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1.  Maintenance of MHC Class IIB diversity in a recently established songbird population 
Journal of avian biology  2012;43(2):109-118.
We examined variation at MHC Class IIB genes in a recently established population of dark-eyed juncos (Junco hyemalis) in a coastal urban environment in southern California, USA relative to an ancestral-range population from a nearby species-typical montane environment. The founding population is estimated to have been quite small, but we predicted that variation at the major histocompatibility complex (MHC) among the founders would nevertheless be preserved owing to the high functional significance of MHC. Previous studies of MHC in songbirds have had varying degrees of success in isolating loci, as passerines show extensive MHC gene duplication. In order to compare diversity in the two populations, we employed two published approaches to sequencing MHC Class II exon 2: direct sequencing with exon-based primers, and traditional cloning and sequencing with intron-based primers. Results from both methods show that the colonist population has maintained high levels of variation. Our results also indicate varying numbers of alleles across individuals, corroborating evidence for gene duplication in songbird MHC. While future studies in songbirds may need to take a genomic approach to fully understand the structure of MHC in this lineage, our results show that it is possible to use traditional methods to reveal functional variation across populations.
doi:10.1111/j.1600-048X.2012.05504.x
PMCID: PMC3368239  PMID: 22685370
MHC; birds; passerines; colonization
2.  Early spring sex differences in luteinizing hormone response to gonadotropin releasing hormone in co-occurring resident and migrant dark-eyed juncos (Junco hyemalis) 
Highlights
•In early spring female juncos vary in LH following repeated stimulation with GnRH.•Resident and migrant males do not vary in LH.•Suggests the pituitary as a critical point of control for reproductive timing.•Sex difference suggests selection shaped responsiveness at critical time points.
To optimally time reproduction, animals must coordinate changes in the hypothalamo-pituitary-gonadal (HPG) axis. The extent of intra-species variation in seasonal timing of reproductive function is considerable, both within and among populations. Dark-eyed junco (Junco hyemalis) populations are known to differ in their reproductive timing response to cues experienced in the same habitat in late winter/early spring. Specifically in juncos cohabitating on shared wintering grounds, residents initiate breeding and reproductive activity but migrants delay reproductive development and prepare to migrate before breeding. Here, we test the hypothesis that the pituitary gland acts as a ‘control point’ to modulate differential HPG axis activity across populations. We sampled free-living resident and migrant juncos on their shared over-wintering grounds in March, thus all individuals were experiencing the same environmental cues, including photoperiod. We predicted that during this critical time of transition, residents would more readily respond to repeated gonadotropin releasing hormone (GnRH) stimulation with increases in luteinizing hormone (LH), in contrast to migrants, which should delay full reproductive activity. Our data indicate that migrant females, while still on the overwintering grounds, have a reduced LH response to repeated GnRH injections compared to resident females. Male migrant and resident birds did not differ in their responsiveness to repeated GnRH. Our results suggest a sex difference in the costs of mistimed activation of the HPG axis, with female migrants being less responsive than residents females and males to repeated stimulation. Further, our data implicate a key role for the pituitary in regulating appropriate reproductive timing responses.
doi:10.1016/j.ygcen.2016.06.031
PMCID: PMC5036536  PMID: 27374492
Seasonal breeding; Phenology; Supplemental cues; Sex differences; Songbird
3.  Recent postglacial range expansion drives the rapid diversification of a songbird lineage in the genus Junco 
Pleistocene glacial cycles are thought to have played a major role in the diversification of temperate and boreal species of North American birds. Given that coalescence times between sister taxa typically range from 0.1 to 2.0 Myr, it has been assumed that diversification occurred as populations were isolated in refugia over long periods of time, probably spanning one to several full glacial cycles. In contrast, the rapid postglacial range expansions and recolonization of northern latitudes following glacial maxima have received less attention as potential promoters of speciation. Here we report a case of extremely rapid diversification in the songbird genus Junco as a result of a single continent-wide range expansion within the last 10 000 years. Molecular data from 264 juncos sampled throughout their range reveal that as the yellow-eyed junco (Junco phaeonotus) of Mesoamerica expanded northward following the last glacial maximum, it speciated into the dark-eyed junco (Junco hyemalis), which subsequently diversified itself into at least five markedly distinct and geographically structured morphotypes in the USA and Canada. Patterns of low genetic structure and diversity in mitochondrial DNA and amplified fragment length polymorphism loci found in dark-eyed juncos relative to Mesoamerican yellow-eyed juncos provide support for the hypothesis of an expansion from the south, followed by rapid diversification in the north. These results underscore the role of postglacial expansions in promoting diversification and speciation through a mechanism that represents an alternative to traditional modes of Pleistocene speciation.
doi:10.1098/rspb.2007.0852
PMCID: PMC2279216  PMID: 17725978
speciation; postglacial expansion; phylogeography; Holocene; Junco
4.  Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation 
Behavioral Ecology  2012;23(5):960-969 .
Novel or changing environments expose animals to diverse stressors that likely require coordinated hormonal and behavioral adaptations. Predicted adaptations to urban environments include attenuated physiological responses to stressors and bolder exploratory behaviors, but few studies to date have evaluated the impact of urban life on codivergence of these hormonal and behavioral traits in natural systems. Here, we demonstrate rapid adaptive shifts in both stress physiology and correlated boldness behaviors in a songbird, the dark-eyed junco, following its colonization of a novel urban environment. We compared elevation in corticosterone (CORT) in response to handling and flight initiation distances in birds from a recently established urban population in San Diego, California to birds from a nearby wildland population in the species' ancestral montane breeding range. We also measured CORT and exploratory behavior in birds raised from early life in a captive common garden study. We found persistent population differences for both reduced CORT responses and bolder exploratory behavior in birds from the colonist population, as well as significant negative covariation between maximum CORT and exploratory behavior. Although early developmental effects cannot be ruled out, these results suggest contemporary adaptive evolution of correlated hormonal and behavioral traits associated with colonization of an urban habitat.
doi:10.1093/beheco/ars059
PMCID: PMC3431113  PMID: 22936840
adaptation; boldness; corticosterone; evolution; junco; urbanization
5.  Effect of Restricted Preen-Gland Access on Maternal Self Maintenance and Reproductive Investment in Mallards 
PLoS ONE  2010;5(10):e13555.
Background
As egg production and offspring care are costly, females should invest resources adaptively into their eggs to optimize current offspring quality and their own lifetime reproductive success. Parasite infections can influence maternal investment decisions due to their multiple negative physiological effects. The act of preening – applying oils with anti-microbial properties to feathers – is thought to be a means by which birds combat pathogens and parasites, but little is known of how preening during the reproductive period (and its expected disease-protecting effects) influences maternal investment decisions at the level of the egg.
Methodology/Principal Findings
Here, we experimentally prevented female mallards (Anas platyrhynchos) from accessing their preen gland during breeding and monitored female immunoresponsiveness (e.g., plasma lysozyme concentration) as well as some egg traits linked to offspring quality (e.g., egg mass, yolk carotenoid content, and albumen lysozyme levels). Females with no access to their preen gland showed an increase in plasma lysozyme level compared to control, normally preening females. In addition, preen-gland-restricted females laid significantly lighter eggs and deposited higher carotenoid concentrations in the yolk compared to control females. Albumen lysozyme activity did not differ significantly between eggs laid by females with or without preen gland access.
Conclusion/Significance
Our results establish a new link between an important avian self-maintenance behaviour and aspects of maternal health and reproduction. We suggest that higher yolk carotenoid levels in eggs laid by preen-gland-restricted females may serve to boost health of offspring that would hatch in a comparatively microbe-rich environment.
doi:10.1371/journal.pone.0013555
PMCID: PMC2965083  PMID: 21048952
6.  Can Preening Contribute to Influenza A Virus Infection in Wild Waterbirds? 
PLoS ONE  2010;5(6):e11315.
Wild aquatic birds in the Orders Anseriformes and Charadriiformes are the main reservoir hosts perpetuating the genetic pool of all influenza A viruses, including pandemic viruses. High viral loads in feces of infected birds permit a fecal-oral route of transmission. Numerous studies have reported the isolation of avian influenza viruses (AIVs) from surface water at aquatic bird habitats. These isolations indicate aquatic environments have an important role in the transmission of AIV among wild aquatic birds. However, the progressive dilution of infectious feces in water could decrease the likelihood of virus/host interactions. To evaluate whether alternate mechanisms facilitate AIV transmission in aquatic bird populations, we investigated whether the preen oil gland secretions by which all aquatic birds make their feathers waterproof could support a natural mechanism that concentrates AIVs from water onto birds' bodies, thus, representing a possible source of infection by preening activity. We consistently detected both viral RNA and infectious AIVs on swabs of preened feathers of 345 wild mallards by using reverse transcription–polymerase chain reaction (RT-PCR) and virus-isolation (VI) assays. Additionally, in two laboratory experiments using a quantitative real-time (qR) RT-PCR assay, we demonstrated that feather samples (n = 5) and cotton swabs (n = 24) experimentally impregnated with preen oil, when soaked in AIV-contaminated waters, attracted and concentrated AIVs on their surfaces. The data presented herein provide information that expands our understanding of AIV ecology in the wild bird reservoir system.
doi:10.1371/journal.pone.0011315
PMCID: PMC2892510  PMID: 20593026
7.  Phenotypic integration and independence: Hormones, performance, and response to environmental change 
Hormones coordinate the co-expression of behavioral, physiological, and morphological traits, giving rise to correlations among traits and organisms whose parts work well together. This article considers the implications of these hormonal correlations with respect to the evolution of hormone-mediated traits. Such traits can evolve owing to changes in hormone secretion, hormonal affinity for carrier proteins, rates of degradation and conversion, and interaction with target tissues to name a few. Critically, however, we know very little about whether these changes occur independently or in tandem, and thus whether hormones promote the evolution of tight phenotypic integration or readily allow the parts of the phenotype to evolve independently. For example, when selection favors a change in expression of hormonally mediated characters, is that alteration likely to come about through changes in hormone secretion (signal strength), changes in response to a fixed level of secretion (sensitivity of target tissues), or both? At one extreme, if the phenotype is tightly integrated and only the signal responds via selection's action on one or more hormonally mediated traits, adaptive modification may be constrained by past selection for phenotypic integration. Alternatively, response to selection may be facilitated if multivariate selection favors new combinations that can be easily achieved by a change in signal strength. On the other hand, if individual target tissues readily “unplug” from a hormone signal in response to selection, then the phenotype may be seen as a loose confederation that responds on a trait-by-trait basis, easily allowing adaptive modification, although perhaps more slowly than if signal variation were the primary mode of evolutionary response. Studies reviewed here and questions for future research address the relative importance of integration and independence by comparing sexes, individuals, and populations. Most attention is devoted to the hormone testosterone (T) and a songbird species, the dark-eyed junco (Junco hyemalis).
doi:10.1093/icb/icp057
PMCID: PMC4012227  PMID: 21665827
8.  Differential migration and an endocrine response to stress in wintering dark-eyed juncos (Junco hyemalis). 
The dark-eyed junco (junco hyemalis) exhibits differential migration in autumn that, in general, results in females overwintering south of males, and young within each sex overwintering north of older birds. Individuals overwintering at higher latitudes face less predictable and more challenging environmental conditions. Rapid increases in circulating levels of the energy-regulating glucocorticosteroid, corticosterone, occur in response to environmental stressors. To establish whether the strength of acute corticosterone secretion was correlated with the probability of encountering poor environmental conditions, we compared the corticosterone stress response (e.g. initial plasma concentrations at the time of capture and 30 min later) in dark-eyed juncos overwintering in Mississippi (MS), USA, near the southern limit of their wintering range, with juncos overwintering in New York (NY), USA, near the northern limit of their wintering range. During two winters, 22 males and one female were sampled in NY; 13 males, 12 females and one bird of undetermined sex were sampled in MS. Not unexpectedly, NY birds carried greater fat reserves that resulted in a significantly higher value of energetic condition (mass corrected for wing cord cubed). There was no difference between the two winters sampled at either site, nor was there an effect of sex on patterns of corticosterone secretion in MS birds. With sexes pooled, MS and NY birds had similar baseline corticosterone levels. However, as predicted, NY birds exhibited significantly higher corticosterone concentrations 30 min after capture. These results support the hypothesis that birds wintering in less predictable, more extreme environments show a higher amplitude corticosterone response, which may enable them to adjust their behaviour and physiology more rapidly in response to environmental stressors such as storms. Adrenocortical sensitivity may be a part of the physiological milieu associated with differential migration in juncos; whether it results from endogenous differences in the migratory programmes of individuals or from acclimatization to local environmental conditions remains to be determined.
PMCID: PMC1690749  PMID: 11052541
9.  Robust behavioral effects of song playback in the absence of testosterone or corticosterone release 
Hormones and behavior  2012;62(4):418-425.
Some species of songbirds elevate testosterone in response to territorial intrusions while others do not. The search for a general explanation for this interspecific variation in hormonal response to social challenges has been impeded by methodological differences among studies. We asked whether song playback alone is sufficient to bring about elevation in testosterone or corticosterone in the dark-eyed junco (Junco hyemalis), a species that has previously demonstrated significant testosterone elevation in response to a simulated territorial intrusion when song was accompanied by a live decoy. We studied two populations of juncos that differ in length of breeding season (6–8 v. 14–16 weeks), and conducted playbacks of high amplitude, long-range song. In one population, we also played low amplitude, short-range song, a highly potent elicitor of aggression in juncos and many songbirds. We observed strong aggressive responses to both types of song, but no detectable elevation of plasma testosterone or corticosterone in either population. We also measured rise in corticosterone in response to handling post-playback, and found full capacity to elevate corticosterone but no effect of song class (long-range or short-range) on elevation. Collectively, our data suggest that males can mount an aggressive response to playback without a change in testosterone or corticosterone, despite the ability to alter these hormones during other types of social interactions. We discuss the observed decoupling of circulating hormones and aggression in relation to mechanisms of behavior and the cues that may activate the HPA and HPG axes.
doi:10.1016/j.yhbeh.2012.07.009
PMCID: PMC3477244  PMID: 22850247
10.  Speciation on Oceanic Islands: Rapid Adaptive Divergence vs. Cryptic Speciation in a Guadalupe Island Songbird (Aves: Junco) 
PLoS ONE  2013;8(5):e63242.
The evolutionary divergence of island populations, and in particular the tempo and relative importance of neutral and selective factors, is of central interest to the study of speciation. The rate of phenotypic evolution upon island colonization can vary greatly among taxa, and cases of convergent evolution can further confound the inference of correct evolutionary histories. Given the potential lability of phenotypic characters, molecular dating of insular lineages analyzed in a phylogenetic framework provides a critical tool to test hypotheses of phenotypic divergence since colonization. The Guadalupe junco is the only insular form of the polymorphic dark-eyed junco (Junco hyemalis), and shares eye and plumage color with continental morphs, yet presents an enlarged bill and reduced body size. Here we use variation in mtDNA sequence, morphological traits and song variables to test whether the Guadalupe junco evolved rapidly following a recent colonization by a mainland form of the dark-eyed junco, or instead represents a well-differentiated “cryptic” lineage adapted to the insular environment through long-term isolation, with plumage coloration a result of evolutionary convergence. We found high mtDNA divergence of the island lineage with respect to both continental J. hyemalis and J. phaeonotus, representing a history of isolation of about 600,000 years. The island lineage was also significantly differentiated in morphological and male song variables. Moreover, and contrary to predictions regarding diversity loss on small oceanic islands, we document relatively high levels of both haplotypic and song-unit diversity on Guadalupe Island despite long-term isolation in a very small geographic area. In contrast to prevailing taxonomy, the Guadalupe junco is an old, well-differentiated evolutionary lineage, whose similarity to mainland juncos in plumage and eye color is due to evolutionary convergence. Our findings confirm the role of remote islands in driving divergence and speciation, but also their potential role as repositories of ancestral diversity.
doi:10.1371/journal.pone.0063242
PMCID: PMC3651090  PMID: 23675466
11.  Shared songs are of lower performance in the dark-eyed junco 
Royal Society Open Science  2016;3(7):160341.
Social learning enables the adjustment of behaviour to complex social and ecological tasks, and underlies cultural traditions. Understanding when animals use social learning versus other forms of behavioural development can help explain the dynamics of animal culture. The dark-eyed junco (Junco hyemalis) is a songbird with weak cultural song traditions because, in addition to learning songs socially, male juncos also invent or improvise novel songs. We compared songs shared by multiple males (i.e. socially learned) with songs recorded from only one male in the population (many of which should be novel) to gain insight into the advantages of social learning versus invention or improvisation. Song types shared by multiple males were on average of lower performance, on aspects of vocal performance that have been implicated in agonistic communication in several species. This was not explained by cultural selection among socially learned songs (e.g. selective learning) because, for shared song types, song performance did not predict how many males shared them. We discuss why social learning does not maximize song performance in juncos, and suggest that some songbirds may add novel songs to culturally inherited repertoires as a means to acquire higher-quality signals.
doi:10.1098/rsos.160341
PMCID: PMC4968478  PMID: 27493786
animal communication; cultural evolution; improvisation; invention; social learning; song performance
12.  Neural steroid sensitivity and aggression: comparing individuals of two songbird subspecies 
Journal of evolutionary biology  2013;26(4):820-831.
Hormones coordinate the expression of complex phenotypes and thus may play important roles in evolutionary processes. When populations diverge in hormone-mediated phenotypes, differences may arise via changes in circulating hormones, sensitivity to hormones, or both. Determining the relative importance of signal and sensitivity requires consideration of both inter- and intra-population variation in hormone levels, hormone sensitivity, and phenotype, but such studies are rare, particularly among closely related taxa. We compared males of two subspecies of the dark-eyed junco (Junco hyemalis) for territorial aggression and associations among behavior, circulating testosterone (T), and gene expression of androgen receptor (AR), aromatase (AROM), and estrogen receptor α in three behaviorally relevant brain regions. Thus, we examined the degree to which evolution may shape behavior via changes in plasma T as compared to key sex steroid binding/converting molecules. We found that the white-winged junco (J. h. aikeni) was more aggressive than the smaller, less ornamented Carolina junco (J. h. carolinensis). The subspecies did not differ in circulating testosterone, but did differ significantly in the abundance of AR and AROM mRNA in key areas of the brain. Within populations, both gene expression and circulating T co-varied significantly and positively with individual differences in aggression. Notably, the differences identified between populations were opposite to those predicted by the patterns among individuals within populations. These findings suggest that hormone-phenotype relationships may evolve via multiple pathways, and that changes that have occurred over evolutionary time do not necessarily reflect standing physiological variation on which current evolutionary processes may act.
doi:10.1111/jeb.12094
PMCID: PMC3622748  PMID: 23517519
Testosterone; aggression; androgen receptor; aromatase; individual variation; divergence; hypothalamus; nucleus taeniae; medial amygdala; ventromedial telencephalon
13.  Intraspecific Correlations of Basal and Maximal Metabolic Rates in Birds and the Aerobic Capacity Model for the Evolution of Endothermy 
PLoS ONE  2012;7(3):e34271.
The underlying assumption of the aerobic capacity model for the evolution of endothermy is that basal (BMR) and maximal aerobic metabolic rates are phenotypically linked. However, because BMR is largely a function of central organs whereas maximal metabolic output is largely a function of skeletal muscles, the mechanistic underpinnings for their linkage are not obvious. Interspecific studies in birds generally support a phenotypic correlation between BMR and maximal metabolic output. If the aerobic capacity model is valid, these phenotypic correlations should also extend to intraspecific comparisons. We measured BMR, Msum (maximum thermoregulatory metabolic rate) and MMR (maximum exercise metabolic rate in a hop-flutter chamber) in winter for dark-eyed juncos (Junco hyemalis), American goldfinches (Carduelis tristis; Msum and MMR only), and black-capped chickadees (Poecile atricapillus; BMR and Msum only) and examined correlations among these variables. We also measured BMR and Msum in individual house sparrows (Passer domesticus) in both summer, winter and spring. For both raw metabolic rates and residuals from allometric regressions, BMR was not significantly correlated with either Msum or MMR in juncos. Moreover, no significant correlation between Msum and MMR or their mass-independent residuals occurred for juncos or goldfinches. Raw BMR and Msum were significantly positively correlated for black-capped chickadees and house sparrows, but mass-independent residuals of BMR and Msum were not. These data suggest that central organ and exercise organ metabolic levels are not inextricably linked and that muscular capacities for exercise and shivering do not necessarily vary in tandem in individual birds. Why intraspecific and interspecific avian studies show differing results and the significance of these differences to the aerobic capacity model are unknown, and resolution of these questions will require additional studies of potential mechanistic links between minimal and maximal metabolic output.
doi:10.1371/journal.pone.0034271
PMCID: PMC3313994  PMID: 22479584
14.  Highly context-specific activation of the HPG axis in the dark-eyed junco and implications for the Challenge Hypothesis 
One of the best studied hormone-behavior interactions is the transient rise in testosterone (T) associated with male-male aggression. However, recent research on songbirds has demonstrated numerous exceptions to this pattern. One species previously thought to elevate T in response to a simulated territorial intrusion is the dark-eyed junco (Junco hyemalis). Here, we show that under most circumstances male juncos do not elevate circulating T or CORT levels in response to social stimuli, despite being physiologically capable of elevating T as indicated by their response to GnRH. The lack of hormonal response was found regardless of the sex of the social stimulus (singing male vs. soliciting female), its sensory modality (song only, song + live lure, song + taxidermic mount), or the timecourse of sampling. Notably, males did elevate T levels when exposed to a simulated territorial intrusion in the days following simulated predation of their chicks. Whether the high T seen in these narrow circumstances represents stage-dependent social modulation of T or re-activation of male reproductive physiology in preparation for re-nesting (i.e. socially independent T modulation) remains to be determined. It is clear, however, that activation of the HPG axis is highly context-specific for male juncos. These results highlight important and unresolved issues regarding the socially mediated component of the challenge hypothesis and how it relates to the evolution of hormone-mediated traits.
doi:10.1016/j.ygcen.2014.03.026
PMCID: PMC4097032  PMID: 24698788
challenge hypothesis; testosterone; social challenge; corticosterone; androgen responsiveness; simulated territorial intrusion; simulated courtship interaction
15.  Sandpipers (Scolopacidae) switch from monoester to diester preen waxes during courtship and incubation, but why? 
Recently, a shift in preen wax composition, from lower molecular weight monoesters to higher molecular weight diesters, was described for individuals of a sandpiper species (red knot, Calidris canutus) that were about to leave for the tundra breeding grounds. The timing of the shift indicated that diester waxes served as a quality signal during mate choice. Here, this hypothesis is evaluated on the basis of a survey of preen wax composition in 19 sandpiper species. All of these species showed the same shift observed in the high-Arctic breeding red knots. As the shift also occurred in temperate breeding species, it is not specific to tundra-breeding sandpipers. Both sexes produced the diester waxes during the incubation period until hatching, in addition to the short period of courtship, indicating that diesters' functions extend beyond that of a sexually selected 'make-up'. The few non-incubating birds examined (males of curlew sandpipers (C. ferruginea) and ruffs (Philomachus pugnax)) had the lowest likelihood of secreting diesters, indicating a functional role for diester preen waxes during incubation. We propose that diester preen waxes enhance olfactory crypticism at the nest.
doi:10.1098/rspb.2002.2132
PMCID: PMC1691136  PMID: 12396488
16.  Mechanistic Drivers of Flexibility in Summit Metabolic Rates of Small Birds 
PLoS ONE  2014;9(7):e101577.
Flexible metabolic phenotypes allow animals to adjust physiology to better fit ecological or environmental demands, thereby influencing fitness. Summit metabolic rate (Msum = maximal thermogenic capacity) is one such flexible trait. Skeletal muscle and heart masses and myocyte metabolic intensity are potential drivers of Msum flexibility in birds. We examined correlations of skeletal muscle and heart masses and pectoralis muscle citrate synthase (CS) activity (an indicator of cellular metabolic intensity) with Msum in house sparrows (Passer domesticus) and dark-eyed juncos (Junco hyemalis) to determine whether these traits are associated with Msum variation. Pectoralis mass was positively correlated with Msum for both species, but no significant correlation remained for either species after accounting for body mass (Mb) variation. Combined flight and leg muscle masses were also not significantly correlated with Msum for either species. In contrast, heart mass was significantly positively correlated with Msum for juncos and nearly so (P = 0.054) for sparrows. Mass-specific and total pectoralis CS activities were significantly positively correlated with Msum for sparrows, but not for juncos. Thus, myocyte metabolic intensity influences Msum variation in house sparrows, although the stronger correlation of total (r = 0.495) than mass-specific (r = 0.378) CS activity with Msum suggests that both pectoralis mass and metabolic intensity impact Msum. In contrast, neither skeletal muscle masses nor pectoralis metabolic intensity varied with Msum in juncos. However, heart mass was associated with Msum variation in both species. These data suggest that drivers of metabolic flexibility are not uniform among bird species.
doi:10.1371/journal.pone.0101577
PMCID: PMC4081579  PMID: 24992186
17.  Coccidial infection does not influence preening behavior in American goldfinches 
Acta Ethologica  2013;17(2):107-111.
Preening behavior in birds is important for the maintenance of thermoregulatory and ornamental functions of plumage. It has been repeatedly demonstrated that birds trade off time between plumage maintenance and other activities. However, the condition-dependent constraints of preening remain virtually unstudied. Here, we present the first experimental test of the hypothesis that intestinal parasite infection impairs preening activity. We studied male American goldfinches (Spinus tristis), a species with carotenoid-based plumage coloration. Following pre-alternate (spring) molt, we manipulated the health of males by infecting some birds with Isospora spp. coccidia and keeping others free of the infection. Although the goldfinches increased preening throughout the captive period, we found no significant effect of coccidial treatment on preening behavior. The effect of coccidia on plumage maintenance may be more pronounced under natural conditions where birds have limited access to food and engage in more activities that might limit time available for preening.
doi:10.1007/s10211-013-0159-z
PMCID: PMC4024122  PMID: 24882939
Feather soiling; Feather grooming; Parasites; Infection; Health
18.  Corticosterone excretion patterns and affiliative behavior over development in ravens (Corvus corax) 
Hormones and behavior  2007;53(1):208-216.
Averse effects of social stress may be buffered by the presence of social allies, which mainly has been demonstrated in mammals and recently also in birds. However, effects of socio-positive behavior prior to fledging in relation to corticosterone excretion in altricial birds have not been investigated yet. We here monitored corticosterone excretion patterns in three groups of hand raised juvenile ravens (n=5, 6 and 11) in the nest, post-fledging (May–July) and when ravens would be independent from their parents (September–November). We related these corticosterone excretion patterns to socio-positive behavior. Behavioral data were collected via focal sampling in each developmental period considered. We analyzed amounts of excreted immunoreactive corticosterone metabolites (CM) using enzyme immuno assays. We collected fecal samples in each developmental period considered and evaluated the most appropriate assay via an isolation stress experiment. Basal CM was significantly higher during the nestling period than post-fledging or when birds were independent. The time nestlings spent allopreening correlated negatively with mean CM. Post-fledging, individuals with higher CM levels sat close to (distance <50 cm) conspecifics more frequently and tended to preen them longer. When birds were independent and a stable rank hierarchy was established, dominant individuals were preened significantly longer than subordinates. These patterns observed in ravens parallel those described for primates, which could indicate that animal species living in a complex social environment may deal with social problems in a similar way that is not restricted to mammals or primates.
doi:10.1016/j.yhbeh.2007.09.021
PMCID: PMC4417709  PMID: 18022623
Ravens; Corvus corax; Corticosterone; Affiliative relationships; Enzyme immunoassay
19.  Feather bacterial load shapes the trade-off between preening and immunity in pigeons 
Background
Complex communities of bacteria inhabit the feathers of all birds. Under normal conditions, individuals maintain a healthy state by defending themselves against these potential invaders by preening. The immune system is only triggered when bacteria gain access into the body. Preening is, however, costly and may trade-off with investment in the immune system. To shed light on how birds balance the trade-off between immunity and preen secretions when facing high or low feather bacterial load, we experimentally manipulated feather bacteria load of feral pigeons (Columba livia), and investigated the effects on immune defenses.
Results
Birds facing high feather bacterial load had lower immune response to PHA skin-swelling test (a measure of induced pro-inflammatory capacity) than controls, while birds facing low feather bacterial load had higher blood bacterial killing ability (a measure of the capacity to eliminate bacterial pathogens) than controls. No other components of the immune system (i.e., hemagglutination and hemolysis capacity of plasma, primary and secondary responses to KLH and quantity of blood parasites) were found to be affected by feather bacterial load.
Conclusion
Pigeons had previously been shown to adjust preening to feather bacterial load. The decrease in the energetically costly inflammatory response of birds experiencing high bacterial load suggests a trade-off between investment in preen secretion and immunity and reinforces the idea that feather microbiota may have a strong impact on the ecology and evolution of the avian host.
doi:10.1186/s12862-015-0338-9
PMCID: PMC4392809  PMID: 25881311
Microbiota; PHA; Bacterial killing ability; Immune system; Pigeons; Columba livia
20.  Behavioral effects of social challenges and genomic mechanisms of social priming: What’s testosterone got to do with it? 
Current zoology  2014;60(6):791-803.
Social challenges from rival conspecifics are common in the lives of animals, and changes in an animal’s social environment can influence physiology and behavior in ways that appear to be adaptive in the face of continued social instability (i.e. social priming). Recently, it has become clear that testosterone, long thought to be the primary mediator of these effects, may not always change in response to social challenges, an observation that highlights gaps in our understanding of the proximate mechanisms by which animals respond to their social environment. Here, our goal is to address the degree to which testosterone mediates organismal responses to social cues. To this end, we review the behavioral and physiological consequences of social challenges, as well as their underlying hormonal and gene regulatory mechanisms. We also present a new case study from a wild songbird, the dark-eyed junco (Junco hyemalis), in which we find largely divergent genome-wide transcriptional changes induced by social challenges and testosterone, respectively, in muscle and liver tissue. Our review underscores the diversity of mechanisms that link the dynamic social environment with an organisms’ genomic, hormonal, and behavioral state. This diversity among species, and even among tissues within an organism, reveals new insights into the pattern and process by which evolution may alter proximate mechanisms of social priming.
doi:10.1093/czoolo/60.6.791
PMCID: PMC5054744  PMID: 27721823
social priming; challenge hypothesis; aggression; hormonal mechanism; testosterone; genomics
21.  Uropygial gland and bib colouration in the house sparrow 
PeerJ  2016;4:e2102.
Birds frequently signal different qualities by plumage colouration, mainly during mating. However, plumage colouration is determined during the moult, and therefore it would indicate the quality of individual birds during the moult, not its current quality. Recent studies, however, suggest that birds could modify plumage colouration by using cosmetic preen oil produced by the uropygial gland. In this study, I show that bib colouration is related to uropygial gland size and body condition in male house sparrows (Passer domesticus). Moreover, I conducted an experiment in which a group of sparrows were inoculated with an antigen, mimicking an illness. In control birds, short-term changes in bib colouration were related to both body condition and change in uropygial gland size. Therefore, birds that reduced uropygial gland size showed a greater colouration change. However, bib colouration did not change with the change in uropygial gland size in experimental birds inoculated with the antigen. Given that the experiment did not affect preen oil production or consumption, this finding tentatively suggests that the immune challenge provoked a change in the composition of preen oil, affecting its cosmetic properties. In short, the results of this study suggest that (1) male house sparrows produce cosmetic preen oil that alters the colouration of their bibs; (2) the more change in uropygial gland size, the more change in bib colouration; and (3) in this way, bib colouration has the potential to signal current health status, since less healthy birds showed less capacity to change bib colouration.
doi:10.7717/peerj.2102
PMCID: PMC4893339  PMID: 27280079
LPS; House sparrow; Mate choice; Cosmetic; Passer domesticus; Uropygial gland; Sexual selection
22.  Testosterone Affects Neural Gene Expression Differently in Male and Female Juncos: A Role for Hormones in Mediating Sexual Dimorphism and Conflict 
PLoS ONE  2013;8(4):e61784.
Despite sharing much of their genomes, males and females are often highly dimorphic, reflecting at least in part the resolution of sexual conflict in response to sexually antagonistic selection. Sexual dimorphism arises owing to sex differences in gene expression, and steroid hormones are often invoked as a proximate cause of sexual dimorphism. Experimental elevation of androgens can modify behavior, physiology, and gene expression, but knowledge of the role of hormones remains incomplete, including how the sexes differ in gene expression in response to hormones. We addressed these questions in a bird species with a long history of behavioral endocrinological and ecological study, the dark-eyed junco (Junco hyemalis), using a custom microarray. Focusing on two brain regions involved in sexually dimorphic behavior and regulation of hormone secretion, we identified 651 genes that differed in expression by sex in medial amygdala and 611 in hypothalamus. Additionally, we treated individuals of each sex with testosterone implants and identified many genes that may be related to previously identified phenotypic effects of testosterone treatment. Some of these genes relate to previously identified effects of testosterone-treatment and suggest that the multiple effects of testosterone may be mediated by modifying the expression of a small number of genes. Notably, testosterone-treatment tended to alter expression of different genes in each sex: only 4 of the 527 genes identified as significant in one sex or the other were significantly differentially expressed in both sexes. Hormonally regulated gene expression is a key mechanism underlying sexual dimorphism, and our study identifies specific genes that may mediate some of these processes.
doi:10.1371/journal.pone.0061784
PMCID: PMC3627916  PMID: 23613935
23.  Testosterone affects reproductive success by influencing extra-pair fertilizations in male dark-eyed juncos (Aves: Junco hyemalis) 
Monogamous male birds typically allocate less effort to courtship and more to parental behaviour than males of polygynous species. The seasonal pattern of testosterone (T) secretion varies accordingly. Monogamous males exhibit a spring peak in plasma T followed by lower levels during the parental phase, while males of polygynous species continue to court females and maintain T at higher levels. To determine whether testosterone underlies the trade-off between mating and parental effort, we treated male dark-eyed juncos (Junco hyemalis) with exogenous T and compared the reproductive success (RS) of T-treated males (T-males) to that of controls. T-males had lower apparent annual RS than controls, probably because elevated T reduced parental care. Nevertheless, annual genetic RS of the treatment groups was similar because (i) T-males suffered fewer losses in genetic RS due to extra-pair fertilizations (EPFs), and (ii) T-males gained more genetic RS through their own EPFs. This is the first hormonal manipulation of an avian phenotype shown to have influenced male RS through EPFs. Together with other studies, it suggests that testosterone may have mediated the evolution of inter- and intraspecific differences in allocation of reproductive effort to mate attraction and parental care.
doi:10.1098/rspb.1997.0223
PMCID: PMC1688731
Hormones Mating Systems Testosterone Reproductive Success Dna Fingerprinting Paternity
24.  Japanese Quail’s Genetic Background Modulates Effects of Chronic Stress on Emotional Reactivity but Not Spatial Learning 
PLoS ONE  2012;7(10):e47475.
Chronic stress is known to enhance mammals’ emotional reactivity and alters several of their cognitive functions, especially spatial learning. Few studies have investigated such effects in birds. We investigated the impact of a two-week stress on Japanese quail’s emotional reactivity and spatial learning. Quail is an avian model widely used in laboratory studies and for extrapolation of data to other poultry species. As sensitivity to chronic stress can be modulated by intrinsic factors, we tested juvenile female Japanese quail from three lines, two of them divergently selected on tonic immobility duration, an indicator of general fearfulness. The different emotional reactivity levels of quail belonging to these lines can be revealed by a large variety of tests. Half of the birds were submitted to repeated unpredictable aversive events for two weeks, whereas the other half were left undisturbed. After this procedure, two tests (open field and emergence tests) evaluated the emotional reactivity of treated and control quails. They were then trained in a T-maze for seven days and their spatial learning was tested. The chronic stress protocol had an impact on resting, preening and foraging in the home cage. As predicted, the emotional reactivity of treated quails, especially those selected for long tonic immobility duration, was higher. Our spatial learning data showed that the treatment enhanced acquisition but not memorization. However, intrinsic fearfulness did not seem to interact with the treatment in this test. According to an inverted U-shaped relationship between stress and cognition, chronic stress can improve the adaptability of birds to a stressful environment. We discussed the mechanisms possibly implied in the increase of emotional reactivity and spatial abilities.
doi:10.1371/journal.pone.0047475
PMCID: PMC3469497  PMID: 23071811
25.  Identification of avian wax synthases 
BMC Biochemistry  2012;13:4.
Background
Bird species show a high degree of variation in the composition of their preen gland waxes. For instance, galliform birds like chicken contain fatty acid esters of 2,3-alkanediols, while Anseriformes like goose or Strigiformes like barn owl contain wax monoesters in their preen gland secretions. The final biosynthetic step is catalyzed by wax synthases (WS) which have been identified in pro- and eukaryotic organisms.
Results
Sequence similarities enabled us to identify six cDNAs encoding putative wax synthesizing proteins in chicken and two from barn owl and goose. Expression studies in yeast under in vivo and in vitro conditions showed that three proteins from chicken performed WS activity while a sequence from chicken, goose and barn owl encoded a bifunctional enzyme catalyzing both wax ester and triacylglycerol synthesis. Mono- and bifunctional WS were found to differ in their substrate specificities especially with regard to branched-chain alcohols and acyl-CoA thioesters. According to the expression patterns of their transcripts and the properties of the enzymes, avian WS proteins might not be confined to preen glands.
Conclusions
We provide direct evidence that avian preen glands possess both monofunctional and bifunctional WS proteins which have different expression patterns and WS activities with different substrate specificities.
doi:10.1186/1471-2091-13-4
PMCID: PMC3316144  PMID: 22305293

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