Variation among vocalizations of Taraba major (Aves: Thamnophilidae) subspecies

Geographical variation of bird vocalizations may be related to factors influencing sound production and sound propagation. If birds, e.g. the Great Antshrike (Taraba major), produce vocalizations that develop normally in the absence of learning, these variations may reflect evolutionary divergence within species. In this case, vocal variation could be influenced by habitat structure, since abiotic features and vegetal cover affect sound propagation through environment. Selective pressures may be acting on populations in different ways, which could culminate in a process of speciation. Thus, we searched for structural variation of Great Antshrike vocalizations between subspecies and sought for relationships between these vocal variation and environmental structure. We found variations in frequency and time features of vocalizations among subspecies, which are correlated to latitude, elevation and climate. We also observed an increase in vocal differences along with an increase in distances between individuals, which could reflect isolation of subspecies and the vocal adaptation to different environments.     

Geographical variation in the vocalizations of the suboscine Thorn‐tailed Rayadito Aphrastura spinicauda

Structural variation in acoustic signals may be related either to the factors affecting sound production such as bird morphology, or to vocal adaptations to improve sound transmission in different environments. Thus, variation in acoustic signals can influence intraspecific communication processes. This will ultimately influence divergence in allopatric populations. The study of geographical variation in vocalizations of suboscines provides an opportunity to compare acoustic signals from different populations, without additional biases caused by song learning and cultural evolution typical of oscines. The aim of this study was to compare vocalizations of distinct populations of a suboscine species, the Thorn‐tailed Rayadito. Four types of vocalizations were recorded in five populations, including all three currently accepted subspecies. Comparisons of each type of vocalization among the five populations showed that some variation existed in the repetitive trill, whereas no differences were found among alarm calls and loud trills. Variation in repetitive trills among populations and forest types suggests that sound transmission is involved in vocal differences in suboscines. Acoustic differences are also consistent with distinguishing subspecies bullocki from spinicauda and fulva, but not the two latter subspecies from each other. Our results suggest that the geographical differentiation in vocalizations observed among Thorn‐tailed Rayadito populations is likely to be a consequence of different ecological pressures. Therefore, incipient genetic isolation of these populations is suggested, based on the innate origin of suboscine vocalizations.     

Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds

Given that evolutionary divergence in mating signals leads to reproductive isolation in numerous animal taxa, understanding what drives signal divergence is fundamental to our understanding of speciation. Mating signals are thought to diverge via several processes, including (1) as a by-product of morphological adaptation, (2) through direct adaptation to the signaling environment, or (3) to facilitate species recognition. According to the first two hypotheses, birdsongs diversify in different foraging niches and habitats as a product of selection for optimal morphology and efficient sound transmission, respectively. According to the third hypothesis, they diversify as a result of selection against maladaptive hybridization. In this study I test all three hypotheses by examining the influence of morphology, acoustic environment, and the presence of closely related congeners on song structure in 163 species of antbird (Thamnophilidae). Unlike oscine passerines, these Neotropical suboscines make ideal subjects because they develop their songs without learning. In other words, patterns of vocal divergence are not complicated by cultural evolution. In support of the morphological adaptation hypothesis, body mass correlates with the acoustic frequency of songs, and bill size with temporal patterning. These relationships were robust, even when controlling for phylogenetic inertia using independent contrasts, suggesting that there has been correlated evolution between morphological and acoustic traits. The results also support the acoustic adaptation hypothesis: birds which habitually sing in the understory and canopy produce higher-pitched songs than those that sing in the midstory, suggesting that song structure is related to the sound transmission properties of different habitat strata. Finally, the songs of sympatric pairs of closely related species are more divergent than those of allopatric pairs, as predicted by the species recognition hypothesis. To my knowledge, these data provide the first direct evidence that species recognition and ecological adaptation operate in tandem, and that the interplay between these factors drives the evolution of mating signals in suboscine birds.     

Genetic population structure and call variation in a passerine bird, the satin bowerbird, Ptilonorhynchus violaceus

Geographic variation in vocalizations is widespread in passerine birds, but its origins and maintenance remain unclear. One hypothesis to explain this variation is that it is associated with geographic isolation among populations and therefore should follow a vicariant pattern similar to that typically found in neutral genetic markers. Alternatively, if environmental selection strongly influences vocalizations, then genetic divergence and vocal divergence may be disassociated. This study compared genetic divergence derived from 11 microsatellite markers with a metric of phenotypic divergence derived from male bower advertisement calls. Data were obtained from 16 populations throughout the entire distribution of the satin bowerbird, an Australian wet-forest-restricted passerine. There was no relationship between call divergence and genetic divergence, similar to most other studies on birds with learned vocalizations. Genetic divergence followed a vicariant model of evolution, with the differentiation of isolated populations and isolation-by-distance among continuous populations. Previous work on Ptilonorhynchus violaceus has shown that advertisement call structure is strongly influenced by the acoustic environment of different habitats. Divergence in vocalizations among genetically related populations in different habitats indicates that satin bowerbirds match their vocalizations to the environment in which they live, despite the homogenizing influence of gene flow. In combination with convergence of vocalizations among genetically divergent populations occurring in the same habitat, this shows the overriding importance that habitat-related selection can have on the establishment and maintenance of variation in vocalizations.     

Acoustic Divergence with Gene Flow in a Lekking Hummingbird with Complex Songs

Hummingbirds have developed a remarkable diversity of learned vocalizations, from single-note songs to phonologically and syntactically complex songs. In this study we evaluated if geographic song variation of wedge-tailed sabrewings (Campylopterus curvipennis) is correlated with genetic divergence, and examined processes that explain best the origin of intraspecific song variation. We contrasted estimates of genetic differentiation, genetic structure, and gene flow across leks from microsatellite loci of wedge-tailed sabrewings with measures for acoustic signals involved in mating derived from recordings of males singing at leks throughout eastern Mexico. We found a strong acoustic structure across leks and geography, where lek members had an exclusive assemblage of syllable types, differed in spectral and temporal measurements of song, and song sharing decreased with geographic distance. However, neutral genetic and song divergence were not correlated, and measures of genetic differentiation and migration estimates indicated gene flow across leks. The persistence of acoustic structuring in wedge-tailed sabrewings may thus best be explained by stochastic processes across leks, in which intraspecific vocal variation is maintained in the absence of genetic differentiation by postdispersal learning and social conditions, and by geographical isolation due to the accumulation of small differences, producing most dramatic changes between populations further apart.     

Call divergence is correlated with geographic and genetic distance in greenish warblers (Phylloscopus trochiloides): a strong role for stochasticity in signal evolution?

Divergence in signalling systems might play a central role in speciation. To assess the importance of possible causes of signal divergence, we examine two types of vocalizations within a geographically variable species complex, the greenish warblers (Phylloscopus trochiloides Sundevall). Calls, which are used by both sexes throughout the year, and songs, which are sung primarily by breeding males, differ distinctly between two distinct Siberian forms. Through a ring of southern populations that connect the northern forms, signal divergence is correlated with both geographic distance and genetic divergence. Calls and songs differ in their particular patterns of geographic variation, probably because of the larger influence of sexual selection on songs than on calls. These patterns are supportive of neither acoustic adaptation nor morphology being major drivers of divergence in vocalizations. Rather, these results support the importance of stochastic evolution of communication systems in the evolution of new species.     

A case of spontaneous acquisition of a human sound by an orangutan

The capacity of nonhuman primates to actively modify the acoustic structure of existing sounds or vocalizations in their repertoire appears limited. Several studies have reported population or community differences in the acoustical structure of nonhuman primate long distance calls and have suggested vocal learning as a mechanism for explaining such variation. In addition, recent studies on great apes have indicated that there are repertoire differences between populations. Some populations have sounds in their repertoire that others have not. These differences have also been suggested to be the result of vocal learning. On yet another level great apes can, after extensive human training, also learn some species atypical vocalizations. Here we show a new aspect of great ape vocal learning by providing data that an orangutan has spontaneously (without any training) acquired a human whistle and can modulate the duration and number of whistles to copy a human model. This might indicate that the learning capacities of great apes in the auditory domain might be more flexible than hitherto assumed. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

GEOGRAPHIC VARIATION IN THE SONGS OF NEOTROPICAL SINGING MICE: TESTING THE RELATIVE IMPORTANCE OF DRIFT AND LOCAL ADAPTATION

Patterns of geographic variation in communication systems can provide insight into the processes that drive phenotypic evolution. Although work in birds, anurans, and insects demonstrates that acoustic signals are sensitive to diverse selective and stochastic forces, processes that shape variation in mammalian vocalizations are poorly understood. We quantified geographic variation in the advertisement songs of sister species of singing mice, montane rodents with a unique mode of vocal communication. We tested three hypotheses to explain spatial variation in the song of the lower altitude species, Scotinomys teguina: selection for species recognition in sympatry with congener, S. xerampelinus, acoustic adaptation to different environments, and stochastic divergence. Mice were sampled at seven sites in Costa Rica and Panamá; genetic distances were estimated from mitochondrial control region sequences, between‐site differences in acoustic environment were estimated from climatic data. Acoustic, genetic and geographic distances were all highly correlated in S. teguina, suggesting that population differentiation in song is largely shaped by genetic drift. Contrasts between interspecific genetic‐acoustic distances were significantly greater than expectations derived from intraspecific contrasts, indicating accelerated evolution of species‐specific song. We propose that, although much intraspecific acoustic variation is effectively neutral, selection has been important in shaping species differences in song.     

Phylogenetic and ecological effects on interspecific variation in structurally simple avian vocalizations

Flight calls are structurally simple avian vocalizations largely associated with sustained migratory flight. We used a multilocus phylogeny of 47 North American wood warblers (Aves: Parulidae) to quantify the extent of phylogenetic signal in flight-call spectrographic characteristics and to remove phylogenetic effects when testing for associations among flight-call attributes, behavioural characters related to migration strategies and ecological habitat variables. We also employed a quantile regression and null model approach to compare a matrix of interspecific phylogenetic divergence with indices of the corresponding acoustic differences derived from spectrographic measurements of flight calls. Nearly half of the measurements of flight-call properties exhibited significant associations with phylogeny. Controlling for phylogenetic effects, high-frequency flight calls were associated with species occupying taller and more open forest canopies. Ecological properties associated with migratory and winter distributions did not correlate with flight-call characteristics. Differences among the evolutionary histories of structural vs. signal properties of flightcalls suggest that phylogenetic and ecological effects are present. The evolution of flight-call syllable structure may involve selection for species recognition, whereas adaptation to the acoustic environment likely has influenced evolution of their spectral and temporal properties. More generally, the historical contribution to variation in behavioural characters is a long-standing source of debate; these results suggest that substantial phylogenetic effects may be present even in vocal traits that may be highly labile. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 155–173.     

Vocal Repertoire of Cebus capucinus: Acoustic Structure, Context, and Usage

Researchers studying nonhuman primate vocal repertoires suggest that convergent environmental, social, and motivational factors account for intra- and interspecific vocal variation. We provide a detailed overview of the vocal repertoire of white-faced capuchins, including acoustic analyses and contextual information of vocal production and vocal usage by different age-sex classes in social interactions. The repertoire is a mixture of graded and discrete vocalizations. In addition, there is general support for structural variation in vocalizations with changes in arousal level. We also identified several combined vocalizations, which might represent variable underlying motivations. Lastly, by including data on the social contexts and production of vocalizations by different age-sex classes, we provide preliminary information about the function of vocalizations in social interactions for individuals of different rank, age, and sex. Future studies are necessary to explore the function of combined vocalizations and how the social function of vocalizations relate to their acoustic structure, because social use of vocalizations may play an important role in shaping vocal evolution.     

Learned Vocal Variation Is Associated with Abrupt Cryptic Genetic Change in a Parrot Species Complex

Contact zones between subspecies or closely related species offer valuable insights into speciation processes. A typical feature of such zones is the presence of clinal variation in multiple traits. The nature of these traits and the concordance among clines are expected to influence whether and how quickly speciation will proceed. Learned signals, such as vocalizations in species having vocal learning (e.g. humans, many birds, bats and cetaceans), can exhibit rapid change and may accelerate reproductive isolation between populations. Therefore, particularly strong concordance among clines in learned signals and population genetic structure may be expected, even among continuous populations in the early stages of speciation. However, empirical evidence for this pattern is often limited because differences in vocalisations between populations are driven by habitat differences or have evolved in allopatry. We tested for this pattern in a unique system where we may be able to separate effects of habitat and evolutionary history. We studied geographic variation in the vocalizations of the crimson rosella (Platycercus elegans) parrot species complex. Parrots are well known for their life-long vocal learning and cognitive abilities. We analysed contact calls across a ca 1300 km transect encompassing populations that differed in neutral genetic markers and plumage colour. We found steep clinal changes in two acoustic variables (fundamental frequency and peak frequency position). The positions of the two clines in vocal traits were concordant with a steep cline in microsatellite-based genetic variation, but were discordant with the steep clines in mtDNA, plumage and habitat. Our study provides new evidence that vocal variation, in a species with vocal learning, can coincide with areas of restricted gene flow across geographically continuous populations. Our results suggest that traits that evolve culturally can be strongly associated with reduced gene flow between populations, and therefore may promote speciation, even in the absence of other barriers.     

Does vocal learning accelerate acoustic diversification? Evolution of contact calls in Neotropical parrots

Learning has been traditionally thought to accelerate the evolutionary change of behavioural traits. We evaluated the evolutionary rate of learned vocalizations and the interplay of morphology and ecology in the evolution of these signals. We examined contact calls of 51 species of Neotropical parrots from the tribe Arini. Parrots are ideal subjects due to their wide range of body sizes and habitats, and their open‐ended vocal learning that allows them to modify their calls throughout life. We estimated the evolutionary rate of acoustic parameters of parrot contact calls and compared them to those of morphological traits and habitat. We also evaluated the effect of body mass, bill length, vegetation density and species interactions on acoustic parameters of contact calls while controlling for phylogeny. Evolutionary rates of acoustic parameters did not differ from those of our predictor variables except for spectral entropy, which had a significantly slower rate of evolution. We found support for correlated evolution of call duration, and fundamental and peak frequencies with body mass, and of fundamental frequency with bill length. The degree of sympatry between species did not have a significant effect on acoustic parameters. Our results suggest that parrot contact calls, which are learned acoustic signals, show evolutionary rates similar to those of morphological traits. This is the first study to our knowledge to provide evidence that change through cultural evolution does not necessarily accelerate the evolutionary rate of traits acquired through life‐long vocal learning.     

Structural Classification of Wild Boar (Sus scrofa) Vocalizations

Determining whether a species' vocal communication system is graded or discrete requires definition of its vocal repertoire. In this context, research on domestic pig (Sus scrofa domesticus) vocalizations, for example, has led to significant advances in our understanding of communicative functions. Despite their close relation to domestic pigs, little is known about wild boar (Sus scrofa) vocalizations. The few existing studies, conducted in the 1970s, relied on visual inspections of spectrograms to quantify acoustic parameters and lacked statistical analysis. Here, we use objective signal processing techniques and advanced statistical approaches to classify 616 calls recorded from semi‐free ranging animals. Based on four spectral and temporal acoustic parameters—quartile Q25, duration, spectral flux, and spectral flatness—extracted from a multivariate analysis, we refine and extend the conclusions drawn from previous work and present a statistically validated classification of the wild boar vocal repertoire into four call types: grunts, grunt‐squeals, squeals, and trumpets. While the majority of calls could be sorted into these categories using objective criteria, we also found evidence supporting a graded interpretation of some wild boar vocalizations as acoustically continuous, with the extremes representing discrete call types. The use of objective criteria based on modern techniques and statistics in respect to acoustic continuity advances our understanding of vocal variation. Integrating our findings with recent studies on domestic pig vocal behavior and emotions, we emphasize the importance of grunt‐squeals for acoustic approaches to animal welfare and underline the need of further research investigating the role of domestication on animal vocal communication.     

Convergence and divergence in Diana monkey vocalizations

Individually distinct vocalizations are widespread among social animals, presumably caused by variation in vocal tract anatomy. A less-explored source of individual variation is due to learned movement patterns of the vocal tract, which can lead to vocal convergence or divergence in social groups. We studied patterns of acoustic similarity in a social call produced by 14 female Diana monkeys (Cercopithecus diana) in two free-ranging groups. Calls showed variability in fundamental frequency contours owing to individual identity and external context. Vocal divergence increased significantly between females during poor visibility and tended to increase in the presence of neighbours. In contrast, vocal convergence increased significantly between females during vocal interactions, because females matched the frequency contour of their own call with another female's preceding call. Our findings demonstrate that these primates have some control over the acoustic fine structure of their most important social vocalization. Vocal convergence and divergence are two opposing processes that enable callers to ensure spatial proximity and social cohesion with other group members.     

Age- and Sex-Related Variations in Clear Calls of <Emphasis Type="Italic">Papio ursinus</Emphasis>

Changes in vocalizations during ontogeny can in principle be related to three factors: growth, maturation, and experience, i.e., learning. While learning is a prerequisite for the proper development of speech, it hardly appears to play a role in the development of the species-typical vocal behavior of nonhuman primates. Nonetheless, subjects of different age and sex often exhibit prominent variation in the structure of their vocalizations. We investigated ontogenetic changes and the emergence of sex-related differences in the acoustic structure of Chacma baboon (Papio ursinus) clear calls. We recorded the vocalizations emitted by individuals separated from the rest of the group or from particular individuals, in a group of baboons in the Moremi Wildlife Reserve, Botswana. We analyzed calls from 58 baboons of both sexes and all age classes. While the structure of the call appeared to be fixed from birth, call duration, the distribution of energy, and the fundamental frequency of the calls, including modulation, varied with age and sex of the caller. We discuss how body size may explain the variations. Some of the variables exhibited a different profile of variation with age between the sexes, with significant differences becoming apparent around puberty. The emergence of these sexual differences may be explained by the onset of sexual dimorphism in body size and mass. To which degree the hormonal status contributes to variation in the calling remains to be investigated.     

Evidence for Dialects in Three Captive Populations of Common Marmosets (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>)

The vocal repertoires of nonhuman primates have long been thought to be invariable across populations and not to result from vocal learning. However, increasing evidence suggests that learning does influence vocal production in nonhuman primates, and that several species modify the structure of their calls in response to social or environmental influences. Vocal usage learning refers to the process whereby an individual learns in which circumstances to produce a certain call type, whereas vocal production learning refers to the process in which signals get modified as the result of individual experiences. Common marmosets (Callithrix jacchus) show socially mediated vocal plasticity as adults and during vocal development. This propensity to engage in simple forms of vocal production learning (accommodation) should produce population-level differences in call structure. To test this prediction, we compared the vocalizations of three captive populations of common marmosets. We analyzed the acoustic structure of 1337 phee calls, 461 trills, and 3611 food calls and compared them with a permutated discriminant function analysis. We found that all call types differed significantly between the three populations, and 76–98% of the calls were correctly classified. As physical differences in body mass and environmental differences between colonies could not explain the call differences, we conclude that vocal accommodation is the most likely explanation for the differences in call structure. This will allow us to further investigate the role and importance of vocal learning in a species increasingly used to study vocal learning and language evolution.     

Ecological drivers of song evolution in birds: Disentangling the effects of habitat and morphology

Environmental differences influence the evolutionary divergence of mating signals through selection acting either directly on signal transmission (“sensory drive”) or because morphological adaptation to different foraging niches causes divergence in “magic traits” associated with signal production, thus indirectly driving signal evolution. Sensory drive and magic traits both contribute to variation in signal structure, yet we have limited understanding of the relative role of these direct and indirect processes during signal evolution. Using phylogenetic analyses across 276 species of ovenbirds (Aves: Furnariidae), we compared the extent to which song evolution was related to the direct influence of habitat characteristics and the indirect effect of body size and beak size, two potential magic traits in birds. We find that indirect ecological selection, via diversification in putative magic traits, explains variation in temporal, spectral, and performance features of song. Body size influences song frequency, whereas beak size limits temporal and performance components of song. In comparison, direct ecological selection has weaker and more limited effects on song structure. Our results illustrate the importance of considering multiple deterministic processes in the evolution of mating signals.     

Parallel evolutionary forces influence the evolution of male and female songs in a tropical songbird

Given the important role that animal vocalizations play in mate attraction and resource defence, acoustic signals are expected to play a significant role in speciation. Most studies, however, have focused on the acoustic traits of male animals living in the temperate zone. In contrast to temperate environments, in the tropics, it is commonplace for both sexes to produce complex acoustic signals. Therefore, tropical birds offer the opportunity to compare the sexes and provide a more comprehensive understanding of the evolution of animal signals. In this study, we quantified patterns of acoustic variation in Rufous‐and‐white Wrens (Thryophilus rufalbus) from five populations in Central America. We quantified similarities and differences between male and female songs by comparing the role that acoustic adaptation, cultural isolation and neutral genetic divergence have played in shaping acoustic divergence. We found that males and females showed considerable acoustic variation across populations, although females exhibited greater population divergence than males. Redundancy analysis and partial‐redundancy analysis revealed significant relationships between acoustic variation and ecological variables, genetic distance, and geographic distance. Both ambient background noise and geographic distance explained a high proportion of variance for both males and females, suggesting that both acoustic adaptation and cultural isolation influence song. Overall, our results indicate that parallel evolutionary forces act on male and female acoustic signals and highlight the important role that cultural drift and selection play in the evolution of both male and female songs.     

Calling at the highway: The spatiotemporal constraint of road noise on Pacific chorus frog communication

Loss of acoustic habitat due to anthropogenic noise is a key environmental stressor for vocal amphibian species, a taxonomic group that is experiencing global population declines. The Pacific chorus frog (Pseudacris regilla) is the most common vocal species of the Pacific Northwest and can occupy human‐dominated habitat types, including agricultural and urban wetlands. This species is exposed to anthropogenic noise, which can interfere with vocalizations during the breeding season. We hypothesized that Pacific chorus frogs would alter the spatial and temporal structure of their breeding vocalizations in response to road noise, a widespread anthropogenic stressor. We compared Pacific chorus frog call structure and ambient road noise levels along a gradient of road noise exposures in the Willamette Valley, Oregon, USA. We used both passive acoustic monitoring and directional recordings to determine source level (i.e., amplitude or volume), dominant frequency (i.e., pitch), call duration, and call rate of individual frogs and to quantify ambient road noise levels. Pacific chorus frogs were unable to change their vocalizations to compensate for road noise. A model of the active space and time (“spatiotemporal communication”) over which a Pacific chorus frog vocalization could be heard revealed that in high‐noise habitats, spatiotemporal communication was drastically reduced for an individual. This may have implications for the reproductive success of this species, which relies on specific call repertoires to portray relative fitness and attract mates. Using the acoustic call parameters defined by this study (frequency, source level, call rate, and call duration), we developed a simplified model of acoustic communication space–time for this species. This model can be used in combination with models that determine the insertion loss for various acoustic barriers to define the impact of anthropogenic noise on the radius of communication in threatened species. Additionally, this model can be applied to other vocal taxonomic groups provided the necessary acoustic parameters are determined, including the frequency parameters and perception thresholds. Reduction in acoustic habitat by anthropogenic noise may emerge as a compounding environmental stressor for an already sensitive taxonomic group.     

Spectral call features provide information about the aggression level of greater mouse-eared bats (Myotis myotis) during agonistic interactions

Bats rely heavily on acoustic signals in order to communicate with each other in a variety of social contexts. Among those, agonistic interactions and accompanying vocalizations have received comparatively little study. Here, we studied the communicational behaviour between male greater mouse-eared bats (Myotis myotis) during agonistic encounters. Two randomly paired adult males were placed in a box that allowed us to record video and sound synchronously. We describe their vocal repertoire and compare the acoustic structure of vocalizations between two aggression levels, which we quantified via the bats’ behaviour. By inspecting thirty, one-minute long encounters, we identified a rich variety of social calls that can be described as two basic call types: echolocation-like, low-frequency sweeps and long, broadband squawks. Squawks, the most common vocalization, were often noisy, i.e. exhibited a chaotic spectral structure. We further provide evidence for individual signatures and the presence of nonlinear phenomena in this species’ vocal repertoire. As the usage and acoustic structure of vocalizations is known to encode the internal state of the caller, we had predicted that the spectral structure of squawks would be affected by the caller’s aggression level. Confirming our hypothesis, we found that increased aggression positively correlated with an increase in call frequency and tonality. We hypothesize that the extreme spectral variability between and within squawks can be explained by small fluctuations in vocal control parameters (e.g. subglottal pressure) that are caused by the elevated arousal, which is in turn influenced by the aggression level.