiation (the “CORT-Flexibility Hypothesis”), and propose six possible corticosterone-driven mechanisms in pre-breeding birds that may delay breeding initiation: altering hormone titers, negative feedback regulation, plasma binding globulin concentrations, intracellular receptor concentrations, enzyme activity and interacting hormone systems. Based on the length of the breeding season and species-specific natural history, we also predict variation in corticosterone-regulated pre-breeding flexibility. Although few studies thus far have examined mechanisms beyond plasma hormone titers, the CORT-Flexibility Hypothesis is grounded on a solid foundation of research showing seasonal variation in the physiological stress response and knowledge of physiological mechanisms modulating corticosteroid effects. We propose six possible mechanisms as testable and falsifiable predictions to help clarify the extent of HPA axis regulation of the initiation of breeding.     

Cortisol levels are positively associated with pup-feeding rates in male meerkats

In societies of cooperative vertebrates, individual differences in contributions to offspring care are commonly substantial. Recent attempts to explain the causes of this variation have focused on correlations between contributions to care and the protein hormone prolactin, or the steroid hormone testosterone. However, such studies have seldom considered the importance of other hormones or controlled for non-hormonal factors that are correlative with both individual hormone levels and contributions to care. Using multivariate statistics, we show that hormone levels explain significant variation in contributions to pup-feeding by male meerkats, even after controlling for non-hormonal effects. However, long-term contributions to pup provisioning were significantly and positively correlated with plasma levels of cortisol rather than prolactin, while plasma levels of testosterone were not related to individual patterns of pup-feeding. Furthermore, a playback experiment that used pup begging calls to increase the feeding rates of male helpers gave rise to parallel increases in plasma cortisol levels, whilst prolactin and testosterone levels remained unchanged. Our findings confirm that hormones can explain significant amounts of variation in contributions to offspring feeding, and that cortisol, not prolactin, is the hormone most strongly associated with pup-feeding in cooperative male meerkats.     

Extra‐pair paternity in birds

Since the first molecular study providing evidence for mating outside the pair bond in birds over 30 years ago, >500 studies have reported rates of extra‐pair paternity (EPP) in >300 bird species. Here, we give a detailed overview of the current literature reporting EPP in birds and highlight the sampling biases and patterns in the data set with respect to taxonomy, avian phylogeny and global regions, knowledge of which will be crucial for correct interpretation of results in future comparative studies. Subsequently, we use this comprehensive dataset to simultaneously test the role of several ecological and life history variables. We do not find clear evidence that variation in EPP across socially monogamous species can be explained by latitude, density (coloniality), migration, generation length, genetic structuring (dispersal distance), or climatic variability, after accounting for phylogeny. These results contrast previous studies, most likely due to the large heterogeneity within species in both EPP and the predictor of interest, indicating that using species averages might be unreliable. Despite the absence of broadscale ecological drivers in explaining interspecific variation in EPP, we suggest that certain behaviours and ecological variables might facilitate or constrain EPP, as indicated by our finding that EPP was negatively associated with latitude within noncolonial species, suggesting a role of breeding synchrony. Thus, rather than focussing on general explanations for variation in EPP across all species, a future focus should be on how various aspects of ecology or life history might have driven variation in EPP among groups of species or populations of the same species. Hence, we argue that variation in EPP can be partly explained when taking the right perspective. This comprehensive overview, and particularly the dataset provided herein will create a foundation for further studies.     

Sources of individual variation in plasma testosterone levels

The steroid hormone testosterone (T) plays a central role in the regulation of breeding in males, because many physiological, morphological and behavioural traits related to reproduction are T dependent. Moreover, in many seasonally breeding vertebrates, male plasma T levels typically show a pronounced peak during the breeding season. While such population-level patterns are fairly well worked out, the sources and the implications of the large variability in individual T levels within the seasonal cycle remain surprisingly little understood. Understanding the potential sources of individual variation in T levels is important for behavioural and evolutionary ecologists, for at least two reasons. First, in 'honest signalling' theory, T is hypothesized to play a critical role as the assumed factor that enforces honesty of the expression of sexually selected quality indicators. Second, T is often considered a key mediator of central life-history trade-offs, such as investment in survival versus reproduction or in mating versus parental care. Here, we discuss the patterns of within- and between-individual variation in male plasma T levels in free-living populations of birds. We argue that it is unclear whether this variability mainly reflects differences in underlying individual quality (intrinsic factors such as genetic or maternal effects) or in the environment (extrinsic factors including time of day, individual territorial status and past experience). Research in avian behavioural endocrinology has mainly focused on the effects of extrinsic factors, while other sources of variance are often ignored. We suggest that studies that use an integrative approach and investigate the relative importance of all potential sources of variation are essential for the interpretation of data on individual plasma T levels.     

Genetic variation in the C-terminal domain of arginine vasotocin receptor in avian species

Arginine vasotocin (AVT) is a neurohypophysial hormone that plays an essential role in various social behaviours. We investigated the degree of polymorphisms in the C-terminal domain of the AVT V2-type receptor (AVT2R) among avian species to determine the mechanism by which genetic polymorphisms in the neuropeptide receptor may contribute to different levels of signal transduction. In passerine birds, AVT2R was characterised by 2 variable regions, both of which were managed by insertion/deletion (indel); however, indels were rarely found in other avian taxa. The presence or absence of deletions in passerines largely affected the properties of the predicted palmitoylation sites at the proximal part of the C-terminal tail. Moreover, we detected intraspecific polymorphisms in estrildid finches based on the number of tri-amino acid (GHQ/EHQ/EHR) repeats in another variable region. Our results indicate that amino acid substitutions and length variation at the C-terminus may impact subsequent signal transduction and affect behavioural traits in wild birds.     

Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them?

Over the past decade, birds have proven to be excellent models to study hormone-mediated maternal effects in an evolutionary framework. Almost all these studies focus on the function of maternal steroid hormones for offspring development, but lack of knowledge about the underlying mechanisms hampers further progress. We discuss several hypotheses concerning these mechanisms, point out their relevance for ecological and evolutionary interpretations, and review the relevant data. We first examine whether maternal hormones can accumulate in the egg independently of changes in hormone concentrations in the maternal circulation. This is important for Darwinian selection and female physiological trade-offs, and possible mechanisms for hormone accumulation in the egg, which may differ among hormones, are reviewed. Although independent regulation of plasma and yolk concentrations of hormones is conceivable, the data are as yet inconclusive for ovarian hormones. Next, we discuss embryonic utilization of maternal steroids, since enzyme and receptor systems in the embryo may have coevolved with maternal effect mechanisms in the mother. We consider dose-response relationships and action pathways of androgens and argue that these considerations may help to explain the apparent lack of interference of maternal steroids with sexual differentiation. Finally, we discuss mechanisms underlying the pleiotropic actions of maternal steroids, since linked effects may influence the coevolution of parent and offspring traits, owing to their role in the mediation of physiological trade-offs. Possible mechanisms here are interactions with other hormonal systems in the embryo. We urge endocrinologists to embark on suggested mechanistic studies and behavioural ecologists to adjust their interpretations to accommodate the current knowledge of mechanisms.     

Evolving the neuroendocrine physiology of human and primate cooperation and collective action

While many hormones play vital roles in facilitating or reinforcing cooperative behaviour, the neurohormones underlying competitive and cooperative behaviours are largely conserved across all mammals. This raises the question of how endocrine mechanisms have been shaped by selection to produce different levels of cooperation in different species. Multiple components of endocrine physiology—from baseline hormone concentrations, to binding proteins, to the receptor sensitivity and specificity—can evolve independently and be impacted by current socio-ecological conditions or individual status, thus potentially generating a wide range of variation within and between species. Here, we highlight several neurohormones and variation in hormone receptor genes associated with cooperation, focusing on the role of oxytocin and testosterone in contexts ranging from parenting and pair-bonding to reciprocity and territorial defence. While the studies reviewed herein describe the current state of the literature with regard to hormonal modulators of cooperation and collective action, there is still a paucity of research on hormonal mechanisms that help facilitate large-scale collective action. We end by discussing several potential areas for future research.     

Interspecific variation in dietary carotenoid assimilation in birds: links to phylogeny and color ornamentation

Many birds use carotenoid pigments to acquire rich red, orange, and yellow coloration in feathers and bare parts that is used as a signal of mate quality. Because carotenoids are derived from foods, much attention has been paid to the role of diet in generating color variation both within and among avian species. Less consideration has been given to physiological underpinnings of color variability, especially among species. Here, I surveyed published literature (e.g. captive feeding studies) on carotenoid assimilation in six bird species and completed additional controlled carotenoid-supplementation experiments in two others to consider the ability of different taxa to extract carotenoids from the diet in relation to phylogeny and coloration. I found that, for a given level of carotenoids in the diet, passerine birds (zebra finch, Taeniopygia guttata; house finch, Carpodacus mexicanus; American goldfinch, Carduelis tristis; society finch, Lonchura domestica) exhibit higher levels of carotenoids in circulation than non-passerines like gamebirds (domestic chicken, Gallus domesticus; red junglefowl, Gallus gallus; Japanese quail, Coturnix coturnix; red-legged partridge, Alectoris rufa). This difference in carotenoid accumulation is likely due to interspecific variation in micelle, chylomicron, or lipoprotein concentrations or affinities for xanthophyll carotenoids. Passerine birds more commonly develop carotenoid-based colors than do birds from ancient avian lineages such as Galliformes, and the physiological differences I uncover may explain why songbirds especially capitalize on carotenoid pigments for color production. Ultimately, because we can deconstruct color traits into component biochemical, physical, and physiological parts, avian color signals may serve as a valuable model for illuminating the proximate mechanisms behind interspecific variation in signal use in animals.     

Plasma carotenoid concentrations of incubating American kestrels (Falco sparverius) show annual,seasonal, and individual variation and explain reproductive outcome

In wild birds, the proximate and ultimate factors that affect circulating carotenoid concentrations remain poorly understood. We studied variation in plasma carotenoid concentrations across several scales: annual, seasonal, pair, territory and individual, and evaluated whether plasma carotenoid concentrations explained reproductive outcome of wild American kestrels (Falco sparverius). We sampled plasma carotenoid concentrations of 99 female and 80 male incubating kestrels from April to June in 2008 to 2012. Plasma carotenoid concentrations were explained by an interaction between year and sex, date, and random effects for pair and individual identity. In general, plasma carotenoid concentrations of males were significantly higher than females, but this depended on year. Within a breeding season, earlier nesting kestrels had higher carotenoid concentrations than later nesting kestrels, a pattern that is coincident with seasonal trends in local fitness. Pair and individual identity explained variation in carotenoid concentrations suggesting that carotenoid concentrations of mated birds were correlated, and some individuals consistently maintained higher carotenoid levels than others. Male carotenoid concentrations were positively associated with number of young fledged per pair. These results are consistent with the hypothesis that higher quality individuals have higher carotenoid levels compared to lower quality individuals, despite annual variations in carotenoid availability.     

Differential initiation of translation of a single estrogen receptor mRNA could explain some estradiol resistance cases.

Cell response to steroid stimulation is generally acknowledged to be mediated by an intracellular protein known as a receptor. Response intensity is related to the affinity of the receptor and to the number of sites occupied by its specific ligand. Although verified in the majority of experimental and clinical studies, certain phenomena of steroid hormone resistance would seem to challenge this assertion. Application of gene molecular biology to determine the action mechanisms of steroid hormones has partially explained cell resistance in terms of genetic modifications. The work presented here shows that in certain cases, estrogen resistance could be explained by regulation of translation of the single messenger RNA coding for the receptor.     

鸟类社会行为中的嗅觉通讯研究进展

长期以来, 学者普遍认为大多数鸟类的嗅觉能力较弱或丧失。早期实验未能得到统一而清晰的结果, 进一步扩大了这一认知误区。随着研究手段和技术的发展, 解剖学、电生理学、分子生物学和行为生态学等学科提供了鸟类嗅觉存在的证据。目前, 相关研究在鸟类14目33科中发现了嗅觉通讯的证据。与视觉和听觉一样, 这一感觉通路可能在鸟类的觅食、导航、防御、隐蔽、警戒和交流等社会行为中发挥着重要作用。本文着重于嗅觉通讯在鸟类社会行为中的功能, 通过回顾近十年的相关研究, 综述鸟类嗅觉在物种和个体识别、繁殖行为、亲缘识别、配偶选择与竞争等方面发挥的作用。我们也指出: 研究手段的创新将揭示更多鸟类物种在社会行为中对于嗅觉通讯的运用。此外, 当前研究多聚焦于少数物种和单一层面(如生理、生态和环境等), 使用分子生物学、解剖与生理学、行为学和神经生物学手段的整合研究较为缺乏; 而后者更有可能全面地揭示鸟类嗅觉通讯的复杂机理及其在社会行为中发挥的多种功能。     

Phenotypic plasticity in the scaling of avian basal metabolic rate

Many birds exhibit short-term, reversible adjustments in basal metabolic rate (BMR), but the overall contribution of phenotypic plasticity to avian metabolic diversity remains unclear. The available BMR data include estimates from birds living in natural environments and captive-raised birds in more homogenous, artificial environments. All previous analyses of interspecific variation in BMR have pooled these data. We hypothesized that phenotypic plasticity is an important contributor to interspecific variation in avian BMR, and that captive-raised populations exhibit general differences in BMR compared to wild-caught populations. We tested this hypothesis by fitting general linear models to BMR data for 231 bird species, using the generalized least-squares approach to correct for phylogenetic relatedness when necessary. The scaling exponent relating BMR to body mass in captive-raised birds (0.670) was significantly shallower than in wild-caught birds (0.744). The differences in metabolic scaling between captive-raised and wild-caught birds persisted when migratory tendency and habitat aridity were controlled for. Our results reveal that phenotypic plasticity is a major contributor to avian interspecific metabolic variation. The finding that metabolic scaling in birds is partly determined by environmental factors provides further support for models that predict variation in scaling exponents, such as the allometric cascade model.     

Neural sensitivity to sex steroids predicts individual differences in aggression: implications for behavioural evolution

Testosterone (T) regulates many traits related to fitness, including aggression. However, individual variation in aggressiveness does not always relate to circulating T, suggesting that behavioural variation may be more closely related to neural sensitivity to steroids, though this issue remains unresolved. To assess the relative importance of circulating T and neural steroid sensitivity in predicting behaviour, we measured aggressiveness during staged intrusions in free-living male and female dark-eyed juncos (Junco hyemalis). We compared aggressiveness to plasma T levels and to the abundance of androgen receptor (AR), aromatase (AROM) and oestrogen receptor alpha (ORα) mRNA in behaviourally relevant brain areas (avian medial amygdala, hypothalamus and song control regions). We also asked whether patterns of covariation among behaviour and endocrine parameters differed in males and females, anticipating that circulating T may be a better predictor of behaviour in males than in females. We found that circulating T related to aggressiveness only in males, but that gene expression for ORα, AR and AROM covaried with individual differences in aggressiveness in both sexes. These findings are among the first to show that individual variation in neural gene expression for three major sex steroid-processing molecules predicts individual variation in aggressiveness in both sexes in nature. The results have broad implications for our understanding of the mechanisms by which aggressive behaviour may evolve.     

Geographic range size and evolutionary age in birds

Together with patterns of speciation and extinction, post-speciation transformations in the range sizes of individual species determine the form of contemporary species range-size distributions. However, the methodological problems associated with tracking the dynamics of a species' range size over evolutionary time have precluded direct study of such range-size transformations, although indirect evidence has led to several models being proposed describing the form that they might take. Here, we use independently derived molecular data to estimate ages of species in six monophyletic groups of birds, and examine the relationship between species age and global geographic range size. We present strong evidence that avian range sizes are not static over evolutionary time. In addition, it seems that, with the regular exception of certain taxa (for example island endemics and some threatened species), range-size transformations are non-random in birds. In general, range sizes appear to expand relatively rapidly post speciation; subsequently; and perhaps more gradually, they then decline as species age. We discuss these results with reference to the various models of range-size dynamics that have been proposed.     

No sex difference in yolk steroid concentrations of avian eggs at laying

Yolk steroids of maternal origin have been proposed to influence genetic sex determination in birds, based on sex differences in yolk steroid concentrations of peafowl eggs incubated for 10 days. More recent reports dispute this proposal, as yolk steroids in eggs incubated for 3 days do not show such sex differences. To date, research examining this phenomenon has only analysed incubated eggs, although sex in avian species is determined before incubation begins. This may be a serious methodological flaw because incubation probably affects yolk steroid concentrations. Therefore, we investigated sex differences in yolk steroid concentrations of unincubated avian eggs. We withdrew yolk for steroid analysis from fresh, unincubated Japanese quail (Coturnix japonica) eggs by biopsy, and then incubated those eggs for 10 days, after which we harvested the embryonic material for genetic sexing and the incubated yolk for further steroid analysis. We found no sex differences in fresh Japanese quail eggs; however, sex differences were apparent in yolk steroids by day 10 of incubation, when female eggs had significantly more oestrogen in relation to androgen than male eggs. Concentrations of all yolk androgens decreased dramatically between laying and day 10 of incubation, whereas oestradiol (E2) concentrations increased marginally. Thus, yolk concentrations of androgens and E2 do not appear critical for avian sex determination.     

Exogenous and endogenous corticosterone in feathers

In birds, the steroid hormone corticosterone (CORT) increases in response to real or perceived threats to homeostasis. A long‐term record of CORT exposure is recorded in feathers when the hormone is incorporated into the keratinized tissue, and then preserved when the mature feather is cut off from the blood supply. The opportunity to retrospectively assess the exposure of an individual to stressors by measuring the amount of CORT in a feather has generated excitement amongst avian ecologists. However, this technique is relatively new and requires additional validations. In this study, we performed experiments in wild caught European starlings Sturnus vulgaris to test whether: 1) CORT deposition in the feather depends on time of day and 2) whether an ecologically relevant stressor (unpredictable food access) causes a change in feather CORT. We found that exogenous CORT was incorporated into feathers during the day and the night. However, there was no difference in feather CORT between birds with unpredictable access to food and those with continuous access, indicating that feather CORT might not always detect ecologically relevant stressors.     

POTENTIAL MECHANISMS FOR SEX RATIO ADJUSTMENT IN MAMMALS AND BIRDS

Sex ratio skews in relation to a variety of environmental or parental conditions have frequently been reported among mammals and, though less commonly, among birds. However, the adaptive significance of such sex ratio variation remains unclear. This has, in part, been attributed to the absence of a low-cost physiological mechanism for sex ratio manipulation by the parent. It is shown here that several recent findings in reproductive biology are suggestive of many potential pathways by which gonadotropins and steroid hormones could interfere with the sex ratio at birth. And these hormone levels are well-known to be influenced by many parameters which have been invoked in correlating with offspring sex ratios. Hence, it is argued that the significant, but inconsistent sex ratio biases reported in mammalian and avian populations are coherent with current knowledge on reproductive physiology in those species. However, whether such variations can be viewed at as a consequence of physiological constraint or as adaptive sex ratio adjustment, has still to be determined.     

Minireview: the intersection of steroid receptors with molecular chaperones: observations and questions

An involvement of molecular chaperones in the action and well-being of steroid receptors was recognized early in the molecular era of hormone research. However, this has continued to be a topic of much enquiry and some confusion. All steroid receptors associate with heat shock protein 90, the main character of a series of multiprotein chaperone complexes generally referred to as the "heat shock protein 90 chaperoning machine." Receptor association with chaperones occurs in an ordered, step-wise fashion and is necessary for the maintenance of unliganded receptor in a state ready to bind and respond to hormone. Chaperones additionally modulate how receptors respond to hormone and activate target genes. Although much is known about the participants in this chaperoning process and the consequences of chaperoning, many key questions remain unanswered, particularly those concerning molecular mechanisms, cellular dynamics, and the functions of an array of cochaperone proteins. Here, we point out several areas in need of investigation to encourage new ideas and participants in this burgeoning field.     

鸟类羽色多态现象：概念及其进化机制假说

多态现象对了解物种的遗传、变异和进化有着重要意义,鸟类羽色多态现象的进化机制,是多态现象研究中非常重要的内容。鸟类羽色多态现象的进化机制假说主要有：分化选择假说、异类选择假说和非随机性交配假说等。本文对鸟类羽色多态现象的概念和以上进化机制假说进行了综述,并针对鸟类羽色多态现象进化机制研究中存在争议的问题及研究的不足提出了自己的看法。