Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata)

In a wide range of bird species, females have been shown to express active preferences for males that sing more complex songs. Current sexual selection theory predicts that for this signal to remain an honest indicator of male quality, it must be associated with an underlying cost of development or maintenance. There has been considerable debate questioning the costs associated with song production and learning. Recently, the nutritional stress hypothesis proposed that song complexity could act as an indicator of early developmental history, since the song control nuclei in the brain are laid down early in life. Here we test the nutritional stress hypothesis, by investigating the effects of dietary stress on the quality of adult song produced. In addition, we tested the effects of elevated corticosterone during development on song production to test its possible involvement in mediating the effects of developmental stress. The results demonstrate that both dietary restriction and elevated corticosterone levels significantly reduced nestling growth rates. In addition, we found that experimentally stressed birds developed songs with significantly shorter song motif duration and reduced complexity. These results provide novel experimental evidence that complex song repertoires may have evolved as honest signals of male quality, by indicating early developmental rearing conditions.     

Song evolution,speciation, and vocal learning in passerine birds

Phenotypic divergence can promote reproductive isolation and speciation, suggesting a possible link between rates of phenotypic evolution and the tempo of speciation at multiple evolutionary scales. To date, most macroevolutionary studies of diversification have focused on morphological traits, whereas behavioral traits─including vocal signals─are rarely considered. Thus, although behavioral traits often mediate mate choice and gene flow, we have a limited understanding of how behavioral evolution contributes to diversification. Furthermore, the developmental mode by which behavioral traits are acquired may affect rates of behavioral evolution, although this hypothesis is seldom tested in a phylogenetic framework. Here, we examine evidence for rate shifts in vocal evolution and speciation across two major radiations of codistributed passerines: one oscine clade with learned songs (Thraupidae) and one suboscine clade with innate songs (Furnariidae). We find that evolutionary bursts in rates of speciation and song evolution are coincident in both thraupids and furnariids. Further, overall rates of vocal evolution are higher among taxa with learned rather than innate songs. Taken together, these findings suggest an association between macroevolutionary bursts in speciation and vocal evolution, and that the tempo of behavioral evolution can be influenced by variation in developmental modes among lineages.     

Song learning by prairie warblers: When,where, and from whom

Songbirds of many species acquire their songs by imitating the songs of conspecific singers. Conclusive evidence of such imitation comes from controlled laboratory studies, but such studies do not reveal when and where songbirds learn their songs under natural conditions. To determine the timing and location of song learning in a population of prairie warblers, we compared the songs of yearling prairie warblers of known hatching location to the songs of other birds in the yearlings' natal and first breeding areas. The comparisons yielded a likely model song (and model singer) for each of the song types used by the focal yearlings. We supplemented our findings from the song comparisons with inferences drawn from an analysis of local geographic variation in songs. This analysis revealed that shared song types showed no tendency to be geographically clustered within the study area. Taken together, our data suggest that prairie warblers learn their songs during the hatch year, at locations somewhat distant (mean distance 1,437 m) from their natal site, most likely as birds wander about during the post-fledging period.     

Song learning in domesticated canaries in a restricted acoustic environment

Many songbirds learn their songs early in life from a song model. In the absence of such a model, they develop an improvised song that often lacks the species-typical song structure. Open-ended learners, such as the domesticated canary, are able to modify their songs in adulthood, although the mechanisms that guide and time the song-learning process are still not fully understood. In a previous study, we showed that male domesticated canaries lacking an adult song model in their first year substantially change their song repertoire and composition when exposed to normally reared conspecifics in their second year. Here, we investigate song development in descendants of canaries that were raised and kept as a peer group without a song model. Such males represent tutors with abnormal song characteristics. Interestingly, the F₁ generation developed quite normal song structure, and when brought into an environment with normally raised canaries in their second year, they did not modify their songs substantially. These results suggest that contact with an adult song model early in life is crucial for song crystallization, but also that song development is at least partly guided by innate rules. They also question the existing classification of canaries as open-ended learners.     

Early developmental stress negatively affects neuronal recruitment to avian song system nucleus HVC

Adverse environmental conditions can impact the life history trajectory of animals. Adaptive responses enable individuals to cope with unfavorable conditions, but altered metabolism and resource allocation can bear long‐term costs. In songbirds, early developmental stress can cause lifelong changes in learned song, a culturally transmitted trait, and nestlings experiencing developmental stress develop smaller song control nucleus HVCs. We investigated whether nutrition‐related developmental stress impacts neurogenesis in HVC, which may explain how poor nutrition leads to smaller HVC volume. We provided different quality diets (LOW and HIGH) by varying the husks‐to‐seeds ratio to zebra finch families for the first 35 days after the young hatched (PHD). At PHD14–18 and again at nutritional independence (PHD35), juveniles were injected with different cell division markers. To monitor growth, we took body measures at PHD10, 17, and 35. At PHD35 the number of newly recruited neurons in HVC and the rate of proliferation in the adjacent ventricular zone (VZ) were counted. Males raised on the LOW diet for their first weeks of life had significantly fewer new neurons in HVC than males raised on the HIGH diet. At the time when these new HVC neurons were born and labeled in the VZ (PHD17) the birds exposed to the LOW diet had significantly lower body mass. At PHD35 body mass or neuronal proliferation no longer differed. Our study shows that even transitory developmental stress can have negative consequences on the cellular processes underlying the development of neural circuits. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 107–118, 2016     

Song learning accelerates allopatric speciation

The songs of many birds are unusual in that they serve a role in identifying conspecific mates, yet they are also culturally transmitted. Noting the apparently high rate of diversity in one avian taxon, the songbirds, in which song learning appears ubiquitous, it has often been speculated that cultural transmission may increase the rate of speciation. Here we examine the possibility that song learning affects the rate of allopatric speciation. We construct a population-genetic model of allopatric divergence that explores the evolution of genes that underlie learning preferences (predispositions to learn some songs over others). We compare this with a model in which mating signals are inherited only genetically. Models are constructed for the cases where songs and preferences are affected by the same or different loci, and we analyze them using analytical local stability analysis combined with simulations of drift and directional sexual selection. Under nearly all conditions examined, song divergence occurs more readily in the learning model than in the nonlearning model. This is a result of reduced frequency-dependent selection in the learning models. Cultural evolution causes males with unusual genotypes to tend to learn from the majority of males around them, and thus develop songs compatible with the majority of the females in the population. Unusual genotypes can therefore be masked by learning. Over a wide range of conditions, learning therefore reduces the waiting time for speciation to occur and can be predicted to accelerate the rate of speciation.     

白头鹎鸣唱特征的季节差异分析

许多动物的声通讯行为存在显著的季节变化,鸟类的鸣唱也是如此。雄鸟鸣唱具有宣告领域和吸引配偶的功能,在繁殖季节与非繁殖季节之间应存在一定差异,但差异如何？具体表现在哪些方面？这在很多鸟类中尚未可知。本研究以一种在秋季也有显著鸣唱行为的城市常见小型鸣禽——白头鹎（Pycnonotussinensis）为研究对象,比较其在春季（繁殖季）与秋季（非繁殖季）的鸣唱差异,并分析可能的原因。于2020至2021连续两年的春、秋季分别在武汉地区各采集了27只和30只雄性白头鹎的鸣唱录音,共测量分析春季鸣唱372个,秋季鸣唱435个。对测得的各鸣唱参数数据进行季节间比较,结果显示,白头鹎的鸣唱持续时间和鸣唱音节数存在显著季节差异,春季鸣唱的持续时间较秋季更长,鸣唱音节数更多。鸣唱的频率、能量分布等其他声学参数,以及鸣唱型出现率（反映鸣唱曲目大小）均未表现出显著季节差异。白头鹎鸣唱的时程特征相对其他鸣声特征更具季节可塑性。此外,还发现同一采样点的白头鹎春、秋两季使用相同的鸣唱型。本研究结果表明,春季白头鹎的单位时间鸣唱输出量更大,鸣唱行为更活跃,这与繁殖季节鸟类的领域性更强、为繁殖成功投入更多相一致。白头...     

河北塞罕坝褐柳莺鸣唱特征分析

2014年7月至8月,在天气良好的情况下,每天上午5:00至10:00时,利用TASCAM DR-680型录音机外接Sennheiser ME67话筒,录制了河北塞罕坝林场处于繁殖期的褐柳莺(Phylloscopus fuscatus)鸣声。录音的采样精度为16 bit,采样频率设置为44.1 k Hz。共获得41只个体清晰可供分析的录音,平均每只个体录到(47±16)句录音。利用Raven pro分析软件测量鸣唱参数,如每个句子和音节的最低频率、最高频率、起始频率及终止频率、持续时间和音节(音素)个数。进行统计分析后,发现河北地区褐柳莺鸣唱语句包含两种类型,句型较单一不变的S-song和句型多变的V-song。褐柳莺鸣唱句子的最高频率为(7.04±0.89)k Hz,最低频率为(1.75±0.30)k Hz,起始频率为(4.53±2.00)k Hz,终止频率(3.22±1.43)k Hz,句子的持续时间(1.24±0.32)s,由(6.50±1.91)个音节组成。基于语图上音节形态的差异,共发现49种不同的音节类型,每只个体鸣唱中使用2到30种音节类型。     

Song as an indicator of parasitism in the sedge warbler

We studied female choice and reproductive success in a marked population of sedge warblers Acrocephalus schoenobaenus, from 1995 to 1996. Three genera of parasitic blood protozoans, namely Haemoproteus sp. Trypanosoma sp. Plasmodium sp., were identified from blood samples taken from all breeding adults. Relatively high prevalence values of 19.5% in 1995 and 37.5% in 1996 were associated with increased levels of white blood cells relative to the number of red blood cells. Compared with nonparasitized males, parasitized males had significantly lower repertoire sizes in both years of the study; in one year, they also spent less time in song flights and weighed less. They also provisioned their broods at a lower rate. Parasitized females produced the same clutch size as nonparasitized females, although their broods were smaller at 7 days old. We suggest that haematozoan infections may reduce the expression of sexually selected song traits. Furthermore, such infections may influence the standard of parental care provided by males, although further research is needed to determine whether this is mediated through genetic resistance to parasitism or the effects of parasitism upon immediate body condition. Copyright 1999 The Association for the Study of Animal Behaviour.     

Beneficial developmental acclimation in reproductive performance under cold but not heat stress

Thermal plasticity can help organisms coping with climate change. In this study, we analyse how laboratory populations of the ectotherm species Drosophila subobscura, originally from two distinct latitudes and evolving for several generations in a stable thermal environment (18 °C), respond plastically to new thermal challenges. We measured adult performance (fecundity traits as a fitness proxy) of the experimental populations when exposed to five thermal regimes, three with the same temperature during development and adulthood (15-15 °C, 18-18 °C, 25-25 °C), and two where flies developed at 18 °C and were exposed, during adulthood, to either 15 °C or 25 °C. Here, we test whether (1) flies undergo stress at the two more extreme temperatures; (2) development at a given temperature enhances adult performance at such temperature (i.e. acclimation), and (3) populations with different biogeographical history show plasticity differences. Our findings show (1) an optimal performance at 18 °C only if flies were subjected to the same temperature as juveniles and adults; (2) the occurrence of developmental acclimation at lower temperatures; (3) detrimental effects of higher developmental temperature on adult performance; and (4) a minor impact of historical background on thermal response. Our study indicates that thermal plasticity during development may have a limited role in helping adults cope with warmer - though not colder - temperatures, with a potential negative impact on population persistence under climate change. It also emphasizes the importance of analysing the impact of temperature on all stages of the life cycle to better characterize the thermal limits.     

鸣禽发声学习行为的神经生物学机制

鸣禽发声学习的控制系统主要由一条直接神经通路和一条辅助神经通路组成,由前脑控制发声学习的最高中枢ＨＶＣ、旁嗅叶的Ｘ区和巨细胞核外侧部（ｌＭＡＮ）组成的辅助通路,对鸟类发声学习行为的发育和调制具有重要作用。发声控制系统中神经元类型、数量及再生与更替、神经组构及其重组、神经介质和受体的分布等差异,决定了鸣禽在发声学习行为表现的差异以及性双态性。本文对近年鸟类控制发声学习行煌神经生物学机制的进展作了较为     

Stimulus sampling as an exploration mechanism for fast reinforcement learning

Reinforcement learning in neural networks requires a mechanism for exploring new network states in response to a single, nonspecific reward signal. Existing models have introduced synaptic or neuronal noise to drive this exploration. However, those types of noise tend to almost average out—precluding or significantly hindering learning —when coding in neuronal populations or by mean firing rates is considered. Furthermore, careful tuning is required to find the elusive balance between the often conflicting demands of speed and reliability of learning. Here we show that there is in fact no need to rely on intrinsic noise. Instead, ongoing synaptic plasticity triggered by the naturally occurring online sampling of a stimulus out of an entire stimulus set produces enough fluctuations in the synaptic efficacies for successful learning. By combining stimulus sampling with reward attenuation, we demonstrate that a simple Hebbian-like learning rule yields the performance that is very close to that of primates on visuomotor association tasks. In contrast, learning rules based on intrinsic noise (node and weight perturbation) are markedly slower. Furthermore, the performance advantage of our approach persists for more complex tasks and network architectures. We suggest that stimulus sampling and reward attenuation are two key components of a framework by which any single-cell supervised learning rule can be converted into a reinforcement learning rule for networks without requiring any intrinsic noise source. This work was supported by the Swiss National Science Foundation grant K-32K0-118084.     

Three models of song learning: Evidence from behavior

Research on avian song learning has traditionally been based on an instructional model, as exemplified by the sensorimotor model of song development. Several large-scale, species-wide field studies of learned birdsongs have revealed that variation is narrowly restricted to certain aspects of song structure. Other aspects are sufficiently stereotyped and so widely shared by species' members that they qualify as species-specific universals. The limitations on natural song variation are difficult to reconcile with a fully open, instructive model of song learning. An alternative model based on memorization by selection postulates a system of innate neural templates that facilitate the recognition and rapid memorization of conspecific song patterns. Behavioral evidence compatible with this model includes learning preferences, rapid conspecific song learning, and widespread ocurrence of species-specific song universals that are recognized innately but fail to develop in songs of social isolates. A third model combines instruction, in the memorization phase, with selection during song production. An overproduced repertoire of plastic songs previously memorized by instruction is winnowed by selection imposed during social interactions at the time of adult song crystallization. Selection during production is well established as a factor in the song development of several species, in the form of action-based learning. The possible role of selective processes in song memorization merits further neurobiological investigation. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 501–516, 1997     

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.     

Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris)

Bird song is a sexually selected male trait where females select males on the basis of song quality. It has recently been suggested that the quality of the adult male song may be determined by nutritional stress during early development. Here, we test the 'nutritional-stress hypothesis' using the complex song of the European starling. Fledgling starlings were kept under experimental treatment (unpredictable short-term food deprivations) or control conditions (ad libitum food supply), for three months immediately after independence. We measured their physiological and immune responses during the treatment and recorded song production during the following spring. Birds in the experimental group showed increased mass during the treatment and also a significantly suppressed humoral response compared with birds in the control group. There was no difference between the groups in the cell-mediated response. Next spring, males in the experimental group spent less time singing, sang fewer song bouts, took longer to start singing and also sang significantly shorter song bouts. These data support the hypothesis that both the quality and quantity of song produced by individual birds reflect past developmental stress. The results also suggest the 'nutritional-stress hypothesis' is best considered as a more general 'developmental-stress hypothesis'.     

Animal learning as a source of developmental bias

As a form of adaptive plasticity that allows organisms to shift their phenotype toward the optimum, learning is inherently a source of developmental bias. Learning may be of particular significance to the evolutionary biology community because it allows animals to generate adaptively biased novel behavior tuned to the environment and, through social learning, to propagate behavioral traits to other individuals, also in an adaptively biased manner. We describe several types of developmental bias manifest in learning, including an adaptive bias, historical bias, origination bias, and transmission bias, stressing that these can influence evolutionary dynamics through generating nonrandom phenotypic variation and/or nonrandom environmental states. Theoretical models and empirical data have established that learning can impose direction on adaptive evolution, affect evolutionary rates (both speeding up and slowing down responses to selection under different conditions) and outcomes, influence the probability of populations reaching global optimum, and affect evolvability. Learning is characterized by highly specific, path‐dependent interactions with the (social and physical) environment, often resulting in new phenotypic outcomes. Consequently, learning regularly introduces novelty into phenotype space. These considerations imply that learning may commonly generate plasticity first evolution.