Immune genotypes, immune responses, and survival in a wild bird population.

Individuals vary in their immune genotype, inbreeding coefficient f, immune responses, survival to adulthood, and adult longevity. However, whether immune genes predict survival or longevity, whether such relationships are mediated through immune responses, and how f affects immune genotype remain unclear. We use a wild song sparrow (Melospiza melodia) population in which survival to adulthood, adult longevity, and f were measured precisely, and in which immune responses have previously been assessed. We investigate four toll-like receptor (TLR) and the major histocompatibility complex (MHC) class IIB exon 2 genes. We test whether immune genes predict fitness (survival to adulthood or adult longevity); whether immune genes predict immune response; whether immune response predicts fitness and whether fitness, immune responses, or immune genotypes are correlated with f. We find that survival to adulthood is not associated with immune gene variation, but adult longevity is decreased by high MHC allele diversity (especially in birds that were relatively outbred), and by the presence of a specific MHC supertype. Immune responses were affected by specific immune genotypes. Survival to adulthood and adult longevity were not predicted by immune response, implying caution in the use of immune response as a predictor for fitness. We also found no relationship between f and immune genotype. This finding indicates that immune gene associations with longevity and immune response are not artefacts of f, and suggests that pathogen-mediated selection at functional loci can slow the loss of genetic variation arising from genetic drift and small population size.

Olfactory camouflage and communication in birds.

Smell is a sensory modality that is rarely considered in birds, but evidence is mounting that olfaction is an important aspect of avian behaviour and ecology. The uropygial gland produces an odoriferous secretion (preen oil) that can differ seasonally and between the sexes. These differences are hypothesized to function in olfactory camouflage, i.e. minimizing detection by nest predators (olfactory crypsis hypothesis), and/or intraspecific olfactory communication, particularly during breeding (sex semiochemical hypothesis). However, evidence for seasonal and sex differences in preen oil is mixed, with some studies finding differences and others not, and direct evidence for the putative function(s) of seasonal variation and sex differences in preen oil remains limited. We conducted a systematic review of the evidence for such changes in preen oil chemical composition, finding seasonal differences in 95% of species (57/60 species in 35 studies) and sex differences in 47% of species (28/59 species in 46 studies). We then conducted phylogenetic comparative analyses using data from 59 bird species to evaluate evidence for both the olfactory crypsis and sex semiochemical hypotheses. Seasonal differences were more likely in the incubating than non-incubating sex in ground-nesting species, but were equally likely regardless of incubation strategy in non-ground-nesting species. This result supports the olfactory crypsis hypothesis, if ground nesters are more vulnerable to olfactorily searching predators than non-ground nesters. Sex differences were more likely in species with uniparental than biparental incubation and during breeding than non-breeding, consistent with both the olfactory crypsis and sex semiochemical hypotheses. At present, the data do not allow us to disentangle these two hypotheses, but we provide recommendations that will enable researchers to do so.

Stronger population differentiation at infection-sensing than infection-clearing innate immune loci in songbirds: Different selective regimes for different defenses.

Parasite-mediated selection is widespread at loci involved in immune defense, but different defenses may experience different selective regimes. For defenses involved in clearing infections, purifying selection favoring a single most efficacious allele likely predominates. However, for defenses involved in sensing and recognizing infections, evolutionary arms races may make positive selection particularly important. This could manifest primarily within populations (e.g., balancing selection maintaining variation) or among them (e.g., spatially varying selection enhancing population differences in allele frequencies). We genotyped three toll-like receptors (TLR; involved in sensing infections) and three avian beta-defensins (involved in clearing infections) in 96 song sparrows (Melospiza melodia) from three breeding populations that differ in disease resistance. Variation-based indicators of selection (proportion of variable sites, proportion of nonsynonymous SNPs, proportion of sites bearing signatures of positive or purifying selection, rare allele frequencies) did not differ appreciably between the two locus types. However, differentiation was generally higher at infection-sensing than infection-clearing loci. Allele frequencies differed markedly at TLR3, driven by a variant predicted to alter protein function. Geographically structured variants at infection-sensing loci may reflect local adaptation to spatially heterogeneous parasite communities. Selective regimes experienced by infection-sensing versus infection-clearing loci may differ primarily due to parasite-mediated population differentiation.

Preen gland microbiota of songbirds differ across populations but not sexes.

Metabolites produced by symbiotic microbes can affect the odour of their hosts, providing olfactory cues of identity, sex or other salient features. In birds, preen oil is a major source of body odour that differs between populations and sexes. We hypothesized that population and sex differences in preen oil chemistry reflect underlying differences in preen gland microbiota, predicting that these microbes also differ among populations and between the sexes. We further predicted that pairwise similarity in the community composition of preen gland microbiota would covary with that of preen oil chemical composition, consistent with the fermentation hypothesis for chemical recognition. We analysed preen oil chemistry and preen gland bacterial communities of song sparrows Melospiza melodia. Birds were sampled at sites for which population and sex differences in preen oil have been reported, and at a third site that has been less studied. Consistent with prior work in this system, we found population and sex differences in preen oil chemistry. By contrast, we found population differences but not sex differences in the community composition of preen gland microbes. Overall similarity in the community composition of preen gland microbiota did not significantly covary with that of preen oil chemistry. However, we identified a subset of six microbial genera that maximally correlated with preen oil composition. Although both preen gland microbiota and preen oil composition differ across populations, we did not observe an overall association between them that would implicate symbiotic microbes in mediating variation in olfactory cues associated with preen oil. Instead, certain subsets of microbes may be involved in mediating olfactory cues in birds, but experiments are required to test this.

Many loci make light work: High individual diversity despite low population diversity and random mating at class I MHC in a Critically Endangered island songbird.

Multi-cellular organisms are under constant attack from parasites, making immune defence a critical aspect of fitness. In vertebrate animals, genes of the major histocompatibility complex (MHC) determine the breadth of pathogens to which individuals can respond. Having many MHC alleles can confer better protection against infectious disease, and balancing selection at MHC is widespread. Indeed, MHC loci are famously variable, with some populations harbouring thousands of alleles (Biedrzycka et al., 2018; Robinson, Soormally, Hayhurst, & Marsh, 2016). MHC has also long fascinated behavioural ecologists because mate choice-for example, preferring MHC-dissimilar partners-may amplify the effects of natural selection (Penn & Potts, 1999). But despite keen interest in the evolutionary ecology of MHC, extensive duplication (Minias, Pikus, Whittingham, & Dunn, 2019) has made these genes challenging to study. In a From the Cover article in this issue of Molecular Ecology, Stervander, Dierickx, Thorley, Brooke, and Westerdahl (2020) characterizes class I MHC in a Critically Endangered songbird, relating genotype to mate choice and survivorship. By inferring copy number and patterns of allelic co-segregation, the authors pave the way to elucidating the genomic architecture of MHC in this bottlenecked population. These insights help reconcile apparently counterintuitive findings: no effect of MHC genotype on mate choice or survival, and high MHC diversity within individuals despite low diversity at the population level. The latter finding is cause for optimism regarding conservation prospects. Moreover, these results suggest that ancient duplication events can have longstanding effects on the adaptive landscapes of natural and sexual selection.

"Balancing" balancing selection? Assortative mating at the major histocompatibility complex despite molecular signatures of balancing selection.

In vertebrate animals, genes of the major histocompatibility complex (MHC) determine the set of pathogens to which an individual's adaptive immune system can respond. MHC genes are extraordinarily polymorphic, often showing elevated nonsynonymous relative to synonymous sequence variation and sharing presumably ancient polymorphisms between lineages. These patterns likely reflect pathogen-mediated balancing selection, for example, rare-allele or heterozygote advantage. Such selection is often reinforced by disassortative mating at MHC. We characterized exon 2 of MHC class II, corresponding to the hypervariable peptide-binding region, in song sparrows (Melospiza melodia). We compared nonsynonymous to synonymous sequence variation in order to identify positively selected sites; assessed evidence for trans-species polymorphisms indicating ancient balancing selection; and compared MHC similarity of socially mated pairs to expectations under random mating. Six codons showed elevated ratios of nonsynonymous to synonymous variation, consistent with balancing selection, and we characterized several alleles similar to those occurring in at least four other avian families. Despite this evidence for historical balancing selection, mated pairs were significantly more similar at MHC than were randomly generated pairings. Nonrandom mating at MHC thus appears to partially counteract, not reinforce, pathogen-mediated balancing selection in this system. We suggest that in systems where individual fitness does not increase monotonically with MHC diversity, assortative mating may help to avoid excessive offspring heterozygosity that could otherwise arise from long-standing balancing selection.

Wax Ester Composition of Songbird Preen Oil Varies Seasonally and Differs between Sexes, Ages, and Populations.

Chemical signaling has been well studied in invertebrates and mammals but less so in birds, due to the longstanding misconception that olfaction is unimportant or even non-existent in this taxon. However, recent findings suggest that olfaction plays an important role in avian mate choice and reproductive behavior, similar to other taxa. The leading candidate source for compounds involved in avian chemical communication is preen oil, a complex mixture secreted from the uropygial gland. Preen oil contains volatile compounds and their potential wax ester precursors, and may act as a reproductive chemosignal. Reproductive signals are generally sexually dimorphic, age-specific, seasonally variable, and may also vary geographically. We tested whether preen oil meets these expectations by using gas chromatography to examine the wax ester composition of preen oil in song sparrows (Melospiza melodia). We found that the wax ester composition of preen oil was significantly different between sexes, age classes, seasons, and populations. Collectively, our results suggest that song sparrow preen oil meets the criteria of a chemical cue that may influence mate choice and reproduction. Our findings in song sparrows, which are sexually monomorphic in plumage, also parallel patterns described for dark-eyed juncos (Junco hyemalis), a closely related songbird with sexually dimorphic plumage. Behavioral tests are needed to confirm that song sparrows attend to the cues present in preen oil, but our findings support the increasingly accepted idea that chemical communication is common and widespread in birds as it is in other taxa.

Purifying Selection in the Toll-Like Receptors of Song Sparrows Melospiza melodia.

Variation in immune gene sequences is known to influence resistance to infectious diseases and parasites, and hence survival and mate choice, across animal taxa. Toll-like receptors (TLRs) comprise one essential gene family in the vertebrate innate immune system and recognize evolutionarily conserved structures from all major microorganism classes. However, the causes and consequences of TLR variation in passerine birds remain largely unexplored. We examined 7 TLR genes in song sparrows (Melospiza melodia), a species that is studied across North America. We then examined sequences from 4 unduplicated TLRs (TLR1LB, TLR3, TLR4, and TLR15) from birds in 2 parts of the species' range (N = 27, N = 6), tested for evidence of selection, and conducted pilot analyses of the role of TLR heterozygosity in survival. We identified 45 SNPs: 19 caused changes in amino acid sequences and 2 of these were likely deleterious. We found no evidence of codon-level episodic positive selection but detected purifying selection at codons in all TLRs. Contrary to expectations we found no strong correlation between heterozygosity at TLRs and inbreeding coefficient f (estimate ± standard error [SE] = -0.68 ± 0.37, Radj2 = 0.08, F1,25 = 3.38, P = 0.08). In addition, pilot analyses revealed no relationship between TLR heterozygosity and survival (ß ± SE: 0.09 ± 2.00, P = 0.96), possibly due to small sample size. Further analyses of genetic diversity in TLRs are likely to advance understanding of the effects of innate immune gene diversity on the fitness and persistence of wild populations.

Exposing migratory sparrows to Plasmodium suggests costs of resistance, not necessarily of infection itself.

Migratory birds move through multiple habitats and encounter a diverse suite of parasites. This raises concern over migrants' role in transporting infectious disease between breeding and wintering grounds, and along migratory flyways. Trade-offs between flight and immune defenses could interfere with infected individuals' migratory timing and success, potentially affecting infection dynamics. However, experimental evidence that parasitic infection affects migratory preparation or timing remains scant. We hypothesized that birds encountering hematozoan parasites shortly before migration incur physical costs (reduced body condition) and behavioral costs (delayed migration), due to the infection itself and/or to the demands of mounting an immune response. We experimentally inoculated song sparrows (Melospiza melodia) with Plasmodium shortly before fall migration. We monitored infection and body composition for 2 weeks after inoculation, and used radiotelemetry to track timing of migratory departure for another 7 weeks after release. Inoculated individuals that resisted infection had lower lean mass 12 days post exposure, relative to controls and infected individuals. This suggests trade-offs between body composition and immune defenses that might reduce migration success of resistant individuals. Despite group differences in body composition prior to release, we did not detect significant differences in timing of migration departure several weeks later. Thus, malarial infection did not appear to incur detectable costs to body composition or to migratory timing, at least when exposure occurs several weeks before migration. This study is novel considering not only the costs of infection, but also the costs of resisting infection, in an experimental context.

Population Differences at MHC Do Not Explain Enhanced Resistance of Song Sparrows to Local Parasites.

Infectious disease represents an emerging threat to natural populations, particularly when hosts are more susceptible to novel parasites (allopatric) than to parasites from the local area (sympatric). This pattern could arise through evolutionary processes (host populations become adapted to their local parasites and genetically differentiated from other populations at immune-related loci) and/or through ecological interactions (host individuals develop resistance to local parasites through previous exposure). The relative importance of these candidate mechanisms remains unclear. In jawed vertebrates, genes of the major histocompatibility complex (MHC) play a fundamental role in immunity and are compelling candidates for spatially varying selection. We recently showed that song sparrows (Melospiza melodia) are more susceptible to allopatric than to sympatric strains of malaria (Plasmodium). In the current study, to determine whether population differences at MHC explain this pattern, we characterized the peptide-binding regions of MHC (classes I and II) of birds that did or did not become infected in the previous experiment. We recovered up to 4 alleles per individual at class I, implying at least 2 loci, and up to 26 alleles per individual at class II, implying at least 13 loci. Individuals with more class I alleles were less likely to become infected by Plasmodium, consistent with parasite-mediated balancing selection. However, we found no evidence for population genetic differentiation at either class of MHC, based on 36 individuals sequenced. Resistance to sympatric parasites previously described for this system likely stems from individuals' prior immune experience, not from population differentiation and locally protective alleles at MHC.

Immune profiles vary seasonally, but are not significantly related to migration distance or natal dispersal, in a migratory songbird.

A central tenet of ecoimmunology is that an organism's environment shapes its optimal investment in immunity. For example, the benefits of acquired (relatively pathogen specific) versus innate (nonspecific) immune defenses are thought to vary with the risk of encountering familiar versus unfamiliar pathogens. Because pathogen communities vary geographically, individuals that travel farther during seasonal migration or natal dispersal are predicted to have higher exposure to novel pathogens, and lower exposure to familiar pathogens, potentially favoring investment in innate immunity. During the breeding season, migratory animals' exposure to familiar pathogens should increase, potentially favoring investment in acquired immunity. We hypothesized that song sparrows Melospiza melodia adjust their constitutive immune profiles in response to risk of encountering novel versus familiar pathogens. We predicted that individuals migrating longer distances (inferred from stable hydrogen isotope analysis of claws) and less philopatric individuals (inferred from microsatellite assignment testing) would rely more heavily on acquired than innate defenses. We also predicted that reliance on acquired defenses would increase throughout the early breeding season. Consistent with trade-offs between acquired and innate defenses, levels of immunoglobulin Y (acquired) varied negatively with macrophage phagocytosis activity (innate). Levels of acquired relative to innate immunity did not vary significantly with migration distance or philopatry, but increased throughout the early breeding season. Macrophage phagocytosis was not significantly repeatable between years. Song sparrows appear to shift from innate defenses immediately after migration to acquired defenses with increasing time at the breeding grounds. These patterns highlight the plasticity of constitutive immune defenses in migratory animals.

Song sparrows Melospiza melodia have a home-field advantage in defending against sympatric malarial parasites.

Hosts and parasites interact on both evolutionary and ecological timescales. The outcome of these interactions, specifically whether hosts are more resistant to their local parasites (sympatric) than to parasites from another location (allopatric), is likely to affect the spread of infectious disease and the fitness consequences of host dispersal. We conducted a cross-infection experiment to determine whether song sparrows (Melospiza melodia) have an advantage in dealing with sympatric parasites. We captured birds from two breeding sites 437 km apart, and inoculated them with avian malaria (Plasmodium spp.) cultured either from their capture site or from the other site. Infection risk was lower for birds exposed to sympatric than to allopatric Plasmodium lineages, suggesting that song sparrows may have a home-field advantage in defending against local parasite strains. This pattern was more pronounced at one capture site than at the other, consistent with mosaic models of host-parasite interactions. Home-field advantage may arise from evolutionary processes, whereby host populations become adapted to their local parasites, and/or from ecological interactions, whereby host individuals develop resistance to the local parasites through previous immune exposure. Our findings suggest that greater susceptibility to novel parasites may represent a fitness consequence of natal dispersal.

Testosterone, migration distance, and migratory timing in song sparrows Melospiza melodia.

In seasonally migratory animals, migration distance often varies substantially within populations such that individuals breeding at the same site may overwinter different distances from the breeding grounds. Shorter migration may allow earlier return to the breeding grounds, which may be particularly advantageous to males competing to acquire a breeding territory. However, little is known about potential mechanisms that may mediate migration distance. We investigated naturally-occurring variation in androgen levels at the time of arrival to the breeding site and its relationship to overwintering latitude in male and female song sparrows (Melospiza melodia). We used stable isotope analysis of hydrogen (δ(2)H) in winter-grown claw tissue to infer relative overwintering latitude (migration distance), combined with 14years of capture records from a long-term study population to infer the arrival timing of males versus females. Relative to females, males had higher circulating androgen levels, migrated shorter distances, and were more likely to be caught early in the breeding season. Males that migrate short distances may benefit from early arrival at the breeding grounds, allowing them to establish a breeding territory. Even after controlling for sex and date, androgen levels were highest in individuals that migrated shorter distances. Our findings indicate that androgens and migration distance are correlated traits within and between sexes that may reflect individual variation within an integrated phenotype in which testosterone has correlated effects on behavioral traits such as migration.

Early-life stress has sex-specific effects on immune function in adult song sparrows.

Multiple components of the immune system are modulated by environmental factors, including exposure to stressors. In particular, chronic stressors can impair development of the immune system, leading to alterations in immune function in adulthood. While these effects have been well established in mammals, less is known about how developmental stress modulates immunity in nonmammalian species. We determined the long-term effects of exposure to early-life stressors on immunity in song sparrows including the swelling response to phytohemagglutinin (PHA) and several measures of constitutive innate immunity. Song sparrows were reared in captivity from 3 d of age and exposed to control conditions, food restriction, or corticosterone (CORT) treatment. Males exposed to food restriction or CORT treatment had less swelling of the wing web in response to PHA than control males; however, neither treatment affected the swelling response to PHA in females. The treatments also had sex-specific effects on constitutive innate immune function. Specifically, CORT-treated males had lower antimicrobial capacity toward a strain of the bacterium E. coli but higher antimicrobial activity toward a strain of the fungus Candida albicans compared to food-restricted or control males. In contrast, neither treatment affected constitutive innate immunity in females. These results suggest that male and female song sparrows may differ in how they allocate resources to development of the immune system when reared in stressful or food-limited conditions.

Developmental stress, condition, and birdsong: a case study in song sparrows.

Sexual-selection theory posits that ornaments and displays can reflect a signaler's condition, which in turn is affected both by recent and developmental conditions. Moreover, developmental conditions can induce correlations between sexually selected and other traits if both types of traits exhibit developmental phenotypic plasticity in response to stressors. Thus, sexually selected traits may reflect recent and/or developmental characteristics of signalers. Here, we review data on the relationships between birdsong, a sexually selected trait, and developmental and current condition of birds from a long-term study of a population of song sparrows (Melospiza melodia). Field studies of free-living birds indicate that the complexity of a male's songs, a permanent trait, reflects the size of a song-control region of his brain (HVC), and is correlated with body size and several parameters of immunity, specifically investment in protective proteins. However, the performance of a male's songs, a dynamic trait, is not correlated to immune investment. Complexity of song is correlated with the glucocorticoid stress-response, and in some years response to stress predicts overwinter survival. Experimental manipulations have revealed that stressors in early life impair development of HVC, but that HVC recovers in size by adulthood. These manipulations result in impaired song-complexity and song-learning, but not song-performance. Experimental developmental stressors also affect growth, endocrine physiology, metabolism, and immune-function, often in a sex-specific manner. Combined, these studies suggest that song-complexity provides reliable information about early developmental experience, and about other traits that have critical developmental periods. Birdsong thus provides a multi-faceted sexually selected trait that may be an indicator both of developmental and recent conditions.

Developmental timing of signals affects information content: song complexity but not consistency reflects innate immune strategy in male song sparrows.

In short-lived animals, innate immunity is an important component of fitness and quality. Although receivers cannot generally assess a signaler's immune function directly, sexually selected displays such as birdsong may reflect past or current condition. We investigated the degree to which song complexity and consistency, thought to reflect condition over different developmental timescales, predict multiple aspects of innate immunity in male song sparrows (Melospiza melodia). We also investigated correlations among immune measures. Noncellular components of innate immunity (soluble blood proteins including natural antibody and other protective proteins) were negatively related to cellular (phagocytosis-based) components, suggesting trade-offs within innate immune protection. This pattern underscores the risk of inferring "immunocompetence" from a single metric. Song complexity, a permanent trait in this species, was positively related to noncellular relative to cellular immune components and may thus provide information as to the singer's innate immune strategy (investment in noncellular vs. cellular activity). Such a relationship could arise through shared timing of song learning and antibody repertoire development in early life. Singing consistency, thought to track variation in current condition and measured at both whole-song and syllable scales, did not predict any immune measures. Developmental timing of signals thus appears to influence their information content.

Developmental programming of the HPA and HPG axes by early-life stress in male and female song sparrows.

Variation in early environmental conditions can have long-term effects on physiology and behavior, a process referred to as developmental programming. In particular, exposure to early-life stressors can have long-term effects on regulation of the hypothalamic-pituitary-adrenal (HPA) and hypothalamic-pituitary-gonadal (HPG) axes. Although these effects have been well documented in mammals, less is known about how early-life stress affects regulation of these endocrine systems in non-mammalian species. In the current study, we determined the long-term effects of early-life food restriction or corticosterone (CORT) treatment on the HPA axis of song sparrows (Melospiza melodia), including the responses to restraint stress, dexamethasone challenge, and ACTH challenge. In addition, we assessed long-term effects on the HPG axis by measuring sex steroid levels (testosterone in males and 17ß-estradiol in females) before and after a gonadotropin-releasing hormone (GnRH) challenge. Subjects treated with CORT during development had larger increases in CORT in response to ACTH challenge than food-restricted or control subjects. Neither treatment affected the responses of CORT to restraint or dexamethasone. CORT-treated males also had higher initial testosterone levels, but neither treatment affected testosterone levels post-GnRH. Lastly, although GnRH challenge failed to increase circulating estradiol levels in females, females exposed to food restriction or CORT treatment had lower estradiol levels than control females. These results show that exposure to stress can developmentally program the endocrine system of songbirds and illustrate the importance of considering developmental conditions when determining the factors responsible for inter-individual variation in endocrine regulation.

HPA axis regulation, survival, and reproduction in free-living sparrows: Functional relationships or developmental correlations?

A growing body of theoretical and empirical work has addressed the relationship between hypothalamus-pituitary-adrenal (HPA) function and fitness. For example, the corticosterone (CORT)-fitness and CORT-condition hypotheses predict that baseline and/or stress-induced levels of glucocorticoids should relate to fitness, and recent empirical studies have reported relationships between HPA function and fitness-related sexually selected traits. Here we introduce a framework for evaluating whether such relationships reflect functional relationships or developmental correlations. We then address this framework using data from a free-living population of song sparrows (Melospiza melodia). In two independent studies we have found that song complexity (a sexually selected trait) is correlated with stress reactivity: males with more complex vocal repertoires show reduced CORT response to standardized restraint stress. This pattern likely results from the early life environment concurrently affecting development of both song and the HPA axis. Suppression of CORT by dexamethasone was also correlated to measures of body condition and immune function, and females paired to males with higher stress-induced levels of CORT initiated egg-laying later. Finally, stress reactivity predicted overwinter survival in one year, although not in another. Thus, the relationship between HPA axis function and fitness likely varies temporally and by context. Some fitness-related traits may be functionally related to HPA regulation, but many others may be related through developmental correlation.

Developmental stress has sex-specific effects on nestling growth and adult metabolic rates but no effect on adult body size or body composition in song sparrows.

Variation in the prenatal and postnatal environments can have long-term effects on adult phenotype. In humans and other animals, exposure to stressors can lead to long-term changes in physiology. These changes may predispose individuals to disease, especially disorders involving energy metabolism. In addition, by permanently altering metabolic rates and energy requirements, such effects could have important fitness consequences. We determined the effects of early-life food restriction and corticosterone (CORT) treatment on growth and adult body size, body composition (assessed via quantitative magnetic resonance) and metabolic rates in the song sparrow, Melospiza melodia. Nestlings were hand-raised in captivity from 3 days of age. Treatments (ad libitum food, food restriction or CORT treatment) lasted from day 7 to day 60. Both experimental treatments had sex-specific effects on growth. In the nestling period, CORT-treated males weighed more than controls, whereas CORT-treated females weighed less than controls. Food-restricted males weighed the same as controls, whereas food-restricted females weighed less than controls. Both experimental treatments also had sex-specific effects on standard metabolic rate (SMR). Females exposed to food restriction or CORT treatment during development had higher SMRs in adulthood than control females, but neither stressor affected SMR in males. There were no effects of either treatment on adult body size, body composition (lean or fat mass) or peak metabolic rate. Therefore, early-life stress may have sex-specific programming effects on metabolic rates and energy expenditure in song sparrows. In addition, both treatments affected nestling growth in a manner that exaggerated the typical sex difference in nestling mass, which could provide male nestlings with a competitive advantage over their sisters when developing in a poor-quality environment.

Regulation of the HPA axis is related to song complexity and measures of phenotypic quality in song sparrows.

Regulation of the hypothalamic-pituitary-adrenal (HPA) axis is a key component of the vertebrate stress response. Prior studies have found that variation in HPA responses were correlated to measures of fitness and physiological condition. In addition, sexually-selected traits have also been found to correlate to measures of condition. The proximate mechanisms responsible for such covariation between sexually selected traits and measures of quality are unclear, but could involve variation in HPA regulation. We investigated whether HPA activity is related to song complexity, body size/condition and leukocyte profiles in wild male song sparrows (Melospiza melodia). We characterized three aspects of HPA activity: 1) response to restraint stress; 2) negative feedback, assessed by the ability of exogenous dexamethasone to suppress corticosterone levels; and 3) adrenal sensitivity to exogenous adrenocorticotropic hormone (ACTH). Birds with lower responses to restraint stress had more complex song and more heterophils and higher heterophil to lymphocyte (H:L) ratios. Birds with more effective negative feedback were larger and had fewer heterophils and lower H:L ratios, suggesting lower levels of physiological stress or infection. We observed no relationship between adrenal sensitivity to exogenous ACTH and any of the factors. These findings illustrate important relationships between HPA activity, song complexity, and morphological and physiological traits. Song complexity may thus provide receivers with information about the ability of the singer to cope with stressors.