Immediate and long-term effects of testosterone on song plasticity and learning in juvenile song sparrows

Steroid sex hormones play critical roles in the development of brain regions used for vocal learning. It has been suggested that puberty-induced increases in circulating testosterone (T) levels crystallize a bird's repertoire and inhibit future song learning. Previous studies show that early administration of T crystallizes song repertoires but have not addressed whether new songs can be learned after this premature crystallization. We brought 8 juvenile song sparrows (Melospiza melodia) into the laboratory in the late summer and implanted half of them with subcutaneous T pellets for a two week period in October. Birds treated with T tripled their singing rates and crystallized normal songs in 2 weeks. After T removal, subjects were tutored by 4 new adults. Birds previously treated with T tended toward learning fewer new songs post T, consistent with the hypothesis that T helps to close the song learning phase. However, one T-treated bird proceeded to learn several new songs in the spring, despite singing perfectly crystallized songs in the fall. His small crystallized fall repertoire and initial lag behind other subjects in song development suggest that this individual may have had limited early song learning experience. We conclude that an exposure to testosterone sufficient for crystallization of a normal song repertoire does not necessarily prevent future song learning and suggest that early social experiences might override the effects of hormones in closing song learning.     

Individual variation in response to simulated territorial challenge among territory-holding song sparrows

Lack (1946) suggested that male songbirds exhibit consistent individual differences in the vigor or manner in which they defend their territories against intrusion. The causes and consequences of such individual variation have not been incorporated into models of territoriality, however, because of a lack of experimental data confirming Lack's suggestion. In this paper, we test the possibility that male song sparrows Melospiza melodia who are successful territory holders differ consistently in the vigor with which they defend their territory, by conducting repeated song playback trials with the same set of territory-holding subjects across a breeding season. We found only relatively weak seasonal trends in responsiveness: the amount birds sang in response to playback increased significantly across the breeding season and responsiveness was generally lower when a male's social mate was egg laying. By contrast, we found extensive variation among males in how closely they approached a simulated territorial intrusion. These individual differences remained significantly consistent across four rounds of playback trials that spanned the breeding season as determined by Kendall's coefficient of concordance. Our results confirm that some individual song sparrows are consistently more vigorous than others in territory defense, at least in one conspicuous aspect of their behavior, and suggest that further work is needed to understand the nature and consequences of variation in patterns of defense among successful territory holders.     

Correlations between song acquisition, song production, and plasma levels of testosterone and estradiol in sparrows

Male birdsong is a sexually dimorphic behavior characterized by learned dialects. In a combined study of learning in relation to steroid levels in the plasma, changes in estradiol and testosterone levels were correlated with the timing of the sensitive period for song acquisition and with successive stages in song development. Male swamp sparrows were trained with a changing series of live singing tutors from 26 days to 1 year of age. Song acquisition was concentrated between 26 and 47 days of age (57%). By 85 days of age 71% of acquisition was completed; some occurred as late as 300 days. There were two major periods when testosterone levels were elevated. The first, from 30-80 days, encompassed most of the period of song acquisition. The second, from 260 to at least 360 days of age, coincided with song development. Estradiol levels were elevated from 18 to 170 days of age, encompassing almost all of the period of song acquisition. A marked estradiol peak between 40 and 50 days coincided with a trough in testosterone levels and a hiatus in song acquisition. The strong correlation between the second period of elevated testosterone and song motor development suggests a causal connection, with levels peaking in mid-development and declining during mature song production. Estradiol levels were elevated at the start of the study and remained so during early subsong production, from 30 to 165 days. They then fell to baseline, remaining there throughout the resumption of subsong and plastic song production at 250-326 days. Both estradiol and testosterone are candidates for possibly affecting song acquisition.     

Male song sparrows Melospiza melodia do not announce their female's fertility

We tested the fertility announcement hypothesis, whereby male song during a female's fertile period functions as both a paternity guard and an advertisement for extra-pair copulations, in an eastern population of song sparrows Melospiza melodia over two broods within a breeding season. Our results did not support one of its main predictions: male song rate was not significantly higher in the female's fertile period than in her post-fertile period. Song rate peaked prior to pairing, when males were establishing territories and trying to attract females. Once paired, song rate dropped by a factor of about ten, and was consistently low through all stages of the nesting cycle. Males who failed to pair continued singing at high rates throughout the breeding season. Our results do not support the fertility announcement hypothesis, therefore song rate is not used primarily as a paternity assurance strategy by song sparrows.     

Geographic song discrimination in relation to dispersal distances in song sparrows

Whether geographic variation in signals actually affects communication between individuals depends on whether discriminable differences in signals occur over distances that individuals move in their lifetimes. We measure the ability of song sparrows (Melospiza melodia) to discriminate foreign from local songs using foreign songs recorded at a series of increasing distances and compare the results with previous measurements of dispersal distances. We test discrimination in males using playback of songs on territories and measuring approach and in females using playback to estradiol-treated captives and measuring courtship display. Females fail to discriminate against foreign songs recorded at 18 km but do discriminate against foreign songs recorded at 34, 68, 135, and 540 km. Males fail to discriminate against foreign songs recorded at 18, 34, 68, 135, and 270 km but do discriminate against foreign songs from 540 km. Females are more discriminating, but even they do not discriminate at a distance three times the root-mean-square dispersal distance, as estimated from mtDNA variation. We suggest that female preference for local songs benefits females not because it allows them to reject foreign males but because accurate production of local song serves as a test of song-learning ability.     

Alternative forms of song matching in song sparrows

Song matching, replying to a song with a similar song, occurs in many songbird species. Almost all investigations of song matching have been of type matching, where one bird's reply is unambiguously similar to the other's song (i.e. the same song type). In many populations, however, neighbours do not share song types, and therefore cannot type-match. We hypothesized that a bird lacking a true type match could still song-match a stimulus song with a song from his repertoire that was similar in some way the birds recognized. We tested this hypothesis in song sparrows, Melospiza melodia, in two playback experiments. We played the subject a stranger song that was similar to one or more of his songs, but a type match to none of them. In the first experiment, we used playback songs that began with two buzzes (‘double-buzz’ songs). In the second experiment, we used songs that began with a slow trill that increased in tempo ('speed-up' songs). Birds replied at rates significantly above chance with their own double-buzz, or speed-up song match to the respective types of playback. The results suggest that birds who do not share true song types, can still song-match each other. This broad-sense form of song matching may also occur in populations with low song type sharing. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Female Lincoln's sparrows modulate their behavior in response to variation in male song quality

Sexually reproducing organisms should mate with the highest quality individuals that they can. When female songbirds choose a mate, they are thought to use several aspects of male song that reflect his quality. Under resource-limited environmental conditions, male Lincoln's sparrows (Melospiza lincolnii) vary among one another in several aspects of song quality, including song length, song complexity, and trill performance. In a 2-pronged approach, we tested whether variation in song quality of male Lincoln's sparrows influences the behavior of females that are in a reproductive-like state. Over two trials, we exposed females to songs from the high and low ends of the distribution of naturally occurring song quality variation and found a higher level of behavioral activity in females exposed to high-quality songs, especially when they had first been exposed to low-quality songs. We also examined female phonotaxis toward antiphonally played songs with experimentally elevated and reduced trill performance and found that females moved preferentially toward the songs with elevated trill performance. Contrary to most studies investigating the behavioral responses of wild, female songbirds to variation in male song, we obtained our results without administering exogenous estradiol, which can artificially perturb the female's physiology. Our results demonstrate that the behavior of female Lincoln's sparrows is modulated by the quality of male songs to which they are exposed and that trill performance plays a significant role in this behavioral modulation. Furthermore, as the order of song quality presentation matters, it appears that recent song experience also influences female behavior.     

Male response to historical and geographical variation in bird song

In many species, individuals discriminate among sexual signals of conspecific populations in the contexts of mate choice and male–male competition. Differences in signals among populations (geographical variation) are in part the result of signal evolution within populations (temporal variation). Understanding the relative effect of temporal and geographical signal variation on signal salience may therefore provide insight into the evolution of behavioural discrimination. However, no study, to my knowledge, has compared behavioural response to historical signals with response to current signal variation among populations. Here, I measured the response of male white-crowned sparrows (Zonotrichia leucophrys) to historical songs compared with current songs from their local population, a nearby non-local population and a distant population. Males responded most strongly to current local songs, less, but equally, to historical local and current non-local songs, and least to songs of the distant population. Moreover, response to both temporal and geographical variation in song was proportional to how much songs differed acoustically from current local songs. Signal evolution on an ecological time scale appears to have an effect on signal salience comparable to differences found between current neighbouring populations, supporting the idea that behavioural discrimination among learned signals of conspecific populations can evolve relatively rapidly.     

Long-term maternal effect on offspring immune response in song sparrows Melospiza melodia

Knowledge of the causes of variation in host immunity to parasitic infection and the time-scales over which variation persists, is integral to predicting the evolutionary and epidemiological consequences of host-parasite interactions. It is clear that offspring immunity can be influenced by parental immune experience, for example, reflecting transfer of antibodies from mothers to young offspring. However, it is less clear whether such parental effects persist or have functional consequences over longer time-scales, linking a parent's previous immune experience to future immune responsiveness in fully grown offspring. We used free-living song sparrows (Melospiza melodia) to quantify long-term effects of parental immune experience on offspring immune response. We experimentally vaccinated parents with a novel antigen and tested whether parental vaccination influenced the humoral antibody response mounted by fully grown offspring hatched the following year. Parental vaccination did not influence offspring baseline antibody titres. However, offspring of vaccinated mothers mounted substantially stronger antibody responses than offspring of unvaccinated mothers. Antibody responses did not differ between offspring of vaccinated and unvaccinated fathers. These data demonstrate substantial long-term effects of maternal immune experience on the humoral immune response of fully grown offspring in free-living birds.     

Species song discrimination in adult female song and swamp sparrows

Six female song sparrows (Melospiza melodia) and six female swamp sparrows (Melospiza georgiana) were treated with oestradiol, and their response to song measured by frequency and intensity of copulation-solicitation display. Test stimuli were synthetic songs composed of either song sparrow or swamp sparrow syllables assembled in either song-sparrow-like or swamp-sparrow-like temporal patterns. Female song sparrows responded preferentially to songs containing their own species' syllables and to songs containing their own species' temporal patterns. Swamp sparrows were also sensitive to both syllable type and temporal, pattern, in contrast to male swamp sparrows, which show no preference for swamp sparrow temporal patterns.     

Territory establishment,song learning strategies and survival in song sparrows

In most songbirds, the processes of song learning and territory establishment overlap in the early life and a young bird usually winds up with songs matching those of his territorial neighbors in his first breeding season. In the present study, we examined the relationships among the timing of territory establishment, the pattern of song learning and territorial success in a sedentary population of song sparrows (Melospiza melodia). Males in this population tend to learn their songs from their neighbors and consequently they show high song sharing with neighbors and use these shared songs preferentially in interactions with them. Males also show significant variation in the timing of territory establishment, ranging from their natal summer to the next spring. Using a three-year dataset, we found that the timing of territory establishment did not systematically affect the composition of the song repertoire of the tutee: early establishers and late establishers learned equally as much from their primary tutors and had a similar number of tutors and similar repertoire sizes, nor did timing of territory establishment affect subsequent survival on territory. Therefore, the song-learning program of song sparrows seems versatile enough to lead to high song sharing even for birds that establish territories relatively late.     

Stress,song and survival in sparrows

The stress response—increases in circulating glucocorticoids following a stressor—is typically considered adaptive, but few studies address the fitness consequences of individual variation in stress response. Generally, due to negative consequences of prolonged elevation of glucocorticoids, animals should have a transient stress response just sufficient to cope with the stressor. In rodents, stress responsiveness is affected by early developmental experience, and hyper-responsiveness to stress is linked to morbidity and mortality. We assessed individual variation in stress responses in free-living song sparrows, Melospiza melodia, in relation to fitness-related measures including song and overwinter survival. Birds with greater increases in corticosterone 30 min following restraint stress were less likely to return to breed the following year. Stress responsiveness was also correlated with song complexity: males with fewer syllables in their song repertoires had greater stress reactivity. Our findings support the hypothesis that developmental stressors both impair song development and affect the adult stress response. Thus, individual variation in the stress response may relate to variation in fitness.     

Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia)

The consequences of inbreeding for host immunity to parasitic infection have broad implications for the evolutionary and dynamical impacts of parasites on populations where inbreeding occurs. To rigorously assess the magnitude and the prevalence of inbreeding effects on immunity, multiple components of host immune response should be related to inbreeding coefficient (f) in free-living individuals. We used a pedigreed, free-living population of song sparrows (Melospiza melodia) to test whether individual responses to widely used experimental immune challenges varied consistently with f. The patagial swelling response to phytohaemagglutinin declined markedly with f in both females and males in both 2002 and 2003, although overall inbreeding depression was greater in males. The primary antibody response to tetanus toxoid declined with f in females but not in males in both 2004 and 2005. Primary antibody responses to diphtheria toxoid were low but tended to decline with f in 2004. Overall inbreeding depression did not solely reflect particularly strong immune responses in outbred offspring of immigrant-native pairings or weak responses in highly inbred individuals. These data indicate substantial and apparently sex-specific inbreeding effects on immune response, implying that inbred hosts may be relatively susceptible to parasitic infection to differing degrees in males and females.     

Seasonal changes in song nuclei and song behavior in Gambel's white-crowned sparrows

In males of several songbird species, the morphology of forebrain nuclei that control song changes seasonally. The only seasonally breeding songbird in which seasonal changes in the structure of song control nuclei have been reported not to occur is the nonmigratory Nuttall's subspecies of white-crowned sparrow. In the present study, we manipulated photoperiod and plasma testosterone concentrations in captive male white-crowned sparrows of the migratory Gambel's subspeices. Males exposed to photoperiods and plasma testosterone concentrations typical of those experienced by wild breeding males had larger song control nuclei than males held on a winter photoperiod. We also found seasonal change in stereotypy of spectral and temporal parameters of song in wild Gambel's white-crowned sparrows. We hypothesize that seasonal changes in song control nuclei may correlate with seasonal changes in song stereotypy. © 1995 John Wiley & Sons, Inc.     

From song dialects to speciation in white‐crowned sparrows

The behavioural signals used in mate selection are a key component in the evolution of premating isolating barriers and, subsequently, the formation of new species. The importance of mating signals has a long tradition of study in songbirds, where many species differ in their song characteristics. In oscine songbirds, individual birds usually learn their songs from a tutor. Mistakes during learning can help generate geographic dialects, akin to those within human language groups. In songbirds, dialect differences can often be substantial and there is an intuitive connection between the evolution of song amongst populations at a small scale, and the more substantive song differences between bird species and presumably used in species recognition. However, studies investigating the concordance between putative genetic and behavioural boundaries have generated mixed results. In many cases, this is possibly a function of the poor resolving power of the genetic markers employed. In this issue of Molecular Ecology, Lipshutz et al. ( 2017 ) combine genomic markers with a robust behavioural assay to address the importance of song variation amongst white‐crowned sparrow (Zonotrichia leucophrys) subspecies.     

The fitness consequences of honesty: Under‐signalers have a survival advantage in song sparrows

How honest or reliable signaling can evolve and be maintained has been a major question in evolutionary biology. The question is especially puzzling for a particular class of signals used in aggressive interactions: threat signals. Here, we report a study on song sparrows (Melospiza melodia) in which we assayed males with playbacks on their territories to quantify their aggressiveness (flights and close proximity) and aggressive signaling levels (rates of soft song, a close‐range signal reliably predicting attack) and asked whether these traits affect individuals’ survival on territory. We found that the effect of aggressive signaling via soft song interacted with aggressive behaviors such that there was a negative correlational selection: among males with low aggression, those males that signaled at higher levels (over‐signalers) had higher survival whereas among males with high aggression those that signaled at low levels (under‐signalers) survived longer. In other words, males that deviate from reliable signaling have a survival advantage. These results, along with previous research that suggested most of the deviation from reliable signaling in this system is in the form of under‐signaling (high‐aggression males signaling at low levels) pose a puzzle for future research on how this reliable signaling system is maintained.     

Response to neighbors and strangers by capuchin monkeys (Cebus apella)

Capuchin monkeys in the laboratory were observed when another monkey was introduced to their group. The introduced monkey was either from a hostile neighboring group; from a completely strange group, or from the host group. Attacks were directed primarily toward strange males but were rare. The results were discussed in terms of the neighbor effect, mere exposure theory, and species differences in responses to strangers.     

Species song discrimination in choice experiments with territorial male swamp and song sparrows

Playbacks of synthetic and normal songs were used to determine what song parameters are important to species song recognition by territorial male swamp sparrows (Melospiza georgiana) and song sparrows (Melospiza melodia). Syllable morphology influences the discrimination of conspecific song from song sparrow song in adult swamp sparrows, but temporal pattern does not; this result duplicates that found in studies of song learning of the young in this species. Species song recognition is influenced by both syllable morphology and temporal pattern in adult song sparrows, in contrast to the situation in young sparrows, which seem not to distinguish their own species' song from that of swamp sparrows on either cue.