Sons learn songs from their social fathers in a cooperatively breeding bird

Song learning is hypothesized to allow social adaptation to a local song neighbourhood. Maintaining social associations is particularly important in cooperative breeders, yet vocal learning in such species has only been assessed in systems where social association was correlated with relatedness. Thus, benefits of vocal learning as a means of maintaining social associations could not be disentangled from benefits of kin recognition. We assessed genetic and cultural contributions to song in a species where social association was not strongly correlated with kinship: the cooperatively breeding, reproductively promiscuous splendid fairy-wren (Malurus splendens). We found that song characters of socially associated father-son pairs were more strongly correlated (and thus songs were more similar) than songs of father-son pairs with a genetic, but no social, association (i.e. cuckolding fathers). Song transmission was, therefore, vertical and cultural, with minimal signatures of kinship. Additionally, song characters were not correlated with several phenotypic indicators of male quality, supporting the idea that there may be a tradeoff between accurate copying of tutors and quality signalling via maximizing song performance, particularly when social and genetic relationships are decoupled. Our results lend support to the hypothesis that song learning facilitates the maintenance of social associations by permitting unrelated individuals to acquire similar signal phenotypes.     

Bottlenose dolphins exchange signature whistles when meeting at sea

The bottlenose dolphin, Tursiops truncatus, is one of very few animals that, through vocal learning, can invent novel acoustic signals and copy whistles of conspecifics. Furthermore, receivers can extract identity information from the invented part of whistles. In captivity, dolphins use such signature whistles while separated from the rest of their group. However, little is known about how they use them at sea. If signature whistles are the main vehicle to transmit identity information, then dolphins should exchange these whistles in contexts where groups or individuals join. We used passive acoustic localization during focal boat follows to observe signature whistle use in the wild. We found that stereotypic whistle exchanges occurred primarily when groups of dolphins met and joined at sea. A sequence analysis verified that most of the whistles used during joins were signature whistles. Whistle matching or copying was not observed in any of the joins. The data show that signature whistle exchanges are a significant part of a greeting sequence that allows dolphins to identify conspecifics when encountering them in the wild.     

The different roles of social learning in vocal communication

While vocal learning has been studied extensively in birds and mammals, little effort has been made to define what exactly constitutes vocal learning and to classify the forms that it may take. We present such a theoretical framework for the study of social learning in vocal communication. We define different forms of social learning that affect communication and discuss the required methodology to show each one. We distinguish between contextual and production learning in animal communication. Contextual learning affects the behavioural context or serial position of a signal. It can affect both usage and comprehension. Production learning refers to instances where the signals themselves are modified in form as a result of experience with those of other individuals. Vocal learning is defined as production learning in the vocal domain. It can affect one or more of three systems: the respiratory, phonatory and filter systems. Each involves a different level of control over the sound production apparatus. We hypothesize that contextual learning and respiratory production learning preceded the evolution of phonatory and filter production learning. Each form of learning potentially increases the complexity of a communication system. We also found that unexpected genetic or environmental factors can have considerable effects on vocal behaviour in birds and mammals and are often more likely to cause changes or differences in vocalizations than investigators may assume. Finally, we discuss how production learning is used in innovation and invention, and present important future research questions. Copyright 2000 The Association for the Study of Animal Behaviour.     

Juvenile Galápagos Pelicans Increase Their Foraging Success by Copying Adult Behaviour

Social learning is the building block of culture and traditions in humans and nonhuman animals, and its study has a long history. Most investigations have addressed either the causation or the function of social learning. Though much is known about the underlying mechanisms of social learning, demonstrations of its adaptive value in a natural setting are lacking. Here we show that juvenile brown pelicans (Pelecanus occidentalis) can increase their foraging efficiency by copying adult diving behaviour, suggesting that social learning helps juveniles to find profitable food patches. Our findings demonstrate the potential fitness consequences of behavioural copying and thus highlight the possible adaptive importance of social learning.     

Do female fruit flies (Drosophila serrata) copy the mate choice of others?

Female mate-choice copying is a social learning phenomenon whereby a female's observation of a successful sexual interaction between a male and another female increases her likelihood of subsequently preferring that male. Although mate-choice copying has been documented in several vertebrate species, to our knowledge it has not yet been investigated in insects. Here, we investigated whether female mate-choice copying occurs in the fruit fly Drosophila serrata, a model system for the study of mate preferences and the sexual selection they generate. We used two complementary experiments in which focal females were given a choice between two males that differed in either their apparent (as determined visually by the focal female) or actual recent mating success. Mate-choice copying was evaluated by testing whether focal females mated more frequently with the ‘preferred’ male as opposed to the other male. In both experiments, however, we found no evidence for mate-choice copying. We discuss possible reasons for the apparent absence of mate-choice copying in this species.     

Male and female rufous‐and‐white wrens do not match song types with same‐sex rivals during simulated territorial intrusions

In birds with song repertoires, song‐type matching occurs when an individual responds to another individual's song by producing the same song type. Song‐type matching has been described in multiple bird species and a growing body of evidence suggests that song‐type matching may serve as a conventional signal of aggression, particularly in male birds in the temperate zone. Few studies have investigated song‐type matching in tropical birds or female birds, in spite of the fact that avian biodiversity is highest in the tropics, that female song is widespread in the tropics, and that female song is the ancestral state among songbirds. In this study of rufous‐and‐white wrens Thryophilus rufalbus, a resident neotropical songbird where both sexes sing, we presented territorial males and females with playback that simulated a territorial rival producing shared and unshared songs. In response, both males and females sang matched song types at levels statistically equal to levels expected by chance. Furthermore, males and females exhibited similar levels of aggression and similar vocal behaviours in response to playback of both shared and unshared songs. These results indicate that rufous‐and‐white wrens do not use song‐type matching in territorial conflicts as a conventional signal of aggression. We discuss alternative hypotheses for the function of song‐type sharing in tropical birds. In particular, we point out that shared songs may play an important role in intra‐pair communication, especially for birds where males and females combine their songs in vocal duets, and this may supersede the function of song‐type matching in some tropical birds.     

The function and mechanism of vocal accommodation in humans and other primates

The study of non‐human animals, in particular primates, can provide essential insights into language evolution. A critical element of language is vocal production learning, i.e. learning how to produce calls. In contrast to other lineages such as songbirds, vocal production learning of completely new signals is strikingly rare in non‐human primates. An increasing body of research, however, suggests that various species of non‐human primates engage in vocal accommodation and adjust the structure of their calls in response to environmental noise or conspecific vocalizations. To date it is unclear what role vocal accommodation may have played in language evolution, in particular because it summarizes a variety of heterogeneous phenomena which are potentially achieved by different mechanisms. In contrast to non‐human primates, accommodation research in humans has a long tradition in psychology and linguistics. Based on theoretical models from these research traditions, we provide a new framework which allows comparing instances of accommodation across species, and studying them according to their underlying mechanism and ultimate biological function. We found that at the mechanistic level, many cases of accommodation can be explained with an automatic perception–production link, but some instances arguably require higher levels of vocal control. Functionally, both human and non‐human primates use social accommodation to signal social closeness or social distance to a partner or social group. Together, this indicates that not only some vocal control, but also the communicative function of vocal accommodation to signal social closeness and distance must have evolved prior to the emergence of language, rather than being the result of it. Vocal accommodation as found in other primates has thus endowed our ancestors with pre‐adaptations that may have paved the way for language evolution.     

Automated identification of social interaction criteria in Drosophila melanogaster

The study of social behaviour within groups has relied on fixed definitions of an ‘interaction’. Criteria used in these definitions often involve a subjectively defined cut-off value for proximity, orientation and time (e.g. courtship, aggression and social interaction networks) and the same numerical values for these criteria are applied to all of the treatment groups within an experiment. One universal definition of an interaction could misidentify interactions within groups that differ in life histories, study treatments and/or genetic mutations. Here, we present an automated method for determining the values of interaction criteria using a pre-defined rule set rather than pre-defined values. We use this approach and show changing social behaviours in different manipulations of Drosophila melanogaster. We also show that chemosensory cues are an important modality of social spacing and interaction. This method will allow a more robust analysis of the properties of interacting groups, while helping us understand how specific groups regulate their social interaction space.     

Bat echolocation calls facilitate social communication

Bat echolocation is primarily used for orientation and foraging but also holds great potential for social communication. The communicative function of echolocation calls is still largely unstudied, especially in the wild. Eavesdropping on vocal signatures encoding social information in echolocation calls has not, to our knowledge, been studied in free-living bats so far. We analysed echolocation calls of the polygynous bat Saccopteryx bilineata and found pronounced vocal signatures encoding sex and individual identity. We showed experimentally that free-living males discriminate approaching male and female conspecifics solely based on their echolocation calls. Males always produced aggressive vocalizations when hearing male echolocation calls and courtship vocalizations when hearing female echolocation calls; hence, they responded with complex social vocalizations in the appropriate social context. Our study demonstrates that social information encoded in bat echolocation calls plays a crucial and hitherto underestimated role for eavesdropping conspecifics and thus facilitates social communication in a highly mobile nocturnal mammal.     

Female aggression predicts mode of paternity acquisition in a social lizard

Individual differences in behaviour are ubiquitous in nature. Despite the likely role of selection in maintaining these differences, there are few demonstrations of their fitness consequences in wild populations and, consequently, the mechanisms that link behavioural variation to variation in fitness are poorly understood. Specifically, the consequences of consistent individual differences in behaviour for the evolution of social and mating strategies have rarely been considered. We examined the functional links between variation in female aggression and her social and mating strategies in a wild population of the social lizard Egernia whitii. We show that female Egernia exhibit temporally consistent aggressive phenotypes, which are unrelated to body size, territory size or social density. A female''s aggressive phenotype, however, has strong links to her mode of paternity acquisition (within- versus extra-pair paternity), with more aggressive females having more offspring sired by extra-pair males than less aggressive females. We discuss the potential mechanisms by which female aggression could underpin mating strategies, such as the pursuit/acceptance of extra-pair copulations. We propose that a deeper understanding of the evolution and maintenance of social and mating systems may result from an explicit focus on individual-level female behavioural phenotypes and their relationship with key reproductive strategies.     

Communication in bottlenose dolphins: 50 years of signature whistle research

Bottlenose dolphins (Tursiops truncatus) produce individually distinctive signature whistles that broadcast the identity of the caller. Unlike voice cues that affect all calls of an animal, signature whistles are distinct whistle types carrying identity information in their frequency modulation pattern. Signature whistle development is influenced by vocal production learning. Animals use a whistle from their environment as a model, but modify it, and thus invent a novel signal. Dolphins also copy signature whistles of others, effectively addressing the whistle owner. This copying occurs at low rates and the resulting copies are recognizable as such by parameter variations in the copy. Captive dolphins can learn to associate novel whistles with objects and use these whistles to report on the presence or absence of the object. If applied to signature whistles, this ability would make the signature whistle a rare example of a learned referential signal in animals. Here, we review the history of signature whistle research, covering definitions, acoustic features, information content, contextual use, developmental aspects, and species comparisons with mammals and birds. We show how these signals stand out amongst recognition calls in animals and how they contribute to our understanding of complexity in animal communication.     

Comparisons of different methods to train a young zebra finch (Taeniopygia guttata) to learn a song

Like humans, oscine songbirds exhibit vocal learning. They learn their song by imitating conspecifics, mainly adults. Among them, the zebra finch (Taeniopygia guttata) has been widely used as a model species to study the behavioral, cellular and molecular substrates of vocal learning. Various methods using taped song playback have been used in the laboratory to train young male finches to learn a song. Since different protocols have been applied by different research groups, the efficiency of the studies cannot be directly compared. The purpose of our study was to address this problem. Young finches were raised by their mother alone from day post hatching (dph) 10 and singly isolated from dph 35. One week later, exposure to a song model began, either using a live tutor or taped playback (passive or self-elicited). At dph 100, the birds were transferred to a common aviary. We observed that one-to-one live tutoring is the best method to get a fairly complete imitation. Using self-elicited playback we observed high inter-individual variability; while some finches learned well (including good copying of the song model), others exhibited poor copying. Passive playback resulted in poor imitation of the model. We also observed that finches exhibited vocal changes after dph 100 and that the range of these changes was negatively related to their imitation of the song model. Taken together, these results suggest that social aspects are predominant in the success outcome of song learning in the zebra finch.     

Open-ended song learning in a hummingbird

Vocal learning in birds is typically restricted to a sensitive period early in life, with the few exceptions reported in songbirds and parrots. Here, we present evidence of open-ended vocal learning in a hummingbird, the third avian group with vocal learning. We studied vocalizations at four leks of the long-billed hermit Phaethornis longirostris during a four-year period. Individuals produce a single song repertoire, although several song-types can coexist at a single lek. We found that nine of 49 birds recorded on multiple days (18%) changed their song-type between consecutive recordings. Three of these birds replaced song-types twice. Moreover, the earliest estimated age when song replacement occurred ranged from 186 to 547 days (mean = 307 days) and all nine birds who replaced song-types produced a crystallized song before replacement. The findings indicate that song-type replacement is distinct from an initial early learning sensitive period. As half of lekking males do not survive past the first year of life in this species, song learning may well extend throughout the lifespan. This behaviour would be convergent to vocal learning programmes found in parrots and songbirds.     

Social learning about egg-laying substrates in fruitflies

Social learning, defined as learning from other individuals, has had dramatic effects on some species, including humans, in whom it has generated a rich culture. As a first step in examining the evolution of and mechanisms underlying social learning in insects, we tested for social learning in fruitflies (Drosophila melanogaster). Focal females (observers) that experienced novel food together with mated females (models), who had laid eggs on that food, subsequently exhibited a stronger preference for laying eggs on that food over another novel food compared with focal females that experienced the food alone. We observed no social learning, however, when observers experienced food with potentially more ambiguous social information provided by the presence of either virgin models or aggregation pheromone. This first documentation of social learning about egg-laying substrates in fruitflies builds on recent data indicating intricate use of social information by fruitflies and opens up exciting avenues for research on the evolution and neurogenetics of social learning using biology''s major model system.     

Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning

The extent to which nonhuman primate vocalizations are amenable to modification through experience is relevant for understanding the substrate from which human speech evolved. We examined the vocal behaviour of Guinea baboons, Papio papio, ranging in the Niokolo Koba National Park in Senegal. Guinea baboons live in a multi-level society, with units nested within parties nested within gangs. We investigated whether the acoustic structure of grunts of 27 male baboons of two gangs varied with party/gang membership and genetic relatedness. Males in this species are philopatric, resulting in increased male relatedness within gangs and parties. Grunts of males that were members of the same social levels were more similar than those of males in different social levels (N = 351 dyads for comparison within and between gangs, and N = 169 dyads within and between parties), but the effect sizes were small. Yet, acoustic similarity did not correlate with genetic relatedness, suggesting that higher amounts of social interactions rather than genetic relatedness promote the observed vocal convergence. We consider this convergence a result of sensory–motor integration and suggest this to be an implicit form of vocal learning shared with humans, in contrast to the goal-directed and intentional explicit form of vocal learning unique to human speech acquisition.     

A New Approach that Eliminates Handling for Studying Aggression and the "Loser" Effect in Drosophila melanogaster

Aggressive behavior in Drosophila melanogaster is composed of the sequential expression of stereotypical behavioral patterns (for analysis see ¹). This complex behavior is influenced by genetic, hormonal and environmental factors. As in many organisms, previous fighting experience influences the fighting strategy of flies and the outcome of later contests: losing a fight increases the probability of losing later contests, revealing "loser" effects that likely involve learning and memory ^2-4. The learning and memory that accompanies expression of complex social behaviors like aggression, is sensitive to pre-test handling of animals ^5,6. Many experimental procedures are used in different laboratories to study aggression ^7-9, however, no routinely used protocol that excludes handling of flies is currently available. Here, we report a new behavioral apparatus that eliminates handling of flies, using instead their innate negative geotactic responses to move animals into or out of fighting chambers. In this protocol, small circular fight arenas containing a food cup are divided into two equal halves by a removable plastic slider prior to introduction of flies. Flies enter chambers from their home isolation vials via sliding chamber doors and geotaxis. Upon removal of plastic sliders, flies are free to interact. After specified time periods, flies are separated again by sliders for subsequent experimentation. All of this is done easily without handling of individual flies. This apparatus offers a novel approach to study aggression and the associated learning and memory, including the formation of "loser" effects in fly fights. In addition, this new general-purpose behavioral apparatus can be employed to study other social behaviors of flies and should, in general, be of interest for investigating experience-related changes in fundamental behavioral processes.     

Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos

Embryos were traditionally considered to possess limited learning abilities because of the immaturity of their developing brains. By contrast, neonates from diverse species show behaviours dependent on prior embryonic experience. Stimulus discrimination is a key component of learning and has been shown by a handful of studies in non-human embryos. Superb fairy-wren embryos (Malurus cyaneus) learn a vocal password that has been taught to them by the attending female during incubation. The fairy-wren embryos use the learned element as their begging call after hatching to solicit more parental feeding. In this study, we test whether superb fairy-wren embryos have the capacity to discriminate between acoustical stimuli and whether they show non-associative learning. We measured embryonic heart rate response using a habituation/dishabituation paradigm with eggs sourced from nests in the wild. Fairy-wren embryos lowered their heart rate in response to the broadcasts of conspecific versus heterospecific calls, and in response to the calls of novel conspecific individuals. Thus, fairy-wrens join humans as vocal-learning species with known prenatal learning and individual discrimination.     

Acidic Di-leucine Motif Essential for AP-3–dependent Sorting and Restriction of the Functional Specificity of the Vam3p Vacuolar t-SNARE

The transport of newly synthesized proteins through the vacuolar protein sorting pathway in the budding yeast Saccharomyces cerevisiae requires two distinct target SNAP receptor (t-SNARE) proteins, Pep12p and Vam3p. Pep12p is localized to the pre-vacuolar endosome and its activity is required for transport of proteins from the Golgi to the vacuole through a well defined route, the carboxypeptidase Y (CPY) pathway. Vam3p is localized to the vacuole where it mediates delivery of cargoes from both the CPY and the recently described alkaline phosphatase (ALP) pathways. Surprisingly, despite their organelle-specific functions in sorting of vacuolar proteins, overexpression of VAM3 can suppress the protein sorting defects of pep12Δ cells. Based on this observation, we developed a genetic screen to identify domains in Vam3p (e.g., localization and/or specific protein–protein interaction domains) that allow it to efficiently substitute for Pep12p. Using this screen, we identified mutations in a 7–amino acid sequence in Vam3p that lead to missorting of Vam3p from the ALP pathway into the CPY pathway where it can substitute for Pep12p at the pre-vacuolar endosome. This region contains an acidic di-leucine sequence that is closely related to sorting signals required for AP-3 adaptor–dependent transport in both yeast and mammalian systems. Furthermore, disruption of AP-3 function also results in the ability of wild-type Vam3p to compensate for pep12 mutants, suggesting that AP-3 mediates the sorting of Vam3p via the di-leucine signal. Together, these data provide the first identification of an adaptor protein–specific sorting signal in a t-SNARE protein, and suggest that AP-3–dependent sorting of Vam3p acts to restrict its interaction with compartment-specific accessory proteins, thereby regulating its function. Regulated transport of cargoes such as Vam3p through the AP-3–dependent pathway may play an important role in maintaining the unique composition, function, and morphology of the vacuole.     

Brevity is prevalent in bat short-range communication

Animal communication follows many coding schemes. Less is known about the coding strategy for signal length and rates of use in animal vocal communication. A generalized brevity (negative relation between signal length and frequency of use) is innovatively explored but remains controversial in animal vocal communication. We tested brevity for short-range social and distress sounds from four echolocating bats: adult black-bearded tomb bat Taphozous melanopogon, Mexican free-tailed bat Tadarida brasiliensis, adult greater horseshoe bat Rhinolophus ferrumequinum, and adult least horseshoe bat Rhinolophus pusillus. There was a negative association between duration and number of social but not distress calls emitted. The most frequently emitted social calls were brief, while most distress calls were long. Brevity or lengthiness was consistently selected in vocal communications for each species. Echolocating bats seem to have convergent coding strategy for communication calls. The results provide the evidence of efficient coding in bat social vocalizations, and lay the basis of future researches on the convergence for neural control on bats’ communication calls.