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.     

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.     

Time course of changes in Gambel's white-crowned sparrow song behavior following transitions in breeding condition

Seasonal changes in behavior and in its underlying neural substrate are common across animal taxa. These changes are often triggered by steroid sex hormones. Song in seasonally breeding songbirds provides an excellent example of this phenomenon. In these species, dramatic seasonal changes mediated by testosterone and its metabolites occur in adult song behavior and in the neural circuitry controlling song. While song rate can quickly change in response to seasonal breeding cues, it is unknown how quickly other aspects of song change, particularly the stereotypy of song phonology and syntax. In this study we determined whether and how quickly song rate, phonology, and syntax change in response to breeding and non-breeding physiological cues. We asked these questions using Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii), a closed-ended learner with well-characterized changes in the neural circuitry controlling song behavior. We exposed ten photosensitive sparrows to long-day photoperiod and implanted them with subcutaneous testosterone pellets (day 0) to simulate breeding conditions. We continuously recorded song and found that song rate increased quickly, reaching maximum around day 6. The stereotypy of song phonology changed more slowly, reaching maximum by day 10 or later. Song syntax changed minimally after day 6, the earliest time point examined. After 21 days, we transitioned five birds from breeding to non-breeding condition. Song rate declined precipitously. These results suggest that while song rate changes quickly, song phonology changes more slowly, generally following or in parallel with previously investigated changes in the neural substrate.     

Seasonality in song behaviour revisited: seasonal and annual variants and invariants in the song of the domesticated canary (Serinus canaria)

The song of the domesticated canary (Serinus canaria) is one of the most widely used models to study the neural correlates of behavioural plasticity and the mechanisms of female mate choice. However, only few studies have described the song behaviour in detail and monitored their changes throughout the year, and these data are restricted to the “Waterslager” strain. Here, we studied the song characteristics of the male common domesticated canary at different times of the year, the spring breeding and autumnal non-breeding season, and monitored the birds' songs up to the following breeding season. During breeding, males have increased plasma levels of testosterone, and songs are on average longer and consist of fewer non-repeated syllable types compared to the non-breeding season. When subsequent seasons are compared, song duration and the proportion of non-repeated syllable types change seasonally but not across years. Repertoire size remains constant throughout seasons although syllable types are exchanged. Syllable carry-over is significantly higher from one breeding season to the next than between the breeding and non-breeding season. Further, the repertoire of the breeding season contains more potentially sexually attractive syllable types than that of the non-breeding season. These data show that overall song structure is retained throughout the year while seasonality occurs in the temporal pattern and in repertoire composition.     

Seasonal changes in avian song control circuits do not cause seasonal changes in song discrimination in song sparrows

In seasonally breeding songbirds, brain nuclei of the song control system that act in song perception change in size between seasons. It has been hypothesized that seasonal regression of song nuclei may impair song discrimination. We tested this hypothesis in song sparrows (Melospiza melodia), a species in which males share song types with neighbors and must discriminate between similar songs in territorial interactions. We predicted that song sparrows with regressed song systems would have greater difficulty in discriminating between similar songs. Sparrows were housed either on short days (SD) and had regressed song circuits, or were exposed to long days and implanted with testosterone (LD+T) to induce full growth of the song circuits. We conducted two experiments using a GO/NO-GO operant conditioning paradigm to measure song discrimination ability of each group. Birds learned four (experiment 1) or three (experiment 2) pairs of song types sequentially, with each pair more similar in the number of shared song elements and thus more difficult to discriminate. Circulating T levels differed between the SD and LD+T groups. The telencephalic song nuclei HVc, RA, and area X were larger in the LD+T birds. The two groups of sparrows did not differ, however, in their ability to learn to discriminate between shared song types, regardless of the songs' similarity. These results suggest that seasonal changes in the song control system do not affect birds' ability to make difficult song discriminations.     

Coordinated and dissociated effects of testosterone on singing behavior and song control nuclei in canaries (Serinus canaria)

Temperate zone songbirds that breed seasonally exhibit pronounced differences in reproductive behaviors including song inside and outside the breeding season. Springlike long daylengths are associated with increases in plasma testosterone (T) concentrations, as well as with increases in singing and in the volume of several brain nuclei known to control this behavior. The mechanisms whereby T can induce changes in behavior and brain, and whether or not these effects are differentially regulated, have recently begun to be examined, as has the question of the relative contributions of T and its androgenic and estrogenic metabolites to the regulation of this seasonal behavioral and neural plasticity. In this experiment, we examined the effects of T, 5alpha-dihydrotestosterone, or 17beta-estradiol treatment on castrated male canaries housed on short days and compared neural and behavioral effects in these males to similarly-housed males given only blank implants. We observed that only T treatment was effective in eliciting significant increases in singing behavior after 11 days of hormone exposure. In addition, T alone was effective in increasing the volume of a key song production nucleus, HVC. However, at this time, none of the steroids had any effects on the volumes of two other song control nuclei, Area X of the medial striatum and the robust nucleus of the arcopallium (RA), that are efferent targets of HVC, known to be regulated by androgen in canaries and also to play a role in the control of adult song. T can thus enhance singing well before concomitant androgen-induced changes in the song control system are complete.     

The role of androgen receptors in regulating territorial aggression in male song sparrows

This paper examines the role that androgen receptors (ARs) play in modulating aggressive behavior in male song sparrows, Melospiza melodia morphna. Song sparrows are seasonally breeding, territorial birds that maintain year-round territories with male-female pair bonds formed during the spring breeding season. Plasma testosterone levels peak as territories are established and mates acquired. In late summer, testosterone levels fall and remain basal during the non-breeding season. We examined the role of ARs in regulating territorial aggression in captive song sparrows under short- and long-day conditions as well as just prior to, and at the start of the breading season in freely living birds using the nonsteroidal antiandrogen flutamide to block AR function. Birds were implanted with either empty or drug filled silastic implants for 18 to 42 days and then challenged with a novel male decoy to assess the individual birds level of male-male aggression. Freely living birds remained on their home territory and underwent a simulated territorial intrusion, whereas laboratory-held birds were assessed using a laboratory simulated territorial intrusion and remained in their home cage. Experimental treatment of male song sparrows decreased aggressive behavior during the pre-breeding life history substage (March-April) in freely living birds as well as in laboratory-held birds under long-day (16L:8D) conditions. During the early breeding substage (April-May) there was no measurable effect of flutamide treatment on aggressive behavior, nor was there a difference in behavior in the (8L:16D) laboratory birds. This demonstrates that ARs are an important component of the neuroendocrine control of aggressive behavior. Given that flutamide only affected aggression during the pre-breeding substage and in LD birds, the results suggest that AR dependent control of aggressive behavior changes as song sparrow life history states change.     

A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning

Adult songbirds can incorporate new neurons into HVc, a telencephalic song control nucleus. Neuronal incorporation into HVc is greater in the fall than in the spring in adult canaries (open‐ended song learners) and is temporally related to seasonal song modification. We used the western song sparrow, a species that does not modify its adult song, to test the hypothesis that neuronal incorporation into adult HVc is not seasonally variable in age‐limited song learners. Wild song sparrows were captured during the fall and the spring, implanted with osmotic pumps containing [³H]thymidine, released onto their territories, and recaptured after 30 days. The density, proportion, and number of new HVc neurons were all significantly greater in the fall than in the spring. There was also a seasonal change in the incorporation of new neurons into the adjacent neostriatum that was less pronounced than the change in HVc. This is the first study of neuronal recruitment into the song control system of freely ranging wild songbirds. These results indicate that seasonal changes in HVc neuronal incorporation are not restricted to open‐ended song learners. The functional significance of neuronal recruitment into HVc therefore remains elusive. © 1999 John Wiley & Sons, Inc. J Neurobiol 40: 316–326, 1999     

Song Motor control organizes acoustic patterns on two levels in Bengalese finches (<Emphasis Type="Italic">Lonchura striata</Emphasis> var. <Emphasis Type="Italic">domestica</Emphasis>)

Based on statistical analyses of song sequences, Bengalese finch (Lonchura striata var. domestica) songs do not show unvarying motif repetition as has been found in zebra finches (Taeniopygia guttata). Instead, there are variations of partially stereotyped sequences of song syllables. Although these stereotyped sequences consist of multiple syllables, in most cases these syllables occur together. To examine whether such structures really exist as a vocal production unit, we subjected singing birds to a light flash and determined when the stimulus stopped the songs. When light interruptions were presented within the statistically stereotyped sequences, the subsequent syllables tended to be produced, whereas interruptions presented during the statistically variable sequences tended to cause instantaneous song termination. This suggests that the associations among the song syllables that compose the statistically stereotyped sequences are more order dependent than those for the statistically variable sequences, and the tolerances of syllable pairs to visual interruptions are consistent with the statistical song structures. Additionally, following interruptions, several types of song sequence variations were observed that had not been previously reported. These phenomena might be caused by various effects of the visual stimulus on the hierarchical motor control program.     

Seasonal changes of blood values in Rufous-collared sparrows from high and low altitude

Haematocrit, red blood cell (RBC) count, haemoglobin (Hb) concentration, and plasma solids concentration, were measured in populations ofZonotrichia capensis captured during different seasons of the year at altitudes ranging from sea level up to 3500 m. Winter blood values of birds from high and low altitude proved not to be significantly different. Similar results were obtained during summertime, with the exception of cell Hb content and concentration, which were about 10% higher in low-altitude birds. Seasonal changes in RBC size and number appear to be better correlated with the prevailing summer and winter conditions than with the particular altitudinal distribution of the examined populations.     

Genetic and phenotypic correlations in a natural population of song sparrows

We estimated heritabilities, and genetic and phenotypic correlations between beak and body traits in the song sparrow ( Melospiza melodia ). We compared these estimates to values for the same traits in the Galápagos finches, Geospiza (Boag, 1983; Grant, 1983). Morphological variance is low in the song sparrow, and our results show that genetic and phenotypic correlations are considerably lower than correlations in the morphologically more variable Geospiza. Comparison using a larger sample of Galapagos populations confirms the existence of an association between variance and correlation for phenotypic values. We suggest two possible explanations for this association. First, most traits studied are functionally related, and the joint evolution of variance and correlation may have resulted from stabilizing selection about a line of optimal allometry between traits. Alternatively, introgression between populations and species could have caused correlation and variance to evolve jointly. Both selection and introgression were probably influential in producing the observed pattern, but it is not possible to estimate their relative importance with current data. Genetic and phenotypic correlations were correlated in the song sparrow, but heritabilities of traits varied greatly. As a result, the genetic variance-covariance matrix for traits is not simply a constant multiple of the phenotypic matrix. Evolutionary response to natural selection cannot, therefore, be predicted from the measurement of phenotypic characteristics alone.     

树麻雀肝脏和肌肉产热特征的季节性变化

北温带的小型鸟类,通过增加产热来适应低温环境.基础代谢率(BMR)是内温动物能量预算的重要组成部分.本研究中我们分别在冬季和夏季测定了树麻雀(Passer montanus)的BMR、肝脏和肌肉的线粒体蛋白含量、线粒体呼吸及细胞色素C氧化酶(COX)活力及血清中甲状腺激素(T4)及甲状腺原氨酸(T3)含量的变化.结果显示:树麻雀的体重和BMR冬季显著高于夏季;肝脏的线粒体呼吸、肝脏和肌肉的COX活力冬季较高,夏季较低;血清T3浓度冬季明显高于夏季.这些结果表明:在野外条件下,肝脏和肌肉在细胞水平产热能力的提高和血清T3含量的增加,是树麻雀抵御冬季寒冷的重要方式之一.     

Seasonal changes in testosterone levels in wild Mexican cottontails Sylvilagus cunicularius

We studied serum testosterone levels in the endemic Mexican cottontail, Sylvilagus cunicularius, which has been reported to show seasonal breeding. Animals were trapped in the wild and in a field enclosure in the National Park La Malinche in central Mexico over a period of five years. Serum testosterone (T) levels were quantified by ELISA from blood samples. T levels of adult males were lowest around 4 months after the onset of the annual reproductive season and were already high prior to the onset of breeding. As expected, the T levels of adult females were consistently lower than in males, and there were no differences in T level with respect to female reproductive state. There were no detectable sex-specific differences in juveniles and subadults, but there was a marked increase in T levels between juvenile and adult males. Overall, our study clearly reflects and confirms the seasonal breeding strategy of this species, showing high similarities to the much better studied European rabbit.     

Seasonal variation in gastric myoelectrical activity in young Japanese females

In order to test our hypothesis that there is seasonal variation in digestion and absorption of dietary carbohydrate from the intestine, we previously determined the amount of unabsorbed carbohydrate after breakfast by the breath hydrogen test in the four seasons. In pursuing our hypothesis further, we also recorded gastric myoelectrical activity before and after the breakfasts. In the current report, we describe the seasonality of gastric myoelectrical activity. Twenty-six Japanese female subjects were studied in winter, spring, summer and autumn. The cutaneous electrogastrogram was analysed by spectral analysis to compute the pre- and post-prandial dominant slow wave frequency (DF), and percentage of the 2 - 4 cpm gastric slow wave (Normal %). Two-factor ANOVA indicated that there was no significant seasonal variation in DF and Normal %. These results indicate that seasonal variations in digestion and absorption of dietary carbohydrate are caused by factors other than gastric and small intestinal motility.     

No evidence of inbreeding depression in sperm performance traits in wild song sparrows

Inbreeding is widely hypothesized to shape mating systems and population persistence, but such effects will depend on which traits show inbreeding depression. Population and evolutionary consequences could be substantial if inbreeding decreases sperm performance and hence decreases male fertilization success and female fertility. However, the magnitude of inbreeding depression in sperm performance traits has rarely been estimated in wild populations experiencing natural variation in inbreeding. Further, the hypothesis that inbreeding could increase within‐ejaculate variation in sperm traits and thereby further affect male fertilization success has not been explicitly tested. We used a wild pedigreed song sparrow (Melospiza melodia) population, where frequent extrapair copulations likely create strong postcopulatory competition for fertilization success, to quantify effects of male coefficient of inbreeding (f) on key sperm performance traits. We found no evidence of inbreeding depression in sperm motility, longevity, or velocity, and the within‐ejaculate variance in sperm velocity did not increase with male f. Contrary to inferences from highly inbred captive and experimental populations, our results imply that moderate inbreeding will not necessarily constrain sperm performance in wild populations. Consequently, the widely observed individual‐level and population‐level inbreeding depression in male and female fitness may not stem from reduced sperm performance in inbred males.     

Mate choice for nonadditive genetic benefits and the maintenance of genetic diversity in song sparrows

The lek paradox asserts that strong directional selection via female choice should deplete additive genetic variation in fitness and consequently any benefit to females expressing the preference. Recently, we have provided a novel resolution to the paradox by showing that nonadditive genetic effects such as overdominance can be inherited from parent to offspring, and populations with females that express a mating preference for outbred males maintain higher genetic variation than populations with females that mate randomly. Here, we test our dynamic model using empirical data previously published from a small island population of song sparrows (Melospiza melodia). The model assumes that fitness and male trait expression display overdominance effects. The results demonstrate that female choice for outbred males mediated by directional selection on song repertoire size provides a heritable benefit to offspring through reduced inbreeding depression. Within the population, we estimate the heritability of the inbreeding coefficient to be 0.18 ± 0.08 (SD). Furthermore, we show that mate choice for outbred males increases fitness‐related genetic variation in the population by 12% and thereby reduces inbreeding depression by 1% per generation in typical years and upwards of 15% in severe years. Thus, mate choice may help to stave off population extinction in this and other small populations.     

树麻雀代谢率和器官重量在季节驯化中表型的可塑性变化

动物能量代谢的生理生态特征与物种的分布和丰富度密切相关,基础代谢率(BMR)是内温动物能量预算的重要组成部分。北温带的小型鸟类,通过增加产热来适应低温环境。增加BMR的基础之一是中心器官(代谢机器)发生明显的变化。本研究中我们测定了树麻雀(Passermontanus)的BMR、体重和各器官的重量,分析了麻雀各器官的季节性变化及与BMR的关系。方差分析表明:麻雀的BMR存在明显的季节性变化,在冬季和秋季较高。麻雀内部器官的变化同样有明显的季节性,冬季和秋季麻雀的肝脏、心脏、肌胃、小肠、直肠和整体消化道的重量,都有明显的增加。相关分析表明:麻雀的BMR与肝脏、心脏和消化道等内部器官存在明显的相关性。我们的结果验证了“中心限制假说”,即麻雀体内存在着与BMR相关的“代谢机器”,中心器官是提高麻雀BMR的基础之一。