Randomization Analyses: Mimicry, Geographic Variation and Cultural Evolution of Song in Brood-Parasitic Straw-Tailed Whydahs, Vidua fischeri

Although bird song has been an important model for investigating questions of behavior development, cultural evolution and population differentiation, the quantitative methods of analysis have been problematic. Here we develop and apply quantitative randomization methods to test hypotheses about these processes in a natural population of birds. Songs of the African brood-parasitic straw-tailed whydahs ( Vidua fischeri ) and songs of their host species, the purple grenadier ( Granatina ianthinogaster ), were compared in audiospectrograms for similarity to test the following hypotheses: Whydahs mimic the songs of their host species, they have local song dialects, neighboring males match their song themes, local males match the songs of local hosts, remote populations have different songs according to their geographic distance, and songs undergo cultural evolution over time across generations. Randomization analyses were completed using (1) Mantel matrix statistics and (2) tree-based measures employing Sankoff optimization of Manhattan matrices and approximate randomizations. Our results provide evidence for song mimicry, local song dialects, matching song themes between neighboring males, song matching of local whydah mimics and grenadier song models, correspondence of song differences and geographic distance, and cultural continuity with change in song traditions within a local population. These randomization methods may be useful in other studies of animal communication, and they are sufficiently general for use both with distance matrices derived either from naturalistic impressions of song similarity as in our example or from acoustic measurements.     

Animal learning and memory: an integration of cognition and ecology

A wonderfully lucid framework for the ways to understand animal behaviour is that represented by the four ‘whys’ proposed by Tinbergen (1963). For much of the past three decades, however, these four avenues have been pursued more or less in parallel. Functional questions, for example, have been addressed by behavioural ecologists, mechanistic questions by psychologists and ethologists, ontogenetic questions by developmental biologists and neuroscientists and phylogenetic questions by evolutionary biologists. More recently, the value of integration between these differing views has become apparent. In this brief review, we concentrate especially on current attempts to integrate mechanistic and functional approaches.

Most of our understanding of learning and memory in animals comes from the psychological literature, which tends to use only rats or pigeons, and more occasionally primates, as subjects. The underlying psychological assumption is of general processes that are similar across species and contexts rather than a range of specific abilities. However, this does not seem to be entirely true as several learned behaviours have been described that are specific to particular species or contexts. The first conspicuous exception to the generalist assumption was the demonstration of long delay taste aversion learning in rats (Garcia et al., 1955), in which it was shown that a stimulus need not be temporally contiguous with a response for the animal to make an association between food and illness. Subsequently, a number of other examples, such as imprinting and song learning in birds (e.g., Bolhuis and Honey, 1998; Catchpole and Slater, 1995; Horn, 1998), have been thoroughly researched. Even in these cases, however, it has been typical for only a few species to be studied (domestic chicks provide the ‘model’ imprinting species and canaries and zebra finches the song learning ‘models’). As a result, a great deal is understood about the neural underpinnings and development of the behaviour, but substantially less is understood about interspecific variation and whether variation in behaviour is correlated with variation in neural processing (see review by Tramontin and Brenowitz, 2000 but see ten Cate and Vos, 1999).     

Recent research on the evolution of land birds on the Galápagos

A decade of research on the evolution of Galápagos land birds is reviewed, and outstanding questions to be answered are highlighted. Evolutionary studies have been restric 1 almost entirely to the four species of mockingbirds and the 13 species of Darwin's finches. Long-term field studies have been initiated on representatives of both groups. Co-operative breeding has been discovered in the mockingbirds (and hawks).
Lack's (1945, 1947) monographic treatment of Darwin's finches has been largely upheld and extended by morphological, ecological, behavioural and biochemical studies. While the phylogenetic origins of Darwin's finches still remain uncertain, the major groupings of the finches have been confirmed by the results of protein polymorphism analysis. Fossils of Darwin's finches have been discovered recently: their potential for illuminating evolutionary change has not yet been realized. Three other major developments are (1) quantitative confirmation of the role of interspecific competition in the adaptive radiation, (2) experimental confirmation of the role of morphological and song cues in species recognition, and experimental evidence of their evolution in the speciation process, and (3) direct study of natural selection on heritable quantitative traits in a population, and identification of its causes. Continuing studies of population variation are likely to reveal the contemporary importance of selection, migration and hybridization, and thereby help us to more fully understand the causes of the adaptive radiation of Darwin's finches.     

How social experience shapes song representation in the brain of starlings

Birdsong, like speech, is a learned behaviour whose critical function is to communicate with others and whose development critically depends on social influences. Song learning is a complex phenomenon that involves not only the development of species-specific vocalisations, but also the development of the ability to organise these vocalisations and to use them in an appropriate context. Although the fact that interactions with adult experienced models are essential for song production to develop properly has been well established, far less is known about song perception and processing. The fact that songbirds learn to vocalise and to use their vocalisations selectively through interactions with adults questions whether such interactions are also required for songbirds to perceive and process their vocalisations selectively and whether social interactions may shape song perception and processing as they shape song production. In order to address these questions, our team uses an original neuroethological approach to study the neural bases of song behaviour in a highly social songbird species: the European starlings. We provide here a synthesis of the results we have obtained using this approach over the last decade. Our results show that direct social experience with adult experienced models not only shapes song behaviour but also shapes these songbirds’ brains and their ability to perceive and to process acoustic signals whose communicative value, as well as their acoustic structure, have to be learned.     

Genetics of sexual isolation based on courtship song between two sympatric species: Drosophila ananassae and D. pallidosa

Sexual isolation has been considered one of the primary causes of speciation and its genetic study has the potential to reveal the genetics of speciation. In Drosophila, the importance of courtship songs in sexual isolation between closely related species has been well investigated, but studies analysing the genetic basis of the difference in the courtship songs associated with sexual isolation are less well documented. Drosophila ananassae and Drosophila pallidosa are useful for studies of sexual isolation, because of their sympatric distribution and absence of postmating isolation. Courtship songs are known to play a crucial role in sexual isolation between these two species, and the female discrimination behaviour against the courting male has been revealed to be controlled by a very narrow region on the second chromosome. In this study we investigated the genetic basis controlling the song differences associated with their sexual isolation, using intact and wingless males with chromosomes substituted between species. The results obtained from F₁ hybrid males between these species indicate the dominance of the song characters favoured by D. pallidosa females. In addition, the results obtained from backcross F₂ males indicate that chromosome 2 had a major effect on the control of the song characters associated with sexual isolation.     

Ultraviolet and green parts of the colour spectrum affect egg rejection in the song thrush (Turdus philomelos)

Much attention has been devoted to understanding the evolution of egg mimicry in avian brood parasites. The majority of studies have been based on human perception when scoring the mimicry of the parasitic egg. Surprisingly, there has been no detailed study on the recognition and sensitivity towards differently coloured parasitic eggs. We investigated effect of different colours of the experimental eggs measured by ultraviolet (UV)-visible reflectance spectrophotometry on rejection behaviour in the song thrush ( Turdus philomelos ). We carried out a set of experiments with four blue model eggs representing mimetic eggs, whereas six other colours represented nonmimetic eggs. Our results revealed that two colours originally designed as a mimetic were rejected at a high rate, whereas one group of the nonmimetic was accepted. A multiple regression model of absolute differences between song thrush and experimental eggs on rejection rate showed that the level of mimicry in the UV and green parts of the colour spectrum significantly influenced egg rejection in the song thrush. To our knowledge, this is the first detailed study showing that different colour perception by the birds can affect their responses towards the parasitic egg. These findings suggest that the combination of UV and visible ranges of the spectra plays a major role in the evolution of discrimination processes, as well as in the evolution of the mimicry of the parasitic egg.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 269–276.     

Patterns of song evolution and sexual selection in the oropendolas and caciques

Although oscine bird song is widely thought to have evolvedunder the influence of sexual selection, few studies have usedphylogenetic comparative methods to investigate how these vocalizationshave changed historically. In the present study, we use a molecularphylogeny based on mitochondrial sequence data to reconstructvocal evolution in the oropendolas and caciques, an oscine groupwith diverse taxon-specific song patterns and a wide range inlevels of sexual size dimorphism. Our reconstructions show thatlarge changes in song organization and structure have occurredon branches of the phylogeny with relatively high levels ofsize dimorphism. The particular vocal components that changed,however, often differed in different phylogenetic lineages.These patterns indicate that sexual selection has had importantinfluences on song evolution in these birds, but has targeteddifferent components of song in different taxa. Our resultsprovide insight into how sexual selection influences bird songand suggest directions for future research to uncover the behavioralmechanisms driving vocal evolution.     

Frequency sensitivity in the auditory periphery of male and female black-capped chickadees (Poecile atricapillus)

The black-capped chickadee is a songbird that has been used extensively as a model of animal communication in field and laboratory settings. Although many studies have focused on the complex call and song systems of the black-capped chickadee, relatively fewer studies have focused on chickadee audition. However, we do know from behavioral and molecular work that chickadees (and auditory processing areas in their brains) discriminate between artificially generated tones, between conspecific and heterospecific vocalizations, and among different types of conspecific vocalizations. In this paper we investigate peripheral auditory processing of frequency in the black-capped chickadee and the potential influence of sex on frequency sensitivity using a technique called auditory evoked potentials. We found that male and female black-capped chickadees did not differ in any measure of frequency sensitivity. Both sexes had the greatest sensitivity to frequencies between 2 and 4 kHz. This range of frequencies is well represented in black-capped chickadee song, partially supporting the idea that sender and receiver coevolve. Finally, we suggest that the call and song system of North American parids make them an ideal taxonomic group for comparative work exploring the relationship between call systems and the evolution of auditory processing.     

Phenotypic and genomic plasticity of alternative male reproductive tactics in sailfin mollies

A major goal of modern evolutionary biology is to understand the causes and consequences of phenotypic plasticity, the ability of a single genotype to produce multiple phenotypes in response to variable environments. While ecological and quantitative genetic studies have evaluated models of the evolution of adaptive plasticity, some long-standing questions about plasticity require more mechanistic approaches. Here, we address two of those questions: does plasticity facilitate adaptive evolution? And do physiological costs place limits on plasticity? We examine these questions by comparing genetically and plastically regulated behavioural variation in sailfin mollies (Poecilia latipinna), which exhibit striking variation in plasticity for male mating behaviour. In this species, some genotypes respond plastically to a change in the social environment by switching between primarily courting and primarily sneaking behaviour. In contrast, other genotypes have fixed mating strategies (either courting or sneaking) and do not display plasticity. We found that genetic and plastic variation in behaviour were accompanied by partially, but not completely overlapping changes in brain gene expression, in partial support of models that predict that plasticity can facilitate adaptive evolution. We also found that behavioural plasticity was accompanied by broader and more robust changes in brain gene expression, suggesting a substantial physiological cost to plasticity. We also observed that sneaking behaviour, but not courting, was associated with upregulation of genes involved in learning and memory, suggesting that sneaking is more cognitively demanding than courtship.     

The evolutionary importance of behavioural development: the ontogeny and phylogeny of bird song

It has been proposed that ontogeny may be an important constraint on the evolution of morphological traits. In this paper, ontogeny is discussed as a possible constraint on behavioural evolution. A literature review of the development of song in oscine birds (Passeriformes; Passeres) shows that song development follows von Baer's law; that is, that development proceeds from early, generally distributed stages to later, specialized stages. Song ontogeny is found to parallel phylogeny in a lineage of sparrows (Emberizidae; Emberizinae). Possible cases of paedomorphosis (slowing down or truncation of development) in bird song are discussed, specifically in the family Mimidae and in the reed warbler, Acrocephalus palustris (Muscicapidae; Sylviinae). Finally, the implications of developmental constraints for the study of the adaptive significance of behaviour are discussed.     

Rufous‐capped Warblers Basileuterus rufifrons show seasonal,temporal and annual variation in song use

In the majority of songbird species, males have repertoires of multiple song types used for mate attraction and territory defence. The wood‐warblers (family Parulidae) are a diverse family of songbirds in which males of many migratory species use different song types or patterns of song delivery (known as ‘singing modes’) depending on context. The vocal behaviour of most tropical resident warblers remains undescribed, although these species differ ecologically and behaviourally from migratory species, and may therefore differ in their vocal behaviour. We test whether male Rufous‐capped Warblers Basileuterus rufifrons use distinct singing modes by examining song structure and context‐dependent variation in their songs. We recorded multiple song bouts from 50 male Warblers in a Costa Rican population over 3 years to describe seasonal, diel and annual variation in song structure and vocal behaviour. We found that Rufous‐capped Warbler songs are complex, with many syllable types shared both within and between males’ repertoires. Males varied their song output depending on context: they sang long songs at a high rate at dawn and during the breeding season, and shortened songs in the presence of a vocalizing female mate. Unlike many migratory species, Rufous‐capped Warblers do not appear to have different singing modes; they did not change the song variants used or the pattern of song delivery according to time of day, season or female vocal activity. Our research provides the first detailed vocal analysis of any Basileuterus warbler species, and enhances our understanding of the evolution of repertoire specialization in tropical resident songbirds.     

The relationship between latitude,migration and the evolution of bird song complexity

For the past several decades it has been proposed that birds show latitudinal variation in song complexity. How universal this variation may be and what factors generate it, however, are still largely unknown. Furthermore, while migration is confounded with latitude, migratory behaviour alone may also be associated with variation in song complexity. In this paper we review the literature to assess current ideas on how latitude and migratory behaviour may drive large‐scale geographical patterns of song complexity. At least seven distinct hypotheses have been proposed in 29 studies of the topic. Four of these hypotheses posit that sexual selection pressures co‐vary with latitude and/or migration, resulting in concordant changes in song. Other hypotheses suggest that mechanisms other than sexual selection, such as large‐scale changes in environmental sound transmission properties, may be at play. Sixteen studies found support for increased song complexity with increased latitude and/or migration, whereas 13 did not. Relatively few studies exist on this topic, and methodological differences between them and variable definitions of ‘complexity’ make it difficult to determine whether results are comparable and concordant. At a minimum, it is possible to conclude there is no strong evidence that song complexity increases with latitude and/or migration in all birds. Future work should focus on examining multiple hypotheses at once to further advance our understanding of how latitude, migration and song complexity may or may not be related.     

Culture and courtship in vertebrates: a review of social learning and transmission of courtship systems and mating patterns

Female and male animals often choose mates based upon the complementarity of their courtship behaviours and preferences. The importance of this fact on the evolutionary dynamics of populations has long been appreciated. What has not been appreciated is the role that social learning might play in the transmission of systems of courtship behaviour across generations. This paper addresses the social transmission of courtship behavioural traditions in vertebrates. It discusses views of culture in the context of behavioural signals and preferences in courtship. It then reviews empirical evidence for culture-like processes affecting courtship behaviour, focusing on studies of song learning in passerine birds and work on social learning of mating preferences. The paper concludes with potential future directions for research on social traditions in systems of courtship behaviour, including determining mechanisms of transmission, genetic and non-social environmental effects, and selective factors influencing the stability of behavioural traditions over time. By integrating proximate and ultimate questions for the transmission of courtship systems, this work would increase our understanding of the ways individual development, cultural processes, and population evolution influence, and are in turn influenced by, one another.     

The promise of behavioural biology

The studies of behaviour that were strongly rooted in biology have had a long tradition of bringing together the ‘how’ and the ‘why’ questions. This integrative approach will serve the subject well in the postgenomic era as the long trend towards analysis at lower and lower levels starts to reverse. The new studies will make use of the resources uncovered by molecular biology and the neurosciences but will use the behaviour of the whole animal to measure outcomes and the context in which behaviour occurs to frame analytical questions. Two examples are given of how movement between levels of analysis is being used with increasing power and promise. The first is the study of filial imprinting in birds where many of the molecular and neural mechanisms involved have been uncovered and are now being integrated to explain the behaviour of the whole animal. The second is the triggering during sensitive periods in early life by environmental events of one of several alternative modes of development leading to different phenotypes. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Bird song,ecology and speciation

The study of bird song dialects was once considered the most promising approach for investigating the role of behaviour in reproductive divergence and speciation. However, after a series of studies yielding conflicting results, research in the field slowed significantly. Recent findings, on how ecological factors may lead to divergence in both song and morphology, necessitate a re-examination. We focus primarily on species with learned song, examine conflicting results in the literature and propose some potential new directions for future studies. We believe an integrative approach, including an examination of the role of ecology in divergent selection, is essential for gaining insight into the role of song in the evolution of assortative mating. Habitat-dependent selection on both song and fitness-related characteristics can lead to parallel divergence in these traits. Song may, therefore, provide females with acoustic cues to find males that are most fit for a particular habitat. In analysing the role of song learning in reproductive divergence, we focus on post-dispersal plasticity in a conceptual framework. We argue that song learning may initially constrain reproductive divergence, while in the later stages of population divergence it may promote speciation.     

Singing in the moonlight: dawn song performance of a diurnal bird varies with lunar phase

It is well established that the lunar cycle can affect the behaviour of nocturnal animals, but its potential to have a similar influence on diurnal species has received less research attention. Here, we demonstrate that the dawn song of a cooperative songbird, the white-browed sparrow weaver (Plocepasser mahali), varies with moon phase. When the moon was above the horizon at dawn, males began singing on average 10 min earlier, if there was a full moon compared with a new moon, resulting in a 67% mean increase in performance period and greater total song output. The lack of a difference between full and new moon dawns when the moon was below the horizon suggests that the observed effects were driven by light intensity, rather than driven by other factors associated with moon phase. Effects of the lunar cycle on twilight signalling behaviour have implications for both pure and applied animal communication research.     

Steroid interactions with structure and function of avian song control regions

Following the pioneering work of Nottebohm, the brain regions involved in song production in songbirds have become a focus of extensive research in several laboratories. As both singing behavior and the neuroanatomy of song control regions are strongly affected by sex steroids in many songbird species, this system has become regarded as an ideal model system in which one can potentially determine how steroids affect neuronal anatomy, how altered anatomy leads to altered physiology, and how the altered physiology causes changes in singing. In the initial part of this review, I shall focus on canaries and zebra finches as most of our knowledge of the song system has been obtained from these two species. I shall describe singing behavior, the constituents of the song system, what is known of how these nuclei contribute to song, and how each is affected by steroid fluctuations. I shall then speculate on new ways of posing questions on hormone—anatomy interaction in this system (which I will illustrate with preliminary data from my own lab). This review will be brief as several reviews of aspects of the song system have recently been published (Arnold, 1982; Nottebohm, 1984; Arnold and Gorski, 1984; DeVoogd, 1984; Konishi, 1985).     

Evolutionary genetics of partial migration – the threshold model of migration revis(it)ed

Partial migration is a common and widespread phenomenon in animal populations. Even though the ecological causes for the evolution and maintenance of partial migration have been widely discussed, the consequences of the genetics underlying differences in migration patterns have been little acknowledged. Here, I revise current ideas on the genetics of partial migration and identify open questions, focussing on migration in birds. The threshold model of migration describing the inheritance and phenotypic expression of migratory behaviour is strongly supported by experimental results. As a consequence of migration being a threshold trait, high levels of genetic variation can be preserved, even under strong directional selection. This is partly due to strong environmental canalization. This cryptic genetic variation may explain rapid de novo evolution of migratory behaviour in resident populations and the high prevalence of partial migration in animal populations. To date the threshold model of migration has been tested only under laboratory conditions. For obtaining a more realistic representation of migratory behaviour in the wild, the simple threshold model needs to be extended by considering that the threshold of migration or the liability may be modified by environmental effects. This environmental threshold model is valid for both facultative and obligate migration movements, and identifies genetic accommodation as an important process underlying evolutionary change in migration status. Future research should aim at identifying the major environmental variables modifying migration propensity and at determining reaction norms of the threshold and liability across variation in these variables.     

Song Feature Specific Analysis of Isolate Song Reveals Interspecific Variation in Learned Components

Studies of avian vocal development without exposure to conspecific song have been conducted in many passerine species, and the resultant isolate song is often interpreted to represent an expression of the genetic code for conspecific song. There is wide recognition that vocal learning exists in oscine songbirds, but vocal learning has only been thoroughly investigated in a few model species, resulting in a narrow view of birdsong learning. By extracting acoustic signals from published spectrograms, we have reexamined the findings of isolate studies with a universally applicable semi‐automated quantitative analysis regimen. When song features were analyzed in light of three different production aspects (respiratory, syringeal, and central programming of sequence), all three show marked interspecific variability in how close isolate song features are to normal. This implies that song learning mechanisms are more variable than is commonly recognized. Our results suggest that the interspecific variation shows no readily observable pattern reflecting phylogeny, which has implications for understanding the mechanisms behind the evolution of avian vocal communication. We emphasize that song learning in passerines provides an excellent opportunity to investigate the evolution of a complex, plastic trait from a phylogenetic perspective.