Phylogeny and the evolution of calling songs in Gryllus (Insecta, Orthoptera, Gryllidae)

Acoustic signalling is the most important communication modality for crickets. While it has been studied intensively, few authors have analysed the evolution of cricket acoustic signals within a macroevolutionary perspective, still fewer with respect to its phylogenetic aspects. This may be due in part to the lack of acoustic and phylogenetic data; there are also difficulties involved in applying phylogenetic methods to acoustic data. The most critical aspect may be describing calls using characteristics consistent with current criteria for homology. In this paper we discuss, in relation to the evolution of the North American species of Gryllus , the reliability of these criteria and describe songs using two complementary sets of characters: (i) general structure (carrier frequencies and main temporal features), and (ii) 'special quality' (particular features at a lower structural level).     

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.     

How the environment shapes animal signals: a test of the acoustic adaptation hypothesis in frogs

Long‐distance acoustic signals are widely used in animal communication systems and, in many cases, are essential for reproduction. The acoustic adaptation hypothesis (AAH) implies that acoustic signals should be selected for further transmission and better content integrity under the acoustic constraints of the habitat in which they are produced. In this study, we test predictions derived from the AAH in frogs. Specifically, we focus on the difference between torrent frogs and frogs calling in less noisy habitats. Torrents produce sounds that can mask frog vocalizations and constitute a major acoustic constraint on call evolution. We combine data collected in the field, material from scientific collections and the literature for a total of 79 primarily Asian species, of the families Ranidae, Rhacophoridae, Dicroglossidae and Microhylidae. Using phylogenetic comparative methods and including morphological and environmental potential confounding factors, we investigate putatively adaptive call features in torrent frogs. We use broad habitat categories as well as fine‐scale habitat measurements and test their correlation with six call characteristics. We find mixed support for the AAH. Spectral features of torrent frog calls are different from those of frogs calling in other habitats and are related to ambient noise levels, as predicted by the AAH. However, temporal call features do not seem to be shaped by the frogs’ calling habitats. Our results underline both the complexity of call evolution and the need to consider multiple factors when investigating this issue.     

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.     

Evolution of Acoustic Communication Signals of Mammals: Friendly Close-Range Vocalizations in Felidae (Carnivora)

The distribution of the three friendly close-range vocalization types known in the Felidae was plotted on a recently published phylogeny of the cat family (Felidae) based on sequence comparisons of two mitochondrial DNA genes and other molecular and biochemical characters, with extrapolated divergence ages of its various lineages. It was found to be congruent with this phylogeny. One of the sound types is likely to be present in 30 species of the family (documented in 22 so far), another is present in 4, and the third in 2 species only; these sound types represent a phylogenetic transformation series. The latter two vocalization types also differ considerably from the first in the mode of sound production. From this, evolutionary conservatism over a long epoch for the one widespread vocalization type can be inferred, and less conservatism in the type present in four species, while the emergence of the least common type is evidence of relatively considerable and rapid evolutionary change. Thus, acoustic communication signals in a group of taxa can evolve at considerably different rates, and for a specific character this rate can differ between different lineages of that group. The ultimate causes of the evolutionary stability or of the subsequent relatively rapid change in sound structure and mode of sound production in these felid vocalizations are unknown.     

Airborne vs. radio-transmitted vocalizations in two primates: a technical report

Elucidating the structure and function of joint vocal displays (e.g. duet, chorus) recorded with a conventional microphone has proved difficult in some animals owing to the complex acoustic properties of the combined signal, a problem reminiscent of multi-speaker conversations in humans. Towards this goal, we set out to simultaneously compare air-transmitted (AT) with radio-transmitted (RT) vocalizations in one pair of humans and one pair of captive Bolivian grey titi monkeys (Plecturocebus donacophilus) all equipped with an accelerometer – or vibration transducer – closely apposed to the larynx. First, we observed no crosstalk between the two radio transmitters when subjects produced vocalizations at the same time close to each other. Second, compared with AT acoustic recordings, sound segmentation and pitch tracking of the RT signal was more accurate, particularly in a noisy and reverberating environment. Third, RT signals were less noisy than AT signals and displayed more stable amplitude regardless of distance, orientation and environment of the animal. The microphone outperformed the accelerometer with respect to sound spectral bandwidth and speech intelligibility: the sounds of RT speech were more attenuated and dampened as compared to AT speech. Importantly, we show that vocal telemetry allows reliable separation of the subjects’ voices during production of joint vocalizations, which has great potential for future applications of this technique with free-ranging animals.     

SENSORY DRIVE DOES NOT EXPLAIN REPRODUCTIVE CHARACTER DISPLACEMENT OF MALE ACOUSTIC SIGNALS IN THE UPLAND CHORUS FROG (PSEUDACRIS FERIARUM)

Biotic and abiotic factors have been proposed to explain patterns of reproductive character displacement, but which factor is most important to character displacement of acoustic signals is not clear. Male vocalizations of the frog Pseudacris feriarum are known to undergo reproductive character displacement in areas of sympatry with P. brimleyi and P. nigrita. Despite evidence for reinforcement as an important mechanism, local adaptation via sensory drive might explain this pattern because Pseudacris breed in different habitat types and mating signals are exposed to a variety of environments. We tested the sensory drive hypothesis by playing synthesized vocalizations representing the spectrum of variation in P. feriarum at 12 different study sites. If sensory drive has occurred, then vocalizations should transmit better in the site of origin or at ecologically similar sites. We found that variation in acoustic signals did not produce better transmission in particular sites, the effect of site was uniform, and acoustic signals often transmitted better in habitats external to their origin. Ecological variation among habitats did not explain signal degradation. Our playback experiments, ecological analyses, and comparisons of different habitat types provide no support for sensory drive as a process promoting reproductive character displacement in this system. Reinforcement is the more likely primary mechanism.     

Nonlinear acoustic complexity in a fish 'two-voice' system

Acoustic signals play essential roles in social communication and show a strong selection for novel morphologies leading to increased call complexity in many taxa. Among vertebrates, repeated innovations in the larynges of frogs and mammals and the syrinx of songbirds have enhanced the spectro-temporal content, and hence the diversity of vocalizations. This acoustic diversification includes nonlinear characteristics that expand frequency profiles beyond the traditional categorization of harmonic and broadband calls. Fishes have remained a notable exception to evidence for such acoustic innovations among vertebrates, despite their being the largest group of living vertebrates that also exhibit widespread evolution of sound production. Here, we combine rigorous acoustic and mathematical analyses with experimental silencing of the vocal motor system to show how a novel swim bladder mechanism in a toadfish enables it to generate calls exhibiting nonlinearities like those found among frogs, birds and mammals, including primates. By showing that fishes have evolved nonlinear acoustic signalling like all other major lineages of vocal vertebrates, these results suggest strong selection pressure favouring this mechanism to enrich the spectro-temporal content and complexity of vocal signals.     

Neotropical frogs and mating songs: The evolution of advertisement calls in glassfrogs

Anurans emit advertisement calls with the purpose of attracting mates and repelling conspecific competitors. The evolution of call traits is expected to be associated with the evolution of anatomical and behavioural traits due to the physics of call emission and transmission. The evolution of vocalizations might imply trade‐offs with other energetically costly behaviours, such as parental care. Here, we investigated the association between body size, calling site, parental care and call properties (call duration, number of notes, peak frequency, frequency bandwidth and call structure) of the advertisement calls of glassfrogs (Centrolenidae)—a family of Neotropical, leaf‐dwelling anurans—using phylogenetic comparative methods. We also explored the tempo and mode of evolution of these traits and compared them with those of three morphological traits associated with body size, locomotion and feeding. We generated and compiled acoustic data for 72 glassfrog species (46% of total species richness), including representatives of all genera. We found that almost all acoustic traits have significant, but generally modest, phylogenetic signal. Peak frequency of calls is significantly associated with body size, whereas call structure is significantly associated with calling site and paternal care. Thus, the evolution of body size, calling site and paternal care could constrain call evolution. The estimated disparity of acoustic traits was larger than that of morphological traits and the peak in disparity of acoustic traits generally occurred later in the evolution of glassfrogs, indicating a historically recent outset of the acoustic divergence in this clade.     

Reconstructing the evolution of complex bird song in the oropendolas

The elaborate songs of songbirds are frequent models for investigating the evolution of animal signals. However, few previous studies have attempted to reconstruct historical changes in song evolution using a phylogenetic comparative approach. In particular, no comparative studies of bird song have used a large number of vocal characters and a well-supported, independently derived phylogeny. We identified 32 features in the complex vocal displays of male oropendolas (genera Psarocolius, Gymnostinops, and Ocyalus) that are relatively invariant within taxa and mapped these characters onto a robust molecular phylogeny of the group. Our analysis revealed that many aspects of oropendola song are surprisingly evolutionarily conservative and thus are potentially useful characters for reconstructing historical patterns. Of the characters that varied among taxa, nearly two thirds (19 of 29) showed no evidence of evolutionary convergence or reversal when mapped onto the tree, which was reflected in a high overall consistency index (CI = 0.78) and retention index (RI = 0.88). Some reconstructed patterns provided evidence of selection on these signals. For example, rapid divergence of the songs of the Montezuma oropendola, Gymnostinops montezuma, from those of closely related taxa suggests the recent influence of strong sexual selection. In general, our results provide insights into the mode of vocal evolution in songbirds and suggest that complex vocalizations can provide information about phylogeny. Based on this evidence, we use song characters to estimate the phylogenetic affinities of three oropendola taxa for which molecular data are not yet available.     

Ontogenesis of agonistic vocalizations in the cichlid fish Metriaclima zebra

While acoustic communication has been described in adults of various fish species, our knowledge about the ontogeny of fish sound production is limited. In adults, sound signals are known to be involved during aggressive interactions. However, aggressive behaviour may appear early in the life of fishes due to the possible competition for food and space. If acoustic signals are used to send information to competitors, sounds are likely to play a role during interactions between juvenile fish as well. The apparition and evolution of sound production were monitored in a group of juveniles of the cichlid fish Metriaclima zebra from hatching to 4months of age. In addition, the link between vocalizations and agonistic behaviour was studied during dyadic interactions at three different ages. Sounds production appeared to be present early in the development of this fish and increased along with the number of aggressive behaviours. Recorded sounds consisted, in juveniles, in isolated pulses showing a decrease in frequency and duration as the fish grew. In adults, sounds became bursts of pulses but the transition from isolated to repetitive pulses was not observed. These results are compared to the existing literature on sound production ontogeny in fishes.     

Phylogeny of North American fireflies (Coleoptera: Lampyridae): implications for the evolution of light signals

Representatives of the beetle family Lampyridae ("fireflies", "lightningbugs") are well known for their use of light signals for species recognition during mate search. However, not all species in this family use light for mate attraction, but use chemical signals instead. The lampyrids have a worldwide distribution with more than 2000 described species, but very little is known about their phylogenetic relationships. Within North America, some lampyrids use pheromones as the major mating signal whereas others use visual signals such as extended glows or short light flashes. Here, we use a phylogenetic approach to illuminate the relationships of North American lampyrids and the evolution of their mating signals. Specifically, to establish the first phylogeny of all North American lampyrid genera, we sequenced nuclear (18S) and mitochondrial (16S and COI) genes to investigate the phylogenetic relationships of 26 species from 16 North American (NA) genera and one species from the genus Pterotus that was removed recently from the Lampyridae. To test the monophyly of the NA firefly fauna we sequenced the same genes from three European lampyrids and three Asian lampyrids, and included all available Genbank data (27 additional Asian lampyrids and a former lampyrid from Asia, Rhagophthalmus). Our results show that the North American lampyrids are not monophyletic. Different subgroups are closely related to species from Europe, Asia and tropical America, respectively. The present classification of fireflies into subfamilies and tribes is not, for the most part, supported by our phylogenetic analysis. Two former lampyrid genera, Pterotus and Rhagophthalmus, which have recently been removed from this family, are in fact nested within the Lampyridae. Further, we found that the use of light as a sexual signal may have originated one or four times among lampyrids, followed by nine or four losses, respectively. Short flashes originated at least twice and possibly three times independently among our study taxa. The use of short flashes as a mating signal was replaced at least once by the use of long glows, and light signals as mating signals were lost at least three times in our study group and replaced by pheromones as the main signal mode.     

Recovering phylogenetic signal from frog mating calls

Goicoechea, N., De La Riva, I. & Padial, J. M. (2010). Recovering phylogenetic signal from frog mating calls. —Zoologica Scripta, 39, 411–154. Few studies have tried to analyse the phylogenetic information contained in frog mating calls. While some of those studies suggest that sexual selection deletes any phylogenetic signal, others indicate that frog calls do retain phylogenetic informative characters. Discordant results can be the outcome of disparate rates of character evolution and evolutionary plasticity of call characters in different groups of frogs, but also the result of applying different coding methods. No study to date has compared the relative performance of different coding methods in detecting phylogenetic signal in calls, hampering thus potential consilience between previous results. In this study, we analyse the strength of phylogenetic signal in 10 mating call characters of 11 related species of frogs belonging to three genera of Andean and Amazonian frogs (Anura: Terrarana: Strabomantidae). We use six quantitative characters (number of notes per call, note length, call length, number of pulses per note, fundamental frequency and dominant frequency) and four qualitative ones (presence/absence of: pseudopulses, frequency modulation in notes, amplitude modulation in notes and amplitude modulation in pulses). We code quantitative characters using four different coding and scaling methods: (i) gap‐coding, (ii) fixed‐scale, (iii) step‐matrix gap‐weighting with between‐characters scaling, and (iv) step‐matrix gap‐weighting with between‐states scaling. All four coding methods indicate that frog calls contain phylogenetic information. These results suggest that divergent selection on frog mating calls may not always be strong enough to eliminate phylogenetic signal. However, coding methods strongly affect the amount of recoverable information. Step‐matrix gap‐weighting with between‐characters scaling and gap‐coding are suggested as the best methods available for coding quantitative characters of frog calls. Also, our results indicate that the arbitrariness in selecting character states and the method for scaling transitions weights, rather than the number of character states, is what potentially biases phylogenetic analyses with quantitative characters.     

Male vocal behavior and phylogeny in deer

The phylogenetic relationships among 11 species of the Cervidae family were inferred from an analysis of male vocalizations. Eighteen characters, including call types (e.g. antipredator barks, mating loudcalls) and acoustic characteristics (call composition, fundamental frequency and formant frequencies), were used for phylogeny inference. The resulting topology and the phylogenetic consistency of behavioral characters were compared with those of current molecular phylogenies of Cervidae and with separate and simultaneous parsimony analyses of molecular and behavioral data. Our results indicate that male vocalizations constitute plausible phylogenetic characters in this taxon. Evolutionary scenarios for the vocal characters are discussed in relation with associated behaviors.     

Social vocalizations of big brown bats vary with behavioral context

Bats are among the most gregarious and vocal mammals, with some species demonstrating a diverse repertoire of syllables under a variety of behavioral contexts. Despite extensive characterization of big brown bat (Eptesicus fuscus) biosonar signals, there have been no detailed studies of adult social vocalizations. We recorded and analyzed social vocalizations and associated behaviors of captive big brown bats under four behavioral contexts: low aggression, medium aggression, high aggression, and appeasement. Even limited to these contexts, big brown bats possess a rich repertoire of social vocalizations, with 18 distinct syllable types automatically classified using a spectrogram cross-correlation procedure. For each behavioral context, we describe vocalizations in terms of syllable acoustics, temporal emission patterns, and typical syllable sequences. Emotion-related acoustic cues are evident within the call structure by context-specific syllable types or variations in the temporal emission pattern. We designed a paradigm that could evoke aggressive vocalizations while monitoring heart rate as an objective measure of internal physiological state. Changes in the magnitude and duration of elevated heart rate scaled to the level of evoked aggression, confirming the behavioral state classifications assessed by vocalizations and behavioral displays. These results reveal a complex acoustic communication system among big brown bats in which acoustic cues and call structure signal the emotional state of a caller.     

Using heterochrony plots to detect the dissociated coevolution of characters

The comparison of developmental sequences among species is notoriously difficult. Here, heterochrony plots are introduced as a new graphic method to detect temporal shifts in the development of characters in pair-wise species comparisons. Plotting the timing of character development in one species against the timing of character development in another species allows us to compare a principally unlimited number of characters simultaneously and can detect whether suites of characters are dissociated from one another or not. Such heterochrony plots can be embedded into a comparative phylogenetic analysis in order to establish whether observed patterns of character codissociation are indeed due to their dissociated coevolution. Comparative phylogenetic analysis may also reveal multiple independent events of dissociated coevolution of the same suite of characters in a certain lineage, suggesting that the characters of this suite reciprocally constrain their evolutionary modifiability, thereby forming a unit of evolution. This ability to identify units of evolution is a prerequisite for assessing the validity of recently proposed scenarios, suggesting that modules of development and/or function tend to act as units of evolution. Starting from a detailed heterochrony plot comparing development in the direct developing frog Eleutherodactylus coqui and in the biphasically developing frog Discoglossus pictus, this comparative approach is illustrated focusing on the evolution of development of limbs, the nervous system and the pharyngeal arches in amphibians.     

Vocal production in nonhuman primates: Acoustics,physiology, and functional constraints on “honest” advertisement

The physiological mechanisms and acoustic principles underlying sound production in primates are important for analyzing and synthesizing primate vocalizations, for determining the range of calls that are physically producible, and for understanding primate communication in the broader comparative context of what is known about communication in other vertebrates. In this paper we discuss what is known about vocal production in nonhuman primates, relying heavily on models from speech and musical acoustics. We first describe the role of the lungs and larynx in generating the sound source, and then discuss the effects of the supralaryngeal vocal tract in modifying this source. We conclude that more research is needed to resolve several important questions about the acoustics of primate calls, including the nature of the vocal tract's contribution to call production. Nonetheless, enough is known to explore the implications of call acoustics for the evolution of primate communication. In particular, we discuss how anatomy and physiology may provide constraints resulting in “honest” acoustic indicators of body size. © 1995 Wiley-Liss, Inc.     

Repeated decrease in vocal repertoire size in Streptopelia doves

Most bird species produce different acoustic signals in different behavioural contexts. This intraspecific variation in signal types is thought to be the result of selection for optimal communication in each context. Doves in the genus Streptopelia have three distinct behavioural contexts in which they produce coo vocalizations. Some Streptopelia species have three acoustically similar coo vocalizations associated with the three contexts, but in others the coo vocalizations differ in acoustic structure. Using a well-resolved phylogeny, we examined whether acoustic differentiation between coo types was the ancestral state. Unexpectedly, the results showed that the common ancestor of Streptopelia had differentiated coos rather than a single coo type. This result implies that context-specific acoustic signals disappeared from the vocal repertoire independently at least two times. We further tested whether different context-dependent signal types follow different evolutionary pathways and whether they differ in rate of evolutionary change. We found that the long-range signal (perch-coo) evolves at a higher rate than the short-range signal (bow-coo). These results are discussed in relation to selection for species recognition and transmission requirements.     

Regulation of vocal amplitude by the blue-throated hummingbird, Lampornis clemenciae

Animals that rely on vocal communication must broadcast sound so that a perceptible signal is transmitted over an appropriate distance. We found that male blue-throated hummingbirds modified the amplitude of their vocalizations in response to both naturally occurring and experimenter-controlled changes in ambient noise levels. This phenomenon is known as the Lombard effect and may increase the efficiency of acoustic signalling. This study demonstrates the effect under natural field conditions and documents the first hummingbird species (Apodiformes: Trochilidae) to show this behaviour. We measured sound pressure levels (SPLs) of Serial Chip territorial advertisement calls across a natural range of ambient noise, primarily due to creeks within male territories. We found a significant correlation between the amplitude of Serial Chips and the amplitude of background noise. To test this relationship, we broadcast recordings of creek noise at high and low amplitudes while target individuals were producing Serial Chip vocalizations. We measured vocal SPLs before and during the playback. Individuals responded to changes in playback creek noise by changing the amplitude of Serial Chip production. We also measured transmission properties of Serial Chip calls through natural habitat to calculate the approximate amplitude of vocalizations at the position of the calling bird. We suggest that amplitude regulation of vocalizations contibutes to signal transmission distance along with the established relationships between singing behaviour, acoustic structure and habitat. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.