Keith W. Sockman

Yolk androgens reduce offspring survival

Females may favour some offspring over others by differential deposition of yolk hormones. In American kestrels (Falco sparverius), we found that yolks of eggs laid late in the sequence of a clutch had more testosterone (T) and androstenedione (A4) than yolks of first–laid eggs. To investigate the effects of these yolk androgens on nestling ‘fitness’, we injected both T and A4 into the yolks of first–laid eggs and compared their hatching time, nestling growth and nestling survival with those of first–laid eggs in which we injected vehicle as a control. Compared to controls, injection of T and A4 at a dose intended to increase their levels to those of later–laid eggs delayed hatching and reduced nestling growth and survival rates. Yolk androgen treatment of egg 1 had no effect on survival of siblings hatching from subsequently laid eggs. The adverse actions of yolk androgen treatment in the kestrel are in contrast to the favourable actions of yolk T treatment found previously in canaries (Serinus canaria). Additional studies are necessary in order to determine whether the deposition of yolk androgens is an adaptive form of parental favouritism or an adverse by–product of endocrine processes during egg formation. Despite its adaptive significance, such ‘transgenerational’ effects of steroid hormones may have helped to evolutionarily shape the hormonal mechanisms regulating reproduction.

Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition

How much effort to expend in any one bout of reproduction is among the most important decisions made by an individual that breeds more than once. According to life-history theory, reproduction is costly, and individuals that invest too much in a given reproductive bout pay with reduced reproductive output in the future. Likewise, investing too little does not maximize reproductive potential. Because reproductive effort relative to output can vary with predictable and unpredictable challenges and opportunities, no single level of reproductive effort maximizes fitness. This leads to the prediction that individuals possessing behavioural mechanisms to buffer challenges and take advantage of opportunities would incur fitness benefits. Here, we review evidence in birds, primarily of altricial species, for the presence of at least two such mechanisms and evidence for and against the seasonal coordination of these mechanisms through seasonal changes in plasma concentrations of the pituitary hormone prolactin. First, the seasonal decline in clutch size of most bird species may partially offset a predictable seasonal decline in the reproductive value of offspring. Second, establishing a developmental sibling-hierarchy among offspring may hedge against unpredictable changes in resource availability and offspring viability or quality, and minimize energy expenditure in raising a brood. The hierarchy may be a product, in part, of the timing of incubation onset relative to clutch completion and the rate of yolk androgen deposition during the laying cycle. Because clutch size should influence the effects of both these traits on the developmental hierarchy, we predicted and describe evidence in some species that females adjust the timing of incubation onset and rate of yolk androgen deposition to match clutch size. Studies on domesticated precocial species reveal an inhibitory effect of the pituitary hormone prolactin on egg laying, suggesting a possible hormonal basis for the regulation of clutch size. Studies on the American kestrel (Falco sparverius) and other species suggest that the seasonal increase in plasma concentrations of prolactin may regulate both a seasonal advance in the timing of incubation onset and a seasonal increase in the rate of yolk androgen deposition. These observations, together with strong conceptual arguments published previously, raise the possibility that a single hormone, prolactin, functions as the basis of a common mechanism for the seasonal adjustment of reproductive effort. However, a role for prolactin in regulating clutch size in any species is not firmly established, and evidence from some species indicates that clutch size may not be coupled to the timing of incubation onset and rate of yolk androgen deposition. A dissociation between the regulation of clutch size and the regulation of incubation onset and yolk androgen deposition may enable an independent response to the predictable and unpredictable challenges and opportunities faced during reproduction.

Recent experience modulates forebrain gene–expression in response to mate–choice cues in European starlings

Mate–choice decisions can be experience dependent, but we know little about how the brain processes stimuli that release such decisions. Female European starlings (Sturnus vulgaris) prefer males with long–bout songs over males with short–bout songs, and show higher expression of the immediate early gene (IEG) ZENK in the auditory forebrain when exposed to long–bout songs than when exposed to short–bout songs. We exposed female starlings to a short–day photoperiod for one of three durations and then, on an increased photophase, exposed them to one week of long–bout or short–bout song experience. We then examined their IEG response to novel long–bout versus novel short–bout songs by quantifying ZENK protein in two song–processing areas: the caudo–medial hyperstriatum ventrale and the caudo–medial neostriatum. ZENK expression in both areas increased with tenure on short–day photoperiods, suggesting that short days sensitize females to song. The ZENK response bias toward long–bout songs was greater in females with long–bout experience than in females with short–bout experience, indicating that the forebrain response bias toward a preferred trait depends on recent experience with that category of trait. This surprising level of neuroplasticity is immediately relevant to the natural history and fitness of the organism, and may underlie a mechanism for optimizing mate–choice criteria amidst locally variable distributions of secondary sexual characteristics.

Sex-specific effects of yolk-androgens on growth of nestling American kestrels

Maternally derived androgen hormones concentrate in avian egg yolks as the yolks grow on the female’s ovary, possibly forming a basis for important maternal effects in birds. In the American kestrel (Falco sparverius), experimental elevation of yolk androgens in the first-laid egg of a clutch (a-egg) to the concentrations found naturally in a clutch’s later-laid eggs reduces the growth rate of a-egg nestlings compared to controls. These findings, together with discoveries from other species that the effects of yolk androgens on growth of female nestlings may differ from their effects on growth of male nestlings, raise the hypothesis that natural changes in yolk-androgen concentrations with laying order are ultimately due to a difference between the sexes in their yolk-androgen sensitivity and between early- and late-laid eggs in their sex ratio. By re-analyzing previously published data and adding to the analysis data from previously unanalyzed blood samples used for sex determination, we investigated possible sex-specific effects of yolk-androgens in the context of a potential sex-biased laying order in free-living American kestrels. We used a multi-level, mixed model with a Gompertz function to analyze growth of nestlings hatching from a-eggs that were control-treated or in which we experimentally elevated yolk-androgen concentrations shortly after laying to the higher concentrations naturally found in later-laid eggs. We discovered that male nestlings were more susceptible than female nestlings to growth inhibition by yolk-androgen elevation but did not find a bias in sex ratio with respect to laying order. Together, these findings do not support the above hypothesis. However, they are consistent with the hypothesis that sex differences in yolk-androgen sensitivity enable mothers to economically tune reproductive effort to an individual offspring’s reproductive value, which can vary more for one sex than the other.

The Role of Prolactin in the Regulation of Clutch Size and Onset of Incubation Behavior in the American Kestrel

In most bird species, the timing of incubation onset may influence the degree of hatching asynchrony, which, together with variation in clutch size, affects reproductive success. In some domesticated species that usually show no hatching asynchrony, plasma prolactin concentrations in females rise with the onset of incubation and the end of laying, and this rise enhances incubation behavior and may terminate laying. To investigate whether a rise in prolactin during laying is involved in the regulation of clutch size and incubation onset in a species with hatching asynchrony, we measured plasma concentrations of immunoreactive prolactin (ir-prolactin) in laying American kestrels, Falco sparverius, and quantified clutch size and incubation behavior. In a separate study, we administered one of three concentrations of ovine prolactin (o-prolactin) via osmotic pumps implanted in females when egg 2 of a clutch was laid. ir-Prolactin concentrations during laying were higher in small than in large clutches and increased in parallel with the development of incubation behavior. o-Prolactin treatment enhanced incubation behavior, but did not affect clutch size, possibly because the manipulation was performed after clutch size had already been determined. Consistent with studies on domesticated species that show synchronous hatching, our results indicate that rising prolactin during laying enhances the expression of incubation behavior in a species that shows hatching asynchrony. Further studies are necessary to determine whether the relationship between prolactin and clutch size in the American kestrel is one of causation or of mere association.

Nest Predation in the Mountain White-Crowned Sparrow

Predation was the largest cause of failure in 1,132 Zonotrichia leucophrys oriantha nests, followed by desertion and inclement weather. Mean annual predation rate was 29.9% and did not vary significantly over the 19 years of the study. This was attributed to the presence of a large, stable population of Beldings ground squirrels, a known predator on Z. 1. oriantha nests. Predation rate was highest during the nestling period, next highest during laying, and lowest during incubation. Mean daily predation rate for the whole nesting cycle was 2.0% per day. Investigator activities at nests frequently caused desertion during laying but seldom thereafter. These activities may have attracted predators on occasion but no convincing, pervasive effect could be demonstrated. Antipredator behaviors included several distraction displays and seasonal shifts in nest locations from above-ground to ground and from pines to willows. Predators at the nest were vigorously attacked but usually to no avail. Nest predation rates did not vary with parental age nor with clutch size.

The integration of song environment by catecholaminergic systems innervating the auditory telencephalon of adult female European starlings

Mate choice is among the most consequential decisions a sexually reproducing organism can make. In many songbird species, females make mate‐choice decisions based, in part, on variation between males in songs that reflect their quality. Importantly, females may adjust their choice relative to the prevalence of high quality songs. In European starlings (Sturnus vulgaris), females prefer males that primarily sing long songs over those that primarily sing short songs, and sensitivity of the auditory telencephalon to song length depends on the prevalence of long songs in the environment. Several lines of evidence suggest a role for noradrenergic innervation of the auditory telencephalon in mediating this neuro‐ and behavioral plasticity. To simulate variation in quality of the song environment, we exposed adult female starlings to 1 week of either long or short songs and then quantified several monoamines and their metabolites in the caudomedial mesopallium and caudomedial nidopallium (NCM) using high performance liquid chromatography. We also used immunocytochemistry to assess these areas for immunoreactive dopamine‐β‐hydroxylase (DBH‐ir), the enzyme that synthesizes norepinephrine. We found that long songs elevated levels of the principal norepinephrine metabolite, the principal dopamine metabolite, and the probability of DBH‐ir in the NCM compared to short songs. Song environment did not appear to influence norepinephrine or dopamine levels. Thus, the quality of the song environment regulates the local secretion of catecholamines, particularly norepinephrine, in the female auditory telencephalon. This may form a basis for plasticity in forebrain sensitivity and mate‐choice behavior based on the prevalence of high‐quality males.

Estradiol-dependent catecholaminergic innervation of auditory areas in a seasonally breeding songbird

A growing body of evidence suggests that gonadal steroids such as estradiol (E2) alter neural responses not only in brain regions associated with reproductive behavior but also in sensory areas. Because catecholamine systems are involved in sensory processing and selective attention, and because they are sensitive to E2 in many species, they may mediate the neural effects of E2 in sensory areas. Here, we tested the effects of E2 on catecholaminergic innervation, synthesis and activity in the auditory system of white‐throated sparrows, a seasonally breeding songbird in which E2 promotes selective auditory responses to song. Non‐breeding females with regressed ovaries were held on a winter‐like photoperiod and implanted with silastic capsules containing either no hormone or E2. In one hemisphere of the brain, we used immunohistochemistry to quantify fibers immunoreactive for tyrosine hydroxylase or dopamine beta‐hydroxylase in the auditory forebrain, thalamus and midbrain. E2 treatment increased catecholaminergic innervation in the same areas of the auditory system in which E2 promotes selectivity for song. In the contralateral hemisphere we quantified dopamine, norepinephrine and their metabolites in tissue punches using HPLC. Norepinephrine increased in the auditory forebrain, but not the midbrain, after E2 treatment. We found that evidence of interhemispheric differences, both in immunoreactivity and catecholamine content that did not depend on E2 treatment. Overall, our results show that increases in plasma E2 typical of the breeding season enhanced catecholaminergic innervation and synthesis in some parts of the auditory system, raising the possibility that catecholamines play a role in E2‐dependent auditory plasticity in songbirds.

Annual variation in vocal performance and its relationship with bill morphology in Lincoln's sparrows, Melospiza lincolnii

Morphology may affect behavioural performance through a direct, physical link or through indirect, secondary mechanisms. Although some evidence suggests that the bill morphology of songbirds directly constrains vocal performance, bill morphology may influence vocal performance through indirect mechanisms also, such as one in which morphology influences foraging and thus the ability to perform some types of vocal behaviour. This raises the possibility for ecologically induced variation in the relationship between morphology and behaviour. To investigate this, I used an information theoretic approach to examine the relationship between bill morphology and several measures of vocal performance in Lincolns sparrows (Melospiza lincolnii). I compared this relationship between two breeding seasons that differed markedly in ambient temperatures, phenology of habitat maturation, and food abundance. I found a strong curvilinear relationship between bill shape (height/width) and vocal performance in the seemingly less hospitable season but not in the other, leading to a difference between seasons in the populations mean vocal performance. Currently, I do not know the cause of this annual variation. However, it could be due to the effects of bill shape on foraging and therefore on time budget, energy balance, or some other behavioural or physiological response that manifests mostly under difficult environmental conditions or, alternatively, to associations between male quality and both vocal performance and bill shape. Regardless of the cause, these results suggest the presence of an indirect, ecologically mediated link between morphology and behavioural performance, leading to annual variation in the prevailing environment of acoustic signals.

Prior Experience with Photostimulation Enhances Photo-Induced Reproductive Development in Female European Starlings: A Possible Basis for the Age-Related Increase in Avian Reproductive Performance

Abstract Reproductive performance in female birds improves with age, and this is generally attributed to experiences obtained during breeding. In temperate-zone species, experience with photostimulation during the first breeding year may prime the hypothalamo-pituitary-gonadal axis to respond to photic cues more rapidly or robustly in subsequent years. To test this idea, we captured 32 photorefractory juvenile (hence naive to photostimulation) female European starlings (Sturnus vulgaris) and held half of them (naive group) on a photoperiod of 8L:16D for 32 wk and the other half (experienced group) on 8L:16D for 12 wk, 16L:8D for 12 wk, and then 8L:16D for 8 wk. When we subsequently transferred all birds to 16L:8D, the increase in body mass, which may presage egg laying in the wild, was more robust in experienced than in naive females. Experienced females also showed a more robust elevation in plasma concentrations of the yolk-precursor protein vitellogenin, although naive females showed an initial rapid but transient rise in vitellogenin that we attribute to their extended exposure to short-day photoperiods prior to photostimulation. Finally, the photo-induced increase in diameter of the largest ovarian follicle, in plasma concentrations of luteinizing hormone, and in the number of septo-preoptic fibers relative to the number of cell bodies immunoreactive to GnRH was greater in experienced than in naive females. Thus, prior experience with photostimulation enhances some initial phases of photo-induced reproductive development and may explain, in part, why reproductive performance improves with age in temperate-zone birds.