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In many cooperatively breeding societies non-breeding individuals help to rear the offspring of breeders. The physiological mechanisms that regulate such cooperative helping behavior are poorly understood, but may have been co-opted, during the evolution of cooperative breeding, from pre-existing mechanisms that regulated parental care. Key among these may be a role for prolactin. Here we investigate whether natural variation in circulating prolactin levels predicts both parental and helper contributions to nestling provisioning in cooperatively breeding white-browed sparrow weavers,Plocepasser mahali. In sparrow weaver groups, a single dominant pair monopolize reproduction and non-breeding subordinates help with nestling feeding. We show that: (i) among parents, dominant females feed nestlings at higher rates, make longer provisioning visits and have higher prolactin levels than dominant males; and (ii) among subordinates, engaged in cooperative helping behavior, those within their natal groups feed nestlings at higher rates and have higher prolactin levels than immigrants. Moreover, continuous variation in prolactin levels positively predicts nestling-provisioning rates and mean provisioning visit durations when all bird classes are combined. These relationships are principally driven by differences among bird classes in both circulating prolactin levels and provisioning traits; the more limited within-class variation in prolactin and provisioning traits were not evidently correlated, highlighting a likely role for additional mechanisms in the fine-scale regulation of care. Our findings broadly support the hypothesis that parental care and cooperative helping behavior are regulated by a common underlying mechanism and highlight the need for experimentation to now establish the causality of any role for prolactin.

Across taxa, the seasonal transition between non-breeding and breeding states is controlled by localised thyroid hormone signalling in the deep brain via reciprocal switching of deiodinase enzyme expression from type 3 (DIO3) to type 2 (DIO2). This reciprocal switch is considered to be mediated by increasing thyroid-stimulating hormone β (TSHβ) release from the pars tuberalis, which occurs in response to a change in photoperiod. Although well characterised in a handful of model organisms in controlled laboratory settings, this pathway remains largely unexplored in free-living animals under natural environmental conditions. In this comparative gene expression study, we investigated hypothalamic thyroid hormone signalling in two seasonally breeding subspecies of white-crowned sparrow (Zonotrichia leucophrys), across the entirety of their annual cycles. The migratory Gambel's (Z. l. gambelii) and resident Nuttall's (Z. l. nuttalii) subspecies differ with respect to timing of reproduction, as well as life history stage and migratory strategies. Although DIO3 mRNA expression was elevated and DIO2 mRNA expression was reduced in the wintering period in both subspecies, DIO2 peaked in both subspecies prior to the onset of reproduction. However, there was differential timing between subspecies in peak DIO2 expression. Intriguingly, seasonal modulation of TSHβ mRNA was only observed in migrants, where expression was elevated at the start of breeding, consistent with observations from other highly photoperiodic species. There was no correlation between TSHβ, DIO2 and gonadotropin-releasing hormone-I mRNA or reproductive metrics in residents. Based on these observed differences, we discuss potential implications for our understanding of how changes in medial basal hypothalamic gene expression mediates initiation of seasonal reproduction.

It has been over 20 years since the first scientific papers on rat tickling were published (1, 2). Rats were found to emit ultrasonic vocalizations in the 50-kHz range (hereafter referred to as USVs) when a human performed rapid manual stimulation on their dorsoventral region. Such tickling of rats by a human hand is trying to imitate the rough-and-tumble play seen in young rats of both sexes (3, 4). Emission of USVs by the rat indicates that it enjoys being tickled (5–7), as USVs have been linked with positive emotions (8, 9), are emitted in anticipation of, and during, social play (10, 11), and have been suggested to be homologous to human laughter (12). To date, more than 70 scientific articles on rat tickling have been published1, and the consensus is that tickling induces positive emotions in rats. Indeed, in a systematic review, LaFollette et al. (13) found that tickling increased USVs and human hand approach behavior, and decreased measures of anxiety in rats. In this Opinion paper, we consider whether current methods of tickling overemphasize the use of pinning (Figure 1) to which there may be a wider response variation than commonly acknowledged. We do not dispute that tickling can be a positive way to handle juvenile rats, but tickling may not always be perceived as a positive interaction by the rat, and we raise the possibility that tickling methods need to be revised. In particular, we suggest incorporating more aspects of play during tickling (increased diversity) and adapting the method to individual rats' responses (increased flexibility) to achieve positive emotions and increased welfare across a wider cohort of rats. Open in a separate window Figure 1 (A) Pinning is a component of social play in rats, where one rat has its dorsal surface pinned to the ground, while the other rat is in a dominant posture above. (B,C) Pinning has become the main component of the methodology used when tickling rats, as it elicits 50-kHz ultrasonic vocalizations (USVs). Pinning has been used in the past as a means to quantify rough-and-tumble play between rats (14). However, rough-and-tumble play is much more than just pinning, and USVs during pinning are frequent when being tickled by a human (1), but less so when being pinned during play (10, 15). Drawings are by Tayla J. Hammond.

A species’ success during the invasion of new areas hinges on an interplay between demographic processes and the outcome of localized selection. Invasive European Starlings (Sturnus vulgaris) established populations in Australia and North America in the 19th century. Here, we compare whole-genome sequences among native and independently introduced European Starling populations from three continents to determine how demographic processes interact with rapid adaptive evolution to generate similar genetic patterns in these recent and replicated invasions. Our results confirm that a post-bottleneck expansion may in fact support local adaptation. We find that specific genomic regions have differentiated even on this short evolutionary timescale, and suggest that selection best explains differentiation in at least two of these regions. This infamous and highly mobile invader adapted to novel selection (e.g., extrinsic factors), perhaps in part due to the demographic boom intrinsic to many invasions.

The role of maternal investment in avian offspring has considerable life history implications on production traits and therefore potential for the poultry industry. A first generation (G1) of Japanese quail (Coturnix japonica) were bred from a 2 × 2 factorial design. Parents were fed either a control or methyl-enhanced (HiBET) diet, and their eggs were treated with a vehicle or corticosterone injection during day 5 of incubation. A subset of G1 birds were subjected to an open field trial (OFT) and capture-restraint stress protocol. Significant effects of HiBET diet were found on parental egg and liver weights, G1 hatch, liver and female reproductive tract weights, egg productivity, latency to leave the OFT central zone, male baseline 11-dehydrocorticosterone, and female androstenedione plasma concentrations. In ovo treatment significantly affected latency to return to the OFT, male baseline testosterone and androstenedione, and change in androstenedione plasma concentration. Diet by treatment interactions were significant for G1 liver weight and male baseline plasma concentrations of corticosterone. These novel findings suggest significant positive effects on reproduction, growth, precociousness, and hypothalamic–pituitary–adrenal axis function from enhanced methyl diets, and are important in understanding how in ovo stressors (representing maternal stress), affect the first offspring generation.

The European starling, Sturnus vulgaris, is an ecologically significant, globally invasive avian species that is also suffering from a major decline in its native range. Here, we present the genome assembly and long-read transcriptome of an Australian-sourced European starling (S. vulgaris vAU), and a second North American genome (S. vulgaris vNA), as complementary reference genomes for population genetic and evolutionary characterisation. S. vulgaris vAU combined 10x Genomics linked-reads, low-coverage Nanopore sequencing, and PacBio Iso-Seq full-length transcript scaffolding to generate a 1050 Mb assembly on 1,628 scaffolds (72.5 Mb scaffold N50). Species-specific transcript mapping and gene annotation revealed high structural and functional completeness (94.6% BUSCO completeness). Further scaffolding against the high-quality zebra finch (Taeniopygia guttata) genome assigned 98.6% of the assembly to 32 putative nuclear chromosome scaffolds. Rapid, recent advances in sequencing technologies and bioinformatics software have highlighted the need for evidence-based assessment of assembly decisions on a case-by-case basis. Using S. vulgaris vAU, we demonstrate how the multifunctional use of PacBio Iso-Seq transcript data and complementary homology-based annotation of sequential assembly steps (assessed using a new tool, SAAGA) can be used to assess, inform, and validate assembly workflow decisions. We also highlight some counter-intuitive behaviour in traditional BUSCO metrics, and present Buscomp, a complementary tool for assembly comparison designed to be robust to differences in assembly size and base-calling quality. Finally, we present a second starling assembly, S. vulgaris vNA, to facilitate comparative analysis and global genomic research on this ecologically important species.

BackgroundThe Japanese quail (Coturnix japonica) is a popular domestic poultry species and an increasingly significant model species in avian developmental, behavioural and disease research.ResultsWe have produced a high-quality quail genome sequence, spanning 0.93 Gb assigned to 33 chromosomes. In terms of contiguity, assembly statistics, gene content and chromosomal organisation, the quail genome shows high similarity to the chicken genome. We demonstrate the utility of this genome through three diverse applications. First, we identify selection signatures and candidate genes associated with social behaviour in the quail genome, an important agricultural and domestication trait. Second, we investigate the effects and interaction of photoperiod and temperature on the transcriptome of the quail medial basal hypothalamus, revealing key mechanisms of photoperiodism. Finally, we investigate the response of quail to H5N1 influenza infection. In quail lung, many critical immune genes and pathways were downregulated after H5N1 infection, and this may be key to the susceptibility of quail to H5N1.ConclusionsWe have produced a high-quality genome of the quail which will facilitate further studies into diverse research questions using the quail as a model avian species.

The annual photoperiod cycle provides the critical environmental cue synchronizing rhythms of life in seasonal habitats. In 1936, Bünning proposed a circadian-based coincidence timer for photoperiodic synchronization in plants. Formal studies support the universality of this so-called coincidence timer, but we lack understanding of the mechanisms involved. Here we show in mammals that long photoperiods induce the circadian transcription factor BMAL2, in the pars tuberalis of the pituitary, and triggers summer biology through the eyes absent/thyrotrophin (EYA3/TSH) pathway. Conversely, long-duration melatonin signals on short photoperiods induce circadian repressors including DEC1, suppressing BMAL2 and the EYA3/TSH pathway, triggering winter biology. These actions are associated with progressive genome-wide changes in chromatin state, elaborating the effect of the circadian coincidence timer. Hence, circadian clock-pituitary epigenetic pathway interactions form the basis of the mammalian coincidence timer mechanism. Our results constitute a blueprint for circadian-based seasonal timekeeping in vertebrates., “Life in a seasonal environment requires appropriate timing of physiological changes to survive, but how the circadian clockwork times these changes remains unclear. Here the authors show that the circadian clock genes BMAL2 and DEC1, in concert with epigenetic pathways in the pituitary, have a central role in seasonal timekeeping in mammals.”

SDH thanks SICB for financial support and the work described here was conducted with the support of EASTBIO DTP from the Biotechnology and Biological Sciences Research Council (BBSRC, to SE), the School of Biology and NSERC (to ZJH), MARIE CURIE (Ares(2016)5869884 to EI), and BBSRC Roslin Institute strategic grant funding (BB/P013759/1, to SLM). EN was supported by the Erasmus Plus student exchange program to SLM. Nest building consists of a series of motor actions, which are concomitant with activity in regions of the anterior motor pathway, the social behaviour network and the reward circuity in nest building adult male zebra finches (Taeniopygia guttata). It is not clear, however, whether this activity is due to nest building, collection and/or manipulation of nest material. To identify which areas of the brain are specifically involved, we used immunohistochemistry to quantify the immediate early gene c-fos in male zebra finches that were nest building (Building), birds given a nestbox but could interact only with tied down nest material (Fixed), and birds that were not given a nestbox or nest material (Control). We investigated the following brain regions: the anterior motor pathway (anterior ventral mesopallium (AMV), anterior nidopallium (AN), anterior striatium (ASt)), areas of the social behaviour network (bed nucleus of the stria terminalis, dorsomedial sub division (BSTmd), lateral septum (LS)), the dopaminergic reward circuitry (ventral tegmental area (VTA)) and the cerebellum. We found that there was greater Fos-ir expression in the BSTmd, LS and AMV with increased material deposition; in LS, AMV ASt and folia VI with increased material carrying; in LS, AMV and ASt with increased nest material tucking; and in LS and all folia (except folium VIII) with increased tugging at tied down material. These data confirm a functional role for areas of the anterior motor pathway, social behaviour network and the cerebellum in nest material collection and manipulation by birds Postprint

The extreme climatic conditions (ECCs) of the Qinghai-Tibet Plateau impose strong selective pressures on the evolution of phenotypic traits in free-living animals. It is not well understood how animals on the Qinghai-Tibet Plateau modify their adrenocortical functions in response to both predictable and unpredictable events of ECCs, especially when the available resources are lowest during the wintering life-history stage. To uncover potential physiological mechanisms, we studied the life history stage dependent features of morphology, the plasma corticosterone response to acute stress and brain glucocorticoid receptor (GR) and mineralocorticoid receptor (MR) mRNA expression in two sympatric snow finches: the white-rumped snow finch (Onychostruthus taczanowskii, WRSF); and the rufous-necked snow finch, Pyrgilauda ruficollis, RNSF) in Qinghai Province, China. Our results showed that (a) baseline corticosterone and stressor-induced corticosterone levels significantly varied with life history stage, but not between the species; (b) in WRSF, GR mRNA expression in the paraventricular nucleus was higher in the wintering stage compared to the pre-basic molt stage. There were no differences in hippocampus MR mRNA expression between stages in either species; (c) in the wintering stage, the suppression of corticosterone secretion in both species was an unexpected strategy in free-living animals. Both convergent and divergent phenotypic traits of adrenocortical responses to acute stress in two sympatric snow finches contribute to our understanding of the coping mechanisms of closely related species in the severe winter on the Qinghai-Tibet Plateau.

The social environment changes circulating hormone levels and expression of social behavior in animals. Social information is perceived by sensory systems, leading to cellular and molecular changes through neural processes. Peripheral reproductive hormone levels are regulated by activity in the hypothalamic-pituitary-gonadal (HPG) axis. Until the end of the last century, the neurochemical systems that convey social information to the HPG axis were not well understood. Gonadotropin-inhibitory hormone (GnIH) was the first hypothalamic neuropeptide shown to inhibit gonadotropin release, in 2000. GnIH is now regarded as a negative upstream regulator of the HPG axis, and it is becoming increasingly evident that it responds to social cues. In addition to controlling reproductive physiology, GnIH seems to modulate the reproductive behavior of animals. Here, we review studies investigating how GnIH neurons respond to social information and describe the mechanisms through which GnIH regulates social behavior.

Male Japanese quail produce high-frequency crow vocalizations to attract females during the breeding season. The nucleus of intercollicularis (ICo) is the midbrain vocal center in birds and electrical stimulation of the ICo produces calls that include crowing. Noradrenaline plays a significant role in sexual behavior but the contribution of noradrenaline in the control of courtship vocalizations in quail has not been well established. Using dose-dependent intracerebroventricular injection of clonidine, an α2-adrenergic receptor- specific agonist, crowing vocalization was immediately suppressed. At the same time as crow suppression by clonidine there was a reduction of immediate early gene, zenk mRNA, in the ICo; no zenk mRNA expression was detected in the dorsomedial division of the nucleus. Using histochemistry, we determined that the ICo receives noradrenergic innervation and expresses α2A-adrenergic receptor mRNA. Taken together, these data suggest that noradrenaline regulates courtship vocalization in quail, possibly via the alpha2A- adrenergic receptor expressed on ICo neurons.

Organisms need to time their annual-cycle stages, like breeding and migration, to occur at the right time of the year. Climate change has shifted the timing of annual-cycle stages at different rates, thereby tightening or lifting time constraints of these annual-cycle stages, a rarely studied consequence of climate change. The degree to which these constraints are affected by climate change depends on whether consecutive stages are causally linked (scenario I) or whether the timing of each stage is independent of other stages (scenario II). Under scenario I, a change in timing in one stage has knock-on timing effects on subsequent stages, whereas under scenario II, a shift in the timing of one stage affects the degree of overlap with previous and subsequent stages. To test this, we combined field manipulations, captivity measurements and geolocation data. We advanced and delayed hatching dates in pied flycatchers (Ficedula hypoleuca) and measured how the timing of subsequent stages (male moult and migration) were affected. There was no causal effect of manipulated hatching dates on the onset of moult and departure to Africa. Thus, advancing hatching dates reduced the male moult-breeding overlap with no effect on the moult-migration interval. Interestingly, the wintering location of delayed males was more westwards, suggesting that delaying the termination of breeding carries over to winter location. Because we found no causal linkage of the timing of annual-cycle stages, climate change could shift these stages at different rates, with the risk that the time available for some becomes so short that this will have major fitness consequences.

Neuroendocrine mechanisms control the seasonal reproduction in birds and mammals. Seasonal reproduction is ubiquitous across vertebrate and invertebrate species, and its timing is extremely crucial in order to maximize offspring survival. The hypothalamus is the key brain region that integrates environmental cues. An endogenous circannual timer with oscillations that approximate one year is also localized in the hypothalamus. Successful timing of reproduction involves the combination of endogenous internal timers that are entrained by local environmental cues. Photoperiod, or the annual change in day length, is the primary cue most temperate animals use to predict future environmental conditions. Birds are able to detect light through photoreceptors located in the medio-basal hypothalamus. These photoreceptors are localized in neuroendocrine regions and regulate the key reproductive neuropeptide gonadotropin-releasing hormone (GnRH). In mammals, retinal photoreceptors transduce light information the suprachiasmatic nucleus in the hypothalamus, which then modulates the nocturnal duration of melatonin. Melatonin in mammals is crucial, as it regulates the neuroendocrine release of GnRH and downstream transitions across seasonal reproductive states. The tanycyte cells lining the third ventricle (3rdV) of the hypothalamus are the critical node for the integration of internal (i.e., circannual timing) and external (e.g., photoperiod) information necessary for the regulation of seasonal reproduction.

The hypothalamic-pituitary-adrenal (HPA) axis is under complex regulatory control at multiple levels. Enzymatic regulation plays an important role in both circulating levels of glucocorticoids and target tissue exposure. Three key enzyme pathways are responsible for the immediate control of glucocorticoids. De novo synthesis of glucocorticoid from cholesterol involves a multistep enzymatic cascade. This cascade terminates with 11 beta-hydroxylase, responsible for the final conversion of 11-deoxy precursors into active glucocorticoids. Additionally, 11 beta-hydroxysteroid dehydrogenase type 1 (11 beta-HSD1) controls regeneration of glucocorticoids from inactive metabolites, providing a secondary source of active glucocorticoids. Localized inactivation of glucocorticoids is under the control of Type 2 11 beta-HSD (11 beta-HSD2). The function of these enzymes is largely unexplored in wild species, particularly songbirds. Here, we investigated the contribution of both clearance and generation of glucocorticoids to regulation of the hormonal stress response via the use of pharmacological antagonists. Additionally, we mapped 11 beta-HSD gene expression. We found 11 beta-HSD1 primarily in liver, kidney and adrenal glands, although it was detectable across all tissue types. 11 beta-HSD2 was predominately expressed in the adrenal glands and kidney with moderate gonadal and liver expression. Inhibition of glucocorticoid generation by metyrapone was found to decrease levels peripherally, while both peripheral and central administration of the 11 beta-HSD2 inhibitor DETC resulted in elevated concentrations of corticosterone. These data suggest that during the stress response, peripheral antagonism of the 11 beta-HSD system has a greater impact on circulating glucocorticoid levels than central control. Further studies should aim to elucidate the respective roles of the 11 beta-HSD and 11 beta-hydroxylase enzymes.

International audience; Most associative learning tests in rodents use negative stimuli, such as electric shocks. We investigated if young rats can learn to associate the presence of an odour with the experience of being tickled (i.e. using an experimenter’s hand to mimic rough-and-tumble play), shown to elicit 50 kHz ultrasonic vocalisations (USVs), which are indicative of positive affect. Male, pair-housed Wistar rats (N = 24) were all exposed to two neutral odours (A and B) presented in a perforated container on alternate days in a test arena. Following 60s of exposure, the rats were either tickled on days when odour A (n = 8) or odour B (n = 8) was present, or never tickled (n = 8). When tickled, rats produced significantly more 50 kHz USVs compared to the days when not being tickled, and compared to control rats. The level of anticipatory 50 kHz USVs in the 60s prior to tickling did not differ significantly between the tickled and control rats. As a retrieval test following the odour conditioning, rats were exposed successively in the same arena to three odours: an unknown neutral odour, extract of fox faeces, and either odours A or B. Compared to controls, 50 kHz USVs of tickled rats increased when exposed to the odour they had previously experienced when tickled, indicating that these rats had learned to associate the odour with the positive experience of being tickled. In a test with free access for 5 min to both arms of a T-maze, each containing one of the odours, rats tickled with odour A spent more time in the arm with this odour. This work is the first to test in a fully balanced design whether rats can learn to associate an odour with tickling, and indicates that positive odour conditioning has potential to be used as an alternative to negative conditioning tests.

The Japanese quail (Coturnix japonica) is a popular domestic poultry species and an increasingly significant model species in avian developmental, behavioural and disease research. We have produced a high-quality quail genome sequence, spanning 0.93 Gb assigned to 33 chromosomes. In terms of contiguity, assembly statistics, gene content and chromosomal organization, the quail genome shows high similarity to the chicken genome. We demonstrate the utility of this genome through three diverse applications. First, we identify selection signatures and candidate genes associated with social behaviour in the quail genome, an important agricultural and domestication trait. Second, we investigate the effects and interaction of photoperiod and temperature on the transcriptome of the quail medial basal hypothalamus, revealing key mechanisms of photoperiodism. Finally, we investigate the response of quail to H5N1 influenza infection. In quail lung, many critical immune genes and pathways were downregulated, and this may be key to the susceptibility of quail to H5N1. This genome will facilitate further research into diverse research questions using the quail as a model avian species.

International audience; The timing of breeding is under selection in wild populations as a result of climate change, and understanding the underlying physiological processes mediating this timing provides insight into the potential rate of adaptation. Current knowledge on this variation in physiology is, however, mostly limited to males. We assessed whether individual differences in the timing of breeding in females are reflected in differences in candidate gene expression and, if so, whether these differences occur in the upstream (hypothalamus) or downstream (ovary and liver) parts of the neuroendocrine system. We used 72 female great tits from two generations of lines artificially selected for early and late egg laying, which were housed in climate-controlled aviaries and went through two breeding cycles within 1 year. In the first breeding season we obtained individual egg-laying dates, while in the second breeding season, using the same individuals, we sampled several tissues at three time points based on the timing of the first breeding attempt. For each tissue, mRNA expression levels were measured using qPCR for a set of candidate genes associated with the timing of reproduction and subsequently analysed for differences between generations, time points and individual timing of breeding. We found differences in gene expression between generations in all tissues, with the most pronounced differences in the hypothalamus. Differences between time points, and early- and late-laying females, were found exclusively in the ovary and liver. Altogether, we show that fine-tuning of the seasonal timing of breeding, and thereby the opportunity for adaptation in the neuroendocrine system, is regulated mostly downstream in the neuro-endocrine system.

Ubiquitous in non-mammalian vertebrates, extra-retinal photoreceptors (ERPs) have been linked to an array of physiological, metabolic, behavioral, and morphological changes. However, the mechanisms and functional roles of ERPs remain one of the enduring questions of modern biology. In this review article, we use a comparative framework to identify conserved roles and distributions of ERPs, highlighting knowledge gaps. We conclude that ERP research can be divided into two largely unconnected categories: (i) identification and localization of photoreceptors and (ii) linkage of non-retinal light reception to behavioral and physiological processes, particularly endocrine systems. However, the emergence of novel gene editing and silencing techniques is enabling the unification of ERP research by allowing the bridging of this divide.

Play is a putatively positive experience and of key interest to the study of affective state in animals. Rats produce 50kHz ultrasonic vocalisation (USVs) during positive experiences, including social play and tickling. The tickling paradigm is intended to mimic social play resulting in positively valanced ultrasonic vocalisation (USV) production. We tested two hypotheses on the relationship between tickling and play: that tickling would increase play behaviour or that play behaviour would increase in anticipation of tickling, and that tickling would share some specific properties of play (rebound and emotional contagion of unexposed cage mates). Male Wistar rats (N=64, with 32 rats/cohort) of 28 days of age were housed in pairs with one rat assigned to be tickled and one as the non-tickled control. Production of 50kHz USVs and hand-following behaviour was measured. Prior to handling, solitary and social play was recorded for 5 minutes in the home cage. A two-day break in tickling was used to assess a potential rebound increase in responses to tickling. Only one rat within each cage was handled to assess emotional contagion through changes in the behaviour of the cage-mate. Solitary but not social play increased prior to tickling relative to controls (p = 0.01). There were marked differences between cohorts; tickled rats in C2 produced less 50kHz USVs than those in C1 (p = 0.04) and overall, C2 rats played less than rats in C1 (social p = 0.04 and solitary p < 0.001) and had a lighter start weight on arrival (p = 0.009) compared with cohort 1 (C1). In C1, there was evidence of rebound in USV production (p < 0.001) and a contagious effect of tickling reflected by increased hand-following in cage mates (p = 0.02). We found a positive relationship between start weight and USV responses to tickling (Rs = 0.43, p < 0.001), suggesting that the divergence in USV production may be due to developmental differences between cohorts. The results suggest that the relationship between tickling and play is complex in that tickling only affected solitary and not social play, and that tickling responses showed rebound and contagion effects on cage-mates which were specific to cohort responses to tickling.

Capture-restraint is often used to investigate the acute hypothalamic–pituitary-adrenal axis (HPA) response to stress in wild and captive animals through the production of glucocorticoids. Although this approach is useful for understanding changes in glucocorticoids, it overlooks potential changes in the complex regulatory systems associated with the glucocorticoid response, including genomic receptors, steroid metabolizing enzymes, carrier proteins, and downstream target proteins (e.g. gonadotropin-inhibitory hormone; GnIH). The present study in captive male white-crowned sparrows (Zonotrichia leucophrys) tests the hypothesis that corticosteroid receptors (mineralocorticoid - MR and glucocorticoid - GR), 11β-hydroxysteroid dehydrogenase 1 (11βHSD1) and 2 (11βHSD2), corticosteroid binding globulin (CBG), and GnIH undergo rapid changes in expression to mediate the glucocorticoid response to acute stress. To determine dynamic changes in gene mRNA expression in the hippocampus, hypothalamus, pituitary gland, and liver, birds were sampled within 3 min of entering the room and after 10, 30, and 60 min of capture restraint stress in a cloth bag. Restraint stress handling increased CBG and decreased GnIH mRNA expression in the liver and hypothalamus, respectively. MR, GR, 11βHSD1, and 11βHSD2 mRNA expression in the brain, pituitary gland, and liver did not change. No correlations were found between gene expression and baseline or stress-induced plasma corticosterone levels. No rapid changes of MR, GR, 11βHSD1, and 11βHSD2 mRNA expression during a standardized acute restraint protocol suggests that tissue level sensitivity may remain constant during acute stressors. However, the observed rise in CBG mRNA expression could act to facilitate transport to target tissues or buffer the rise in circulating glucocorticoids. Further studies on tissue specific sensitivity are warranted.

Corticosterone affects physiology and behavior both during normal daily processes but also in response to environmental challenges and is known to mediate life history trade-offs. Many studies have investigated patterns of corticosterone production at targeted times of year, while ignoring underlying annual profiles. We aimed to understand the annual regulation of hypothalamic-pituitary-adrenal (HPA) axis function of both migrant (Zonotrichia leucophrys gambelii; n = 926) and resident (Z. l. nutalli; n = 688) subspecies of white-crowned sparrow and how it is influenced by environmental conditions – wind, precipitation, and temperature. We predicted that more dramatic seasonal changes in baseline and stress-induced corticosterone would occur in migrants to precisely time the onset of breeding and cope with environmental extremes on their arctic breeding grounds, while changes in residents would be muted as they experience a more forgiving breeding schedule and comparatively benign environmental conditions in coastal California. During the course of a year, the harshest conditions were experienced the summer breeding grounds for migrants, at which point they had higher corticosterone levels compared to residents. For residents, the winter months coincided with harshest conditions at which point they had higher corticosterone levels than migrants. For both subspecies, corticosterone tended to rise as environmental conditions became colder and windier. We found that the annual maxima in stress-induced corticosterone occurred prior to egg lay for all birds except resident females. Migrants had much higher baseline and acute stress-induced corticosterone during breeding compared to residents; where in a harsher environment the timing of the onset of reproduction is more critical because the breeding season is shorter. Interestingly, molt was the only stage within the annual cycle in which subspecies differences were absent suggesting that a requisite reduction in corticosterone may have to be met for feather growth. These data suggest that modulation of the HPA axis is largely driven by environmental factors, social cues, and their potential interactions with a genetic program.

Highlights • We found no habitat-associated difference in food availability (arthropod biomass). • Unlike desert areas, urban areas had no detectable seasonal change in tree growth. • Desert, but not urban birds, had a marked plasma T response to GnRH challenge. • The timing of reproductive development varied inter-annually only in desert birds., Birds often adjust to urban areas by advancing the timing (phenology) of vernal gonad growth. However, the ecological and physiological bases of this adjustment are unclear. We tested whether the habitat-related disparity in gonad growth phenology of male Abert’s towhees, Melozone aberti, is due to greater food availability in urban areas of Phoenix, Arizona USA or, alternatively, a habitat-related difference in the phenology of key food types. To better understand the physiological mechanism underlying variation in gonad growth phenology, we compared the activity of the reproductive system at all levels of hypothalamo-pituitary–gonadal (HPG) axis. We found no habitat-associated difference in food availability (ground arthropod biomass), but, in contrast to the seasonal growth of leaves on desert trees, the leaf foliage of urban trees was already developed at the beginning of our study. Multiple estimates of energetic status did not significantly differ between the non-urban and urban towhees during three years that differed in the habitat-related disparity in gonad growth and winter precipitation levels. Thus, our results provide no support for the hypothesis that greater food abundance in urban areas of Phoenix drives the habitat-related disparity in gonad growth phenology in Abert’s towhees. By contrast, they suggest that differences in the predictability and magnitude of change in food availability between urban and desert areas of Phoenix contribute to the observed habitat-related disparity in gonad growth. Endocrine responsiveness of the gonads may contribute to this phenomenon as desert – but not urban – towhees had a marked plasma testosterone response to GnRH challenge.

Raising nestlings to fledging is energetically demanding for songbirds, requiring parents to balance several major tradeoffs. Nestling growth rates are highly susceptible to variation in environmental conditions and parental investment; highly variable environments with short breeding seasons such as the Arctic magnify these tradeoffs. Arctic nesting passerines provide a good model system in which to explore variation within and between species in growth rates with regards to environmental conditions and the timing of clutch initiation. Here we investigated inter-annual and inter-species variation in nestling mass gain for two species of arctic-breeding passerine: Gambel’s White-crowned Sparrows (Zonotrichia leucophrys gambelii) and Lapland Longspurs (Calcarius lapponicus) across two years. The nestling period of 2014 was both colder (with lower minimum and maximum temperatures) and wetter (with 73% more rainfall) than 2013. Arthropod biomass was also reduced in shrub tundra in 2014 as compared to 2013. Both species showed reductions in rate of daily mass gain of nestlings in 2014 compared to 2013, but we observed no significant difference between species. Furthermore, we found that in 2014 early nesting birds had higher rates of nestling growth than those initiating clutches later in the season. These findings suggest that overall environmental conditions were more challenging for raising nestlings in 2014 as compared to 2013, and that these differences were manifested in a reduced rate of nestling mass gain in both species. Furthermore, both species showed a negative correlation between precipitation and growth rates, while only Lapland Longspurs showed a positive correlation between growth rates and temperature.

The general reproductive effort model attempts to predict the resources that will be allocated to a current reproductive bout or to future survival by aborting the current reproductive attempt. Life-history theory predicts that short-lived species should devote more resources toward a reproductive event because brood value is far greater compared with that of long-lived species that have multiple breeding opportunities. Previous bird studies have used patterns of hormone secretion to understand the regulation of parental investment in response to environmental challenges, such as stress. The two key hormones investigated have been prolactin, which promotes parental investment, and corticosterone, which can reduce parental investment. Research on long-lived seabirds showed that prolactin levels decrease in response to a stressor, but the magnitude of the decline was positively correlated with future reproductive potential. However, little is known about the role of prolactin in short-lived species. Here we present prolactin and corticosterone data from a short-lived Arctic breeding, migratory songbird-the white-crowned sparrow, Zonotrichia leucophrys gambelii-at multiple stages of the breeding and nonbreeding seasons following standardized acute restraint stress. These data show that both prolactin and corticosterone are modulated seasonally. Corticosterone levels increased significantly in response to acute restraint stress during the breeding season in both sexes, but prolactin levels did not change in response to acute restraint stress at any stage of the annual cycle. We found no relationship between corticosterone or prolactin at either baseline or peak induced levels during any stage of breeding.

This work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC) (BB/I019502/1 to S.D.H. and S.L.M.) and by Roslin Institute Strategic Grant funding from the BBSRC (to S.L.M). It is assumed that many birds attempt to conceal their nests by using camouflage. To our knowledge, however, no previous experimental studies have explicitly tested this assumption. To explore whether birds choose materials that match the background colors of nest sites to reduce the conspicuousness of their nests, we offered nest-building male Zebra Finches (Taeniopygia guttata) a choice of nest materials that either matched or did not match the color of their nest cup and the surrounding cage walls. Males chose to nest predominantly with material that matched the background color of the cage. To our knowledge, this is the first experimental evidence that birds actively select materials that camouflage their nests. Publisher PDF

© The Author(s)., The colonization of urban environments by animals is often accompanied by earlier breeding and associated changes in seasonal schedules. Accelerated timing of seasonal reproduction in derived urban populations is a potential cause of evolutionary divergence from ancestral populations if differences in physiological processes that regulate reproductive timing become fixed over time. We compared reproductive development in free-living and captive male dark-eyed juncos deriving from a population that recently colonized a city (~35 years) and ceased migrating to that of conspecifics that live in sympatry with the urban population during winter and spring but migrate elsewhere to breed. We predicted that the earlier breeding sedentary urban birds would exhibit accelerated reproductive development in the spring along the hypothalamic-pituitary-gonadal (HPG) axis as compared to migrants. We found that free-living sedentary urban and migrant juncos differed at the level of the pituitary when measured as baseline luteinizing hormone (LH) levels, but not in increased LH when challenged with Gonadotropin-Releasing Hormone (GnRH). Among captives held in a common garden, and at the level of the gonad, we found that sedentary urban birds produced more testosterone in response to GnRH than migrants living in the same common environment, suggesting greater gonadal sensitivity in the derived urban population. Greater gonadal sensitivity could arise from greater upstream activation by LH or FSH or from reduced suppression of gonadal development by the adrenal axis. We compared abundance of gonadal transcripts for LH receptor (LHR), follicle stimulating hormone receptor (FSHR), glucocorticoid receptor (GR), and mineralocorticoid receptor (MR) in the common-garden, predicting either more abundant transcripts for LHR and FSHR or fewer transcripts for GR and MR in the earlier breeding sedentary urban breeders, as compared to the migrants. We found no difference in the expression of these genes. Together these data suggest that advanced timing of reproduction in a recently derived urban population is facilitated by earlier increase in upstream baseline activity of the HPG and earlier release from gonadal suppression by yet-to-be-discovered mechanisms. Evolutionarily, our results suggest that potential for gene flow between seasonally sympatric populations may be limited due to urban-induced advances in the timing of reproduction and resulting allochrony with ancestral forms., This work was funded by the National Science Foundation (IOS-1257474 to EK and IOS-1257527 to TG). SM acknowledges Roslin Institute strategic grant funding from the Biotechnology and Biological Sciences Research Council (BB/J004316/1 and BB/J004332/1).

Seasonal activation of the vertebrate hypothalamic-pituitary-gonadal (HPG) axis and gonadal development is initiated by gonadotropin-releasing hormone-I (GnRH) release from the hypothalamus. In photoperiodic species, the consistent annual change in photoperiod is the primary environmental signal affecting GnRH cell activity, including changes in the synthesis and secretion of this neuropeptide. Non-photoperiodic environmental cues such as energy availability also influence HPG axis activity, but the mechanisms mediating this influence, in particular on the GnRH system, are unclear. Understanding how the neuroendocrine system integrates environmental information is critical in determining the plasticity and adaptability of physiological responses to changing environments. The primary objective of this study was to investigate GnRH-mediated changes in HPG axis activity and gonadal development in response to energy availability in a wild bird. We hypothesized that negative energy balance inhibits HPG axis activity by affecting GnRH secretion. Moderate food restriction for several weeks in male house finches, Haemorhous mexicanus, decreased body condition and inhibited photoinduced testicular growth compared to birds fed ad libitum. Food restriction did not affect plasma luteinizing hormone (LH; a correlate of GnRH release) or plasma testosterone, but it enhanced the plasma LH response to an injection of the glutamatergic agonist, N-methyl-D-aspartate (NMDA). Thus, food restriction may decrease photoinduced HPG axis activation by acting centrally, in particular by attenuating the release of accumulated GnRH stores.

Every year around 100 million male piglets are castrated in the EU, usually without anaesthesia or post-operative analgesia. This surgical intervention is painful and stressful. Several main players within the pig industry have voluntarily agreed to end the practice of surgical pig castration in the EU by 2018. One alternative to castration is entire male pig production. However, entire males behave differently than castrates, for example, by performing more mounting behaviour, which is suggested to be a welfare problem. The aim of our study was to develop a comprehensive ethogram of different types of mounting and to investigate properties, causes and consequences of mounting behaviour in finishing pigs. The study included 80 entire male and 80 female pigs from two farrowing batches born six weeks apart. Mixed sex and single-sex housing of pigs are both common in pig farming, so to ensure our study was representative, the 160 pigs were assigned to social groups of 20 in three treatments: entire male pigs only (MM, 2 groups, n = 40), entire females only (FF, 2 groups, n = 40) and entire males and females mixed together (MF, 4 groups, n = 80). Measurements took place during the final six weeks before slaughter (between 63.5 and 105.5 kg). Observations of mounting behaviour on 12 days per batch suggested that: (i) males mounted more than females, (ii) within sex, there was no effect of treatment on the amount of mounting (although the statistical power of the study to detect these effects was low), and (iii) there were individual differences in mounting that were stable over time (within sex). Classification of mounting into different categories revealed that sexual mounting was most common overall and in males but only rare in females. Compared to other types of mounting (e.g. caused by crowding or during a fight), sexual mounts lasted longer and provoked more screaming by the recipient. There were no relationships between mounting behaviour on the one hand and dominance rank in food competition tests, the circulating levels of sex hormones (oestradiol, testosterone and progesterone) at the end of the study, the health scores (lameness and scratches) or weight gain on the other hand. The stable individual differences of mounting over time suggest that mounting behaviour is a trait of the individual rather than the appearance of random outbreaks. However, these differences in mounting cannot be explained by dominance behaviour or by differences in sex hormone concentrations that could indicate the onset of puberty. Mounting behaviour and in particular sexual mounting provoked high pitched screaming of the recipients indicating that mounting is a welfare problem. For the welfare assessment of entire male pig production the performance of mounting behaviour should be considered. (C) 2013 Elsevier B.V. All rights reserved.

The glucocorticoid stress response, regulated by the hypothalamic-pituitary-adrenal (HPA) axis, enables individuals to cope with stressors through transcriptional effects in cells expressing the appropriate receptors. The two receptors that bind glucocorticoids-the mineralocorticoid receptor (MR) and glucocorticoid receptor (GR)-are present in a variety of vertebrate tissues, but their expression in the brain is especially important. Neural receptor patterns have the potential to integrate multiple behavioral and physiological traits simultaneously, including self-regulation of glucocorticoid secretion through negative feedback processes. In the present work, we quantified the expression of GR and MR mRNA throughout the brain of a female great tit (Parus major), creating a distribution map encompassing 48 regions. This map, the first of its kind for P. major, demonstrated a widespread but not ubiquitous distribution of both receptor types. In the paraventricular nucleus of the hypothalamus (PVN) and the hippocampus (HP)-the two brain regions that we sampled from a total of 25 birds, we found high GR mRNA expression in the former and, unexpectedly, low MR mRNA in the latter. We examined the covariation of MR and GR levels in these two regions and found a strong, positive relationship between MR in the PVN and MR in the HP and a similar trend for GR across these two regions. This correlation supports the idea that hormone pleiotropy may constrain an individual's behavioral and physiological phenotype. In the female song system, we found moderate GR in hyperstriatum ventrale, pars caudalis (HVC), and moderate MR in robust nucleus of the arcopallium (RA). Understanding intra- and interspecific patterns of glucocorticoid receptor expression can inform us about the behavioral processes (e.g. song learning) that may be sensitive to stress and stimulate future hypotheses concerning the relationships between receptor expression, circulating hormone concentrations and performance traits under selection, including behavior.

This work was supported by the BBSRC (BB/I019502/1 to SDH and SLM) and Roslin Institute Strategic Grant funding from the BBSRC (SLM). Building a structurally robust nest is crucial for reproductive success in many birds. However, we know little about the criteria birds use to select material or where they go to collect it. Here we observed the material collection of male Cape Weavers (Ploceus capensis). Males typically selected long, strong material to build their nests and each male collected material from different locations. Males that built more nests nested in a different area of the colony and flew further to collect nest material than did males that built fewer nests. As these males that flew further to collect material had longer tails and wings and attracted more females to their territories than did males that flew shorter distances, they may have traded off the travel costs of collecting nest materials with benefits gained from holding a territory in a more 'desirable' part of the colony. Nest construction, then, appears to be a multi-dimensional task whereby birds take into account material's structural properties, material proximity to the nest site and territory quality. Males that do this effectively both attract more mates and provide structurally sound nests for their young. Publisher PDF

Individuals at the forefront of a range shift are likely to exhibit phenotypic traits that distinguish them from the population breeding within the historic range. Recent studies have examined morphological, physiological and behavioral phenotypes of individuals at the edge of their range. Several studies have found differences in the hypothalamic–pituitary–adrenal (HPA) axis activity in response to acute restraint stress in individuals at the range limits. HPA axis activation leads to elevations in glucocorticoids that regulate physiology and behavior. Here we compare the hormonal profiles and morphometrics from Gambel’s white-crowned sparrows (Zonotrichia leucophrys gambelii) breeding at the northern limit of the population’s range to those birds breeding within the historic population range. Birds breeding at the northern limit experienced a harsher environment with colder temperatures; however, we found no differences in arthropod prey biomass between the northern limit and more southern (historic) sites. Males at the northern limit had higher body condition scores (mass corrected for body size) compared to individuals within the historic range, but no differences were found in beak and tarsus lengths, wing chord, muscle profile or fat stores. In males during the pre-parental stage, before breeding commenced, HPA axis activity was elevated in birds at the northern limit of the range, but no differences were found during the parental or molt stages. Females showed no differences in HPA axis activity during the parental stage. This study suggests that “pioneering” individuals at the limits of their breeding range exhibit physiology and morphology that are distinct from individuals within the historic range. Electronic supplementary material The online version of this article (doi:10.1007/s00442-015-3447-7) contains supplementary material, which is available to authorized users.

Cumulative evidence indicates that song sparrows, Melospiza melodia morphna, of western Washington State prefer territories close to water. Densities of territories were higher within 50 m of open water and analysis of stomach contents revealed aquatic organisms. An unusually dry period (less open water) in May and June 1997 had no effect on latency of territorial males to respond to a simulated territorial intrusion (STI), but the number of songs and closest approach to the decoy were lower than those recorded in June 1988 (no major dry periods). A laboratory experiment was conducted in which males and females were exposed to long days to stimulate reproductive development. One group received a bath with water daily and the other group received a dry bath (both groups had ad libitum access to drinking water through a glass tube). Birds with a dry bath tended to show reduced photoperiodically-induced gonadal growth compared with birds that had access to water in the bath. Plasma levels of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) increased following photostimulation in all groups. However, LH levels were higher in females with access to water. There were no differences in hormone levels in any of the other groups. Taken together these novel data indicate that presence and access to open water could be an important environmental cue for song sparrows in western Washington State. Implications for global climate change and droughts are suggested.

Maternal aggressive behaviour, which protects the offspring from harm, is one component of maternal behaviour. Not only maternal aggression, but also maternal care and social behaviour in general, is regulated by the brain oxytocin (OXT) and vasopressin (AVP) systems. In the present study, we quantified the intensity of maternal aggression using the maternal defence test at key time points throughout pregnancy, parturition and lactation. Furthermore, we quantified changes in central OXT and arginine AVP V1a receptor (V1a-R) binding in brain regions known to be important in regulating maternal aggression, aiming to investigate whether central changes coincide with the intensity of this behaviour. The intensity of aggression was found to dramatically change over the peripartum period, with its first appearance on the day before parturition. Aggression intensity fell immediately after parturition, although it increased during days 4-7 of lactation, before almost disappearing at weaning. OXT receptor (OTR) and V1a-R binding also showed changes through the peripartum period. OTR binding was highest at parturition within the bed nucleus of the stria terminalis and medial preoptic area and on days 4-7 of lactation in the lateral septum (LS) compared to any other time point during the peripartum period. OTR binding positively correlated with the peak of maternal aggression, suggesting that OXT may act in the LS to facilitate the expression of aggressive behaviour. At parturition, V1a-R binding was at its highest levels in the paraventricular nucleus and central amygdala (CeA) and, in the LS, V1a-R binding positively correlated with aggressive behaviour. V1a-R mRNA expression was also increased within the CeA at parturition. Taken together, the observed fluctuations in OTR and V1a-R binding in the neural circuitry important for regulating maternal behaviour may ensure that maternal aggression is expressed at the correct time during the peripartum period.

Central vasopressin facilitates social recognition and modulates numerous complex social behaviors in mammals, including parental behavior, aggression, affiliation, and pair-bonding. In rodents, social interactions are primarily mediated by the exchange of olfactory information, and there is evidence that vasopressin signaling is important in brain areas where olfactory information is processed. We recently discovered populations of vasopressin neurons in the main and accessory olfactory bulbs and anterior olfactory nucleus that are involved in the processing of social odor cues. In this review, we propose a model of how vasopressin release in these regions, potentially from the dendrites, may act to filter social odor information to facilitate odor-based social recognition. Finally, we discuss recent human research linked to vasopressin signaling and suggest that our model of priming-facilitated vasopressin signaling would be a rewarding target for further studies, as a failure of priming may underlie pathological changes in complex behaviors.

The anterior olfactory nucleus (AON), a component of the main olfactory system, is a cortical region that processes olfactory information and acts as a relay between the main olfactory bulbs and higher brain regions such as the piriform cortex. Utilizing a transgenic rat in which an enhanced green fluorescent protein reporter gene is expressed in vasopressin neurones (eGFP-vasopressin), we have discovered a population of vasopressin neurones in the AON. These vasopressin neurones co-express vasopressin V1 receptors. They also co-express GABA and calbinin-D28k indicating that they are neurochemically different from the newly described vasopressin neurons in the main olfactory bulb. We utilized the immediate early gene product, early growth response protein 1 (Egr-1), to examine the functional role of these vasopressin neurons in processing social and non-social odours in the AON. Exposure of adult rats to a conspecific juvenile or a heterospecific predator odour leads to increases in Egr-1 expression in the AON in a subregion specific manner. However, only exposure to a juvenile increases Egr-1 expression in AON vasopressin neurons. These data suggest that vasopressin neurones in the AON may be selectively involved in the coding of social odour information.

Although the glucocorticoid response to acute short-term stress is an adaptive physiological mechanism that aids in the response to and survival of noxious stimuli, chronic stress is associated with a negative impact on health. In wild-caught European starlings (Sturnus vulgaris), chronic stress alters the responsiveness of hypothalamic-pituitary-adrenal (HPA) axis as measured by the acute corticosterone response. In the present study, we investigated potential underlying neuroendocrine mechanisms by comparing glucocorticoid receptor and mineralocorticoid receptor mRNA expression in the brains of chronically and nonchronically-stressed starlings. Hypothalamic paraventricular nucleus, but not hippocampal, glucocorticoid receptor mRNA expression in chronically-stressed birds was significantly lower compared to controls, suggesting changes in the efficacy of corticosterone negative feedback. In addition, chronically-stressed birds showed a significant decrease in hippocampal MR mRNA expression. Together, these results suggest that chronic stress changes the brain physiology of wild birds and provides important information for the understanding of the underlying mechanisms that result in dysregulation of the HPA axis in wild animals by chronic stress.

Oxytocin released within the brain from both magnocellular and parvocellular systems of the hypothalamus has diverse effects on behavior. When oxytocin is released within the brain, its effects are to diminish fearfulness; this not only encourages social investigation of newcomers, but also may enhance a tendency to express aggression toward an intruder. Oxytocin supports social recognition, redirects behavior away from feeding directed behavior toward sexual behavior, and facilitates the formation of social bonds. This system, which depends not only upon release of oxytocin but also on oxytocin receptor distribution within the brain, becomes particularly important at parturition, when a bond is first formed between mother and offspring.

Hypothalamo-pituitary-adrenal axis responses to various stressors are typically attenuated during lactation, including in rats selectively bred for high or low anxiety. As high-anxiety dams are more aggressive towards intruders than low-anxiety dams during maternal defence, we investigated their hypothalamo-pituitary-adrenal axis responses to this social stress. Maternal defence induced elevated stress responses in high-anxiety dams only; nerve-growth-factor-induced gene B mRNA expression in the parvocellular paraventricular nucleus and adrenocorticotropin hormone secretory responses were substantially enhanced after maternal defence. In contrast, secretory responses to a non-social stress (elevated platform) were not different between high- and low-anxiety dams. Thus, responsiveness of the stress axis in lactation is dependent upon the innate level of anxiety of the dam and, as a consequence, her reactiveness to social threat.

Energy deficiency can suppress reproductive function in vertebrates. As the orchestrator of reproductive function, endocrine activity of the hypothalamo-pituitary–gonadal (HPG) axis is potentially an important mechanism mediating such effects. Previous experiments in wild-caught birds found inconsistent relationships between energy deficiency and seasonal reproductive function, but these experiments focused on baseline HPG axis activity and none have investigated the responsiveness of this axis to endocrine stimulation. Here, we present data from an experiment in Abert's towhees, Melozone aberti, using gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH) challenges to investigate whether energy deficiency modulates the plasma testosterone responsiveness of the HPG axis. Wild-caught birds were either ad libitum fed or energetically constrained via chronic food restriction during photoinduced reproductive development. Energy deficiency did not significantly affect the development of reproductive morphology, the baseline endocrine activity of the HPG axis, or the plasma testosterone response to GnRH challenge. Energy deficiency did, however, decrease the plasma testosterone responsiveness to LH challenge. Collectively, these observations suggest that energy deficiency has direct gonadal effects consisting of a decreased responsiveness to LH stimulation. Our study, therefore, reveals a mechanism by which energy deficiency modulates reproductive function in wild birds in the absence of detectable effects on baseline HPG axis activity., Summary: Energy deficiency in an adult male songbird has no detectable effect on the development of reproductive morphology, but constrains the endocrine responsiveness of the testes.

International audience; Urban animals inhabit an environment considerably different than do their non-urban conspecifics, and to persist urban animals must adjust to these novel environments. The timing of seasonal reproductive development (i.e., growth of gonads and secondary sex organs) is a fundamental determinant of the breeding period and is frequently advanced in urban bird populations. However, the underlying mechanism(s) by which birds adjust the timing of reproductive development to urban areas remain(s) largely unknown. Here, we compared the timing of vernal reproductive development in free-ranging urban and non-urban male Abert's Towhees, Melozone aberti, in Phoenix, Arizona, USA, and tested the non-mutually exclusive hypotheses that earlier reproductive development is due to improved energetic status and/or earlier increase in endocrine activity of the reproductive system. We found that urban birds initiated testicular development earlier than non-urban birds, but this disparity was not associated with differences in body condition, fat stores, or innate immune performance. These results provide no support for the hypothesis that energetic constraints are responsible for delayed reproductive development of non-urban relative to urban male Abert's Towhees. Urban birds did, however, increase their plasma luteinizing hormone, but not plasma testosterone, earlier than non-urban birds. These findings suggest that adjustment to urban areas by Abert's Towhees involves increases in the endocrine activity of the anterior pituitary gland and/or hypothalamus earlier than non-urban towhees.

This work was supported by the BBSRC (BB/I019502/1, S.D.H. and S.L.M.), the Roslin Institute Strategic Grant funding from the BBSRC (S.L.M) and the Leverhulme Trust (S.D.H. and P.T.W.), and A.R.B. gratefully acknowledges the financial support of CNPq (National Council for Scientific and Technological Development, Brazil, grant no. 301558/2012-4). In nature, many animals build structures that can be readily measured at the scale of their gross morphology (e.g. length, volume and weight). Capturing individuality as can be done with the structures designed and built by human architects or artists, however, is more challenging. Here, we tested whether computer-aided image texture classification approaches can be used to describe textural variation in the nests of weaverbirds (Ploceus species) in order to attribute nests to the individual weaverbird that built them. We found that a computer-aided texture analysis approach does allow the assignment of a signature to weaverbirds’ nests. We suggest that this approach will be a useful tool with which to examine individual variation across a range of animal constructions, not just for nests. Publisher PDF

Gambel's white-crowned sparrow is a long distance migrant that undergoes spontaneous gonadal regression as a result of long day exposure. This termination of breeding is caused by the development of photorefractoriness and the birds become insensitive to long days, including continuous light. The present study investigated its possible mechanisms by examining the activity of the gonadotrophin-releasing hormone (GnRH) system under different photoperiodic regimes. We investigated the localisation and distribution of GnRH-I, its precursor pro-GnRH-GAP and GnRH-II in Gambel's white-crowned sparrow brain using immunocytochemistry with specific antibodies during photostimulation and the development of photorefractoriness. The study revealed that photoperiodic treatment, including the onset of photorefractoriness, had no significant effect on the size or number of GnRH-I, pro-GnRH-GAP or GnRH II immunoreactive cells, or the density of the GnRH-I, pro-GnRH-GAP immunoreactive fibres at the median eminence. GnRH-II was not found in the median eminence, suggesting that it does not regulate pituitary gonadotrophin secretion. GnRH-I measurement in hypothalamic extracts by radioimmunoassay did not reveal any significant difference between birds that were photostimulated or in the early stages of photorefractoriness. Furthermore, the action of the excitatory amino acid glutamate agonist N-methyl-D-aspartate on GnRH neurones in photorefractory birds was demonstrated by the significant blockade of luteinising hormone release with a specific GnRH antagonist. Taken together, these results suggest that, in Gambel's white-crowned sparrow, a decrease in GnRH-I secretion is the initial step for the onset of photorefractoriness and not a decrease in GnRH-I biosynthesis.

The termination of seasonal breeding in most photoperiodic passerines is heralded by spontaneous gonadal regression as a result of long day exposure. This phenomenon is termed absolute photorefractoriness and this insensitivity to long days may only be dissipated by short photoperiod exposure. The timing of the transition to a photorefractory stage in adult free-living male Dark-eyed Juncos is age-dependent. Second-year males (SY, entering their first breeding season) molt earlier, suggesting that they become refractory earlier, than older males (ASY). We determined whether the earlier onset of photorefractoriness in SY males concurs with decreased expression of hypothalamic GnRH-I or its precursor, pro-GnRH-GAP. Male SY and ASY juncos were caught at the end of the breeding season either during, or following, testicular regression. Immunoreactivity for GnRH-I and pro-GnRH-GAP was found in perikarya in the preoptic area, and fibers in the median eminence. The number and size of cells immunoreactive for GnRH-I and pro-GnRH-GAP did not significantly differ with age or time of year. In ASY juncos, there was a significant decrease in both GnRH-I and pro-GnRH-GAP staining density at the median eminence following testicular regression at a time of photorefractoriness onset. Density of pro-GnRH-GAP at the median eminence was also reduced following testicular regression in SY males but GnRH-I staining density did not change. Thus, age-class differences in the transition to photorefractoriness do not appear to result from differences in GnRH-I synthesis. Instead, the regulation of GnRH-I secretion by non-photoperiodic factors may determine photorefractoriness onset.

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.

We investigated whether changes in noradrenaline neurotransmission in the hypothalamus could explain the hyporesponsiveness of the hypothalamic-pituitary-adrenal (HPA) axis in late pregnancy. Noradrenaline release within the hypothalamic paraventricular nucleus in response to swim stress, as estimated by microdialysis and high-performance liquid chromatography, was lower in 20-day pregnant rats compared to virgin rats. Driving a central noradrenergic pathway using intravenous cholecystokinin increased adrenocorticotropic hormone (ACTH) secretion in virgin rats, but the response was significantly less in 16-day and 20-day pregnant rats. Thus, the activity of noradrenergic inputs to the paraventricular nucleus and the HPA axis is attenuated in late pregnancy. The sensitivity of the HPA axis to noradrenaline in pregnancy was investigated by intracerebroventricular administration of an α1-receptor antagonist, benoxathian, before and during exposure to swim stress. In virgin rats, benoxathian increased basal and stress-induced ACTH secretion, but in late pregnant rats the benoxathian effects were attenuated, indicating reduced sensitivity of the HPA axis to noradrenaline neurotransmission and/or the inability of the system to become disinhibited at this time. α1A-adrenoreceptor mRNA expression in the parvocellular and magnocellular paraventricular nucleus, measured by in situ hybridisation, was decreased in late pregnant compared to virgin rats. Additionally, blocking endogenous opioid inhibition with naloxone pretreatment restored the ACTH secretory response to cholecystokinin in pregnant rats. Thus, in late pregnancy, there is reduced noradrenergic input to the paraventricular nucleus and reduced α1A-receptor expression in the paraventricular nucleus, both of which may contribute to the reduced responsiveness of the HPA axis in pregnancy. © 2005 Blackwell Publishing Ltd.

We examined plasticity of the stress response among three populations of the white-crowned sparrow ( Zonotrichia leucophrys). These populations breed at different elevations and latitudes and thus have breeding seasons that differ markedly in length. We hypothesize that in populations where birds raise only one or rarely two broods in a season, the fitness costs of abandoning a nest are substantially larger than in closely related populations that raise up to three broods per season. Thus individuals with short breeding seasons should be less responsive to stressors and therefore less likely to abandon their young. In our study, baseline and handling-induced corticosterone levels were similar among populations, but corticosteroid-binding globulins differed, leading to a direct relationship between stress-induced free corticosteroid levels and length of breeding season. There were also population-specific differences in intracellular low-affinity (glucocorticoid-like) receptors in both liver and brain tissue. Although investigations of population-based differences in glucocorticoid secretion are common, this is the first study to demonstrate population-level differences in binding globulins. These differences could lead to dramatically different physiological and behavioral responses to stress.