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1.  Bioacoustic Field Research: A Primer to Acoustic Analyses and Playback Experiments With Primates 
American Journal of Primatology  2013;75(7):643-663.
Acoustic analyses of primate vocalizations as well as playback experiments are staple methods in primatology. Acoustic analyses have been used to investigate the influence of factors such as individuality, context, sex, age, and size on variation in calls. More recent studies have expanded our knowledge on the effects of phylogenetic relatedness and the structure of primate vocal repertoires in general. Complementary playback experiments allow direct testing of hypotheses regarding the attribution of meaning to calls, the cognitive mechanisms underpinning responses, and/or the adaptive value of primate behavior. After briefly touching on the historical background of this field of research, we first provide an introduction to recording primate vocalizations and discuss different approaches to describe primate calls in terms of their temporal and spectral properties. Second, we present a tutorial regarding the preparation, execution, and interpretation of field playback experiments, including a review of studies that have used such approaches to investigate the responses to acoustic variation in calls including the integration of contextual and acoustic information, recognition of kin and social relationships, and social knowledge. Based on the review of the literature and our own experience, we make a number of recommendations regarding the most common problems and pitfalls. The power of acoustic analyses typically hinges on the quality of the recordings and the number of individuals represented in the sample. Playback experiments require profound knowledge of the natural behavior of the animals for solid interpretation; experiments should be conducted sparingly, to avoid habituation of the subjects to the occurrence of the calls; experimenter-blind designs chosen whenever possible; and researchers should brace themselves for long periods of waiting times until the appropriate moments to do the experiment arise. If all these aspects are considered, acoustic analyses and field playback experiments provide unique insights into primate communication and cognition. Am. J. Primatol. 75:643–663, 2013. © 2013 Wiley Periodicals, Inc.
PMCID: PMC3698702  PMID: 23592340
acoustic analysis; alarm calls; cognition; communication; playback experiments
2.  Call Transmission Efficiency in Native and Invasive Anurans: Competing Hypotheses of Divergence in Acoustic Signals 
PLoS ONE  2013;8(10):e77312.
Invasive species are a leading cause of the current biodiversity decline, and hence examining the major traits favouring invasion is a key and long-standing goal of invasion biology. Despite the prominent role of the advertisement calls in sexual selection and reproduction, very little attention has been paid to the features of acoustic communication of invasive species in nonindigenous habitats and their potential impacts on native species. Here we compare for the first time the transmission efficiency of the advertisement calls of native and invasive species, searching for competitive advantages for acoustic communication and reproduction of introduced taxa, and providing insights into competing hypotheses in evolutionary divergence of acoustic signals: acoustic adaptation vs. morphological constraints. Using sound propagation experiments, we measured the attenuation rates of pure tones (0.2–5 kHz) and playback calls (Lithobates catesbeianus and Pelophylax perezi) across four distances (1, 2, 4, and 8 m) and over two substrates (water and soil) in seven Iberian localities. All factors considered (signal type, distance, substrate, and locality) affected transmission efficiency of acoustic signals, which was maximized with lower frequency sounds, shorter distances, and over water surface. Despite being broadcast in nonindigenous habitats, the advertisement calls of invasive L. catesbeianus were propagated more efficiently than those of the native species, in both aquatic and terrestrial substrates, and in most of the study sites. This implies absence of optimal relationship between native environments and propagation of acoustic signals in anurans, in contrast to what predicted by the acoustic adaptation hypothesis, and it might render these vertebrates particularly vulnerable to intrusion of invasive species producing low frequency signals, such as L. catesbeianus. Our findings suggest that mechanisms optimizing sound transmission in native habitat can play a less significant role than other selective forces or biological constraints in evolutionary design of anuran acoustic signals.
PMCID: PMC3796471  PMID: 24155940
3.  How Noisy Does a Noisy Miner Have to Be? Amplitude Adjustments of Alarm Calls in an Avian Urban ‘Adapter’ 
PLoS ONE  2012;7(1):e29960.
Urban environments generate constant loud noise, which creates a formidable challenge for many animals relying on acoustic communication. Some birds make vocal adjustments that reduce auditory masking by altering, for example, the frequency (kHz) or timing of vocalizations. Another adjustment, well documented for birds under laboratory and natural field conditions, is a noise level-dependent change in sound signal amplitude (the ‘Lombard effect’). To date, however, field research on amplitude adjustments in urban environments has focused exclusively on bird song.
We investigated amplitude regulation of alarm calls using, as our model, a successful urban ‘adapter’ species, the Noisy miner, Manorina melanocephala. We compared several different alarm calls under contrasting noise conditions.
Individuals at noisier locations (arterial roads) alarm called significantly more loudly than those at quieter locations (residential streets). Other mechanisms known to improve sound signal transmission in ‘noise’, namely use of higher perches and in-flight calling, did not differ between site types. Intriguingly, the observed preferential use of different alarm calls by Noisy miners inhabiting arterial roads and residential streets was unlikely to have constituted a vocal modification made in response to sound-masking in the urban environment because the calls involved fell within the main frequency range of background anthropogenic noise.
The results of our study suggest that a species, which has the ability to adjust the amplitude of its signals, might have a ‘natural’ advantage in noisy urban environments.
PMCID: PMC3251594  PMID: 22238684
4.  Changes in breeding phenology of eastern Ontario frogs over four decades 
Ecology and Evolution  2013;3(4):835-845.
Global climate change has been implicated in phenological shifts for a variety of taxa. Amphibian species in particular are sensitive to changes in their environment due to their biphasic life history and restricted reproductive requirements. Previous research has shown that not all temperate amphibian species respond similarly to the same suite of climatic or environmental cues, nor are individual species necessarily uniform in their responses across their range. We examined both the timing of spring emergence and calling phenology of eight anuran species in southeastern Ontario, Canada, using an approximately 40-year dataset of historical records of amphibian activity. Rana pipiens was the only species out of eight considered to emerge significantly earlier, by an estimated 22 days over four decades. Both R. pipiens and Bufo americanus have advanced initiation of calling over a four-decade span significantly earlier by an estimated 37.2 and 19.2 days, respectively. Rana sylvatica showed a trend toward earlier emergence by 19 days, whereas we did not detect changes in emergence phenology for the remaining five species. This significant shift in breeding behavior for two species correlates to significant regional increases in spring temperatures of an estimated 2.7–2.8°C overall over four decades. Our study suggests that local temperature increases have affected the timing of emergence and the onset of calling activity in some Ontario anuran species. Global decline or range shifts ultimately may be related to changes in reproductive behavior and timing mediated by shifting climate.
PMCID: PMC3631398  PMID: 23610628
Anuran; calling activity; climate change; emergence; precipitation; reproductive timing; temperature
5.  Real estate ads in Emei music frog vocalizations: female preference for calls emanating from burrows 
Biology Letters  2011;8(3):337-340.
During female mate choice, both the male's phenotype and resources (e.g. his nest) contribute to the chooser's fitness. Animals other than humans are not known to advertise resource characteristics to potential mates through vocal communication; although in some species of anurans and birds, females do evaluate male qualities through vocal communication. Here, we demonstrate that calls of the male Emei music frog (Babina dauchina), vocalizing from male-built nests, reflect nest structure information that can be recognized by females. Inside-nest calls consisted of notes with energy concentrated at lower frequency ranges and longer note durations when compared with outside-nest calls. Centre frequencies and note durations of the inside calls positively correlate with the area of the burrow entrance and the depth of the burrow, respectively. When given a choice between outside and inside calls played back alternately, more than 70 per cent of the females (33/47) chose inside calls. These results demonstrate that males of this species faithfully advertise whether or not they possess a nest to potential mates by vocal communication, which probably facilitates optimal mate selection by females. These results revealed a novel function of advertisement calls, which is consistent with the wide variation in both call complexity and social behaviour within amphibians.
PMCID: PMC3367746  PMID: 22158736
sexual selection; sound communication; mate choice; burrowing frog; phonotaxis tests
6.  Bat echolocation calls: adaptation and convergent evolution 
Bat echolocation calls provide remarkable examples of ‘good design’ through evolution by natural selection. Theory developed from acoustics and sonar engineering permits a strong predictive basis for understanding echolocation performance. Call features, such as frequency, bandwidth, duration and pulse interval are all related to ecological niche. Recent technological breakthroughs have aided our understanding of adaptive aspects of call design in free-living bats. Stereo videogrammetry, laser scanning of habitat features and acoustic flight path tracking permit reconstruction of the flight paths of echolocating bats relative to obstacles and prey in nature. These methods show that echolocation calls are among the most intense airborne vocalizations produced by animals. Acoustic tracking has clarified how and why bats vary call structure in relation to flight speed. Bats using broadband echolocation calls adjust call design in a range-dependent manner so that nearby obstacles are localized accurately. Recent phylogenetic analyses based on gene sequences show that particular types of echolocation signals have evolved independently in several lineages of bats. Call design is often influenced more by perceptual challenges imposed by the environment than by phylogeny, and provides excellent examples of convergent evolution. Now that whole genome sequences of bats are imminent, understanding the functional genomics of echolocation will become a major challenge.
PMCID: PMC1919403  PMID: 17251105
echolocation; bats; adaptation; convergent evolution
7.  Vocal communication in a complex multi-level society: constrained acoustic structure and flexible call usage in Guinea baboons 
Frontiers in Zoology  2013;10:58.
To understand the evolution of acoustic communication in animals, it is important to distinguish between the structure and the usage of vocal signals, since both aspects are subject to different constraints. In terrestrial mammals, the structure of calls is largely innate, while individuals have a greater ability to actively initiate or withhold calls. In closely related taxa, one would therefore predict a higher flexibility in call usage compared to call structure. In the present study, we investigated the vocal repertoire of free living Guinea baboons (Papio papio) and examined the structure and usage of the animals’ vocal signals. Guinea baboons live in a complex multi-level social organization and exhibit a largely tolerant and affiliative social style, contrary to most other baboon taxa. To classify the vocal repertoire of male and female Guinea baboons, cluster analyses were used and focal observations were conducted to assess the usage of vocal signals in the particular contexts.
In general, the vocal repertoire of Guinea baboons largely corresponded to the vocal repertoire other baboon taxa. The usage of calls, however, differed considerably from other baboon taxa and corresponded with the specific characteristics of the Guinea baboons’ social behaviour. While Guinea baboons showed a diminished usage of contest and display vocalizations (a common pattern observed in chacma baboons), they frequently used vocal signals during affiliative and greeting interactions.
Our study shows that the call structure of primates is largely unaffected by the species’ social system (including grouping patterns and social interactions), while the usage of calls can be more flexibly adjusted, reflecting the quality of social interactions of the individuals. Our results support the view that the primary function of social signals is to regulate social interactions, and therefore the degree of competition and cooperation may be more important to explain variation in call usage than grouping patterns or group size.
PMCID: PMC3849383  PMID: 24059742
Evolution; Vocal communication; Call structure; Call usage; Guinea baboon; Social complexity; Competition
8.  Why do shrews twitter? Communication or simple echo-based orientation 
Biology Letters  2009;5(5):593-596.
Shrews are very vocal animals. We tested behaviourally whether the high-pitched laryngeal ‘twittering’ calls of as-yet unclear function serve for communication or echo-based orientation. We used a representative species from each of the two largest phylogenetic groups of shrews. In both species, experimental manipulation of substrate density, but not of the likelihood of conspecific presence, affected the shrews' call rate when exploring an unknown environment. This adaptation of call rate to the degree of habitat clutter parallels bat echolocation and suggests that shrews may use the echoes and reverberations of their calls for identifying routes through their habitat or for probing habitat type. To assess the acoustic feasibility of shrew echo orientation, we ensonified shrew habitats in the field with an ‘artificial shrew’ (small speaker mounted close to a sensitive microphone). The data showed that shrew-like calls can indeed yield echo scenes useful for habitat assessment at close range, but beyond the range of the shrews' vibrissae.
PMCID: PMC2781971  PMID: 19535367
vocal behaviour; echolocation; communication; habitat acoustics; Sorex; Crocidura
9.  Ultrasonic Communication in Rats: Can Playback of 50-kHz Calls Induce Approach Behavior? 
PLoS ONE  2007;2(12):e1365.
Rats emit distinct types of ultrasonic vocalizations, which differ depending on age, the subject's current state and environmental factors. Since it was shown that 50-kHz calls can serve as indices of the animal's positive subjective state, they have received increasing experimental attention, and have successfully been used to study neurobiological mechanisms of positive affect. However, it is likely that such calls do not only reflect a positive affective state, but that they also serve a communicative purpose. Actually, rats emit the highest rates of 50-kHz calls typically during social interactions, like reproductive behavior, juvenile play and tickling. Furthermore, it was recently shown that rats emit 50-kHz calls after separation from conspecifics. The aim of the present study was to test the communicative value of such 50-kHz calls. In a first experiment, conducted in juvenile rats situated singly on a radial maze apparatus, we showed that 50-kHz calls can induce behavioral activation and approach responses, which were selective to 50-kHz signals, since presentation of 22-kHz calls, considered to be aversive or threat signals, led to behavioral inhibition. In two other experiments, we used either natural 50-kHz calls, which had been previously recorded from other rats, or artificial sine wave stimuli, which were identical to these calls with respect to peak frequency, call length and temporal appearance. These signals were presented to either juvenile (Exp. 2) or adult (Exp. 3) male rats. Our data clearly show that 50-kHz signals can induce approach behavior, an effect, which was more pronounced in juvenile rats and which was not selective to natural calls, especially in adult rats. The recipient rats also emitted some 50-kHz calls in response to call presentation, but this effect was observed only in adult subjects. Together, our data show that 50-kHz calls can serve communicative purposes, namely as a social signal, which increases the likelihood of approach in the recipient conspecific.
PMCID: PMC2137933  PMID: 18159248
10.  The juvenile social environment introduces variation in the choice and expression of sexually selected traits 
Ecology and Evolution  2012;2(5):1036-1047.
The juvenile environment provides numerous cues of the intensity of competition and the availability of mates in the near environment. As research demonstrates that the developing individuals can use these cues to alter their developmental trajectories, and therefore, adult phenotypes, we examined whether social cues available during development can affect the expression and the preference of sexually selected traits. To examine this, we used the Australian black field cricket (Telogryllus commodus), a species where condition at maturity is known to affect both male calling effort and female choice. We mimicked different social environments by rearing juveniles in two different densities crossed with three different calling environments. We demonstrate that the social environment affected female response speed but not preference, and male age-specific calling effort (especially the rate of senescence in calling effort) but not the structural/temporal parameters of calls. These results demonstrate that the social environment can introduce variation in sexually selected traits by modifying the behavioral components of male production and female choice, suggesting that the social environment may be an overlooked source of phenotypic variation. We discuss the plasticity of trait expression and preference in reference to estimations of male quality and the concept of condition dependence.
PMCID: PMC3399168  PMID: 22837847
Adult behavior; age-specific calling effort; condition dependence; developmental plasticity; juvenile environment; social environment
11.  Multimodal signaling in the Small Torrent Frog (Micrixalus saxicola) in a complex acoustic environment 
Behavioral Ecology and Sociobiology  2013;67(9):1449-1456.
Many animals use multimodal (both visual and acoustic) components in courtship signals. The acoustic communication of anuran amphibians can be masked by the presence of environmental background noise, and multimodal displays may enhance receiver detection in complex acoustic environments. In the present study, we measured sound pressure levels of concurrently calling males of the Small Torrent Frog (Micrixalus saxicola) and used acoustic playbacks and an inflatable balloon mimicking a vocal sac to investigate male responses to controlled unimodal (acoustic) and multimodal (acoustic and visual) dynamic stimuli in the frogs’ natural habitat. Our results suggest that abiotic noise of the stream does not constrain signal detection, but males are faced with acoustic interference and masking from conspecific chorus noise. Multimodal stimuli elicited greater response from males and triggered significantly more visual signal responses than unimodal stimuli. We suggest that the vocal sac acts as a visual cue and improves detection and discrimination of acoustic signals by making them more salient to receivers amidst complex biotic background noise.
PMCID: PMC3742427  PMID: 23956486
Anura; Acoustic signal; Background noise; Multimodal communication; Visual cue; Vocal sac
12.  The Effect of Habitat Acoustics on Common Marmoset Vocal Signal Transmission 
American journal of primatology  2013;75(9):904-916.
Noisy acoustic environments present several challenges for the evolution of acoustic communication systems. Among the most significant is the need to limit degradation of spectro-temporal signal structure in order to maintain communicative efficacy. This can be achieved by selecting for several potentially complementary processes. Selection can act on behavioral mechanisms permitting signalers to control the timing and occurrence of signal production to avoid acoustic interference. Likewise, the signal itself may be the target of selection, biasing the evolution of its structure to comprise acoustic features that avoid interference from ambient noise or degrade minimally in the habitat. Here, we address the latter topic for common marmoset (Callithrix jacchus) long-distance contact vocalizations, known as phee calls. Our aim was to test whether this vocalization is specifically adapted for transmission in a species-typical forest habitat, the Atlantic forests of northeastern Brazil. We combined seasonal analyses of ambient habitat acoustics with experiments in which pure tones, clicks, and vocalizations were broadcast and rerecorded at different distances to characterize signal degradation in the habitat. Ambient sound was analyzed from intervals throughout the day and over rainy and dry seasons, showing temporal regularities across varied timescales. Broadcast experiment results indicated that the tone and click stimuli showed the typically inverse relationship between frequency and signaling efficacy. Although marmoset phee calls degraded over distance with marked predictability compared with artificial sounds, they did not otherwise appear to be specially designed for increased transmission efficacy or minimal interference in this habitat. We discuss these data in the context of other similar studies and evidence of potential behavioral mechanisms for avoiding acoustic interference in order to maintain effective vocal communication in common marmosets.
PMCID: PMC3787903  PMID: 23592313
Callithrix jacchus; vocal communication; behavioral ecology; sound broadcasts; sound window
13.  Whispering to the Deaf: Communication by a Frog without External Vocal Sac or Tympanum in Noisy Environments 
PLoS ONE  2011;6(7):e22080.
Atelopus franciscus is a diurnal bufonid frog that lives in South-American tropical rain forests. As in many other frogs, males produce calls to defend their territories and attract females. However, this species is a so-called “earless” frog lacking an external tympanum and is thus anatomically deaf. Moreover, A. franciscus has no external vocal sac and lives in a sound constraining environment along river banks where it competes with other calling frogs. Despite these constraints, male A. franciscus reply acoustically to the calls of conspecifics in the field. To resolve this apparent paradox, we studied the vocal apparatus and middle-ear, analysed signal content of the calls, examined sound and signal content propagation in its natural habitat, and performed playback experiments. We show that A. franciscus males can produce only low intensity calls that propagate a short distance (<8 m) as a result of the lack of an external vocal sac. The species-specific coding of the signal is based on the pulse duration, providing a simple coding that is efficient as it allows discrimination from calls of sympatric frogs. Moreover, the signal is redundant and consequently adapted to noisy environments. As such a coding system can be efficient only at short-range, territory holders established themselves at short distances from each other. Finally, we show that the middle-ear of A. franciscus does not present any particular adaptations to compensate for the lack of an external tympanum, suggesting the existence of extra-tympanic pathways for sound propagation.
PMCID: PMC3135622  PMID: 21779377
14.  Driving Factors for the Evolution of Species-Specific Echolocation Call Design in New World Free-Tailed Bats (Molossidae) 
PLoS ONE  2014;9(1):e85279.
Phylogeny, ecology, and sensorial constraints are thought to be the most important factors influencing echolocation call design in bats. The Molossidae is a diverse bat family with a majority of species restricted to tropical and subtropical regions. Most molossids are specialized to forage for insects in open space, and thus share similar navigational challenges. We use an unprecedented dataset on the echolocation calls of 8 genera and 18 species of New World molossids to explore how habitat, phylogenetic relatedness, body mass, and prey perception contribute to echolocation call design. Our results confirm that, with the exception of the genus Molossops, echolocation calls of these bats show a typical design for open space foraging. Two lines of evidence point to echolocation call structure of molossids reflecting phylogenetic relatedness. First, such structure is significantly more similar within than among genera. Second, except for allometric scaling, such structure is nearly the same in congeneric species. Despite contrasting body masses, 12 of 18 species call within a relatively narrow frequency range of 20 to 35 kHz, a finding that we explain by using a modeling approach whose results suggest this frequency range to be an adaptation optimizing prey perception in open space. To conclude, we argue that the high variability in echolocation call design of molossids is an advanced evolutionary trait allowing the flexible adjustment of echolocation systems to various sensorial challenges, while conserving sender identity for social communication. Unraveling evolutionary drivers for echolocation call design in bats has so far been hampered by the lack of adequate model organisms sharing a phylogenetic origin and facing similar sensorial challenges. We thus believe that knowledge of the echolocation call diversity of New World molossid bats may prove to be landmark to understand the evolution and functionality of species-specific signal design in bats.
PMCID: PMC3891751  PMID: 24454833
15.  Timing matters: sonar call groups facilitate target localization in bats 
To successfully negotiate a cluttered environment, an echolocating bat must control the timing of motor behaviors in response to dynamic sensory information. Here we detail the big brown bat's adaptive temporal control over sonar call production for tracking prey, moving predictably or unpredictably, under different experimental conditions. We studied the adaptive control of vocal-motor behaviors in free-flying big brown bats, Eptesicus fuscus, as they captured tethered and free-flying insects, in open and cluttered environments. We also studied adaptive sonar behavior in bats trained to track moving targets from a resting position. In each of these experiments, bats adjusted the features of their calls to separate target and clutter. Under many task conditions, flying bats produced prominent sonar sound groups identified as clusters of echolocation pulses with relatively stable intervals, surrounded by longer pulse intervals. In experiments where bats tracked approaching targets from a resting position, bats also produced sonar sound groups, and the prevalence of these sonar sound groups increased when motion of the target was unpredictable. We hypothesize that sonar sound groups produced during flight, and the sonar call doublets produced by a bat tracking a target from a resting position, help the animal resolve dynamic target location and represent the echo scene in greater detail. Collectively, our data reveal adaptive temporal control over sonar call production that allows the bat to negotiate a complex and dynamic environment.
PMCID: PMC4026696  PMID: 24860509
echolocation behavior; sonar call timing; active sensing; spatial perception; target tracking
16.  Individual, Contextual, and Age-Related Acoustic Variation in Simakobu (Simias concolor) Loud Calls 
PLoS ONE  2013;8(12):e83131.
Primate loud calls have the potential to encode information about the identity, arousal, age, or physical condition of the caller, even at long distances. In this study, we conducted an analysis of the acoustic features of the loud calls produced by a species of Asian colobine monkey (simakobu, Simias concolor). Adult male simakobu produce loud calls spontaneously and in response to loud sounds and other loud calls, which are audible more than 500 m. Individual differences in calling rates and durations exist, but it is unknown what these differences signal and which other acoustic features vary among individuals. We aimed to describe the structure and usage of calls and to examine acoustic features that vary within and among individuals. We determined the context of 318 loud calls and analyzed 170 loud calls recorded from 10 adult males at an undisturbed site, Pungut, Siberut Island, Indonesia. Most calls (53%) followed the loud call of another male, 31% were spontaneous, and the remaining 16% followed a loud environmental disturbance. The fundamental frequency (F0) decreased while inter-unit intervals (IUI) increased over the course of loud call bouts, possibly indicating caller fatigue. Discriminant function analysis indicated that calls were not well discriminated by context, but spontaneous calls had higher peak frequencies, suggesting a higher level of arousal. Individual calls were distinct and individuals were mainly discriminated by IUI, call duration, and F0. Loud calls of older males had shorter IUI and lower F0, while middle-aged males had the highest peak frequencies. Overall, we found that calls were individually distinct and may provide information about the age, stamina, and arousal of the calling male, and could thus be a way for males and females to assess competitors and mates from long distances.
PMCID: PMC3871870  PMID: 24376651
17.  Limited plasticity in the phenotypic variance-covariance matrix for male advertisement calls in the black field cricket, Teleogryllus commodus 
Journal of evolutionary biology  2013;26(5):1060-1078.
Phenotypic integration and plasticity are central to our understanding of how complex phenotypic traits evolve. Evolutionary change in complex quantitative traits can be predicted using the multivariate breeders’ equation, but such predictions are only accurate if the matrices involved are stable over evolutionary time. Recent work, however, suggests that these matrices are temporally plastic, spatially variable and themselves evolvable. The data available on phenotypic variance-covariance matrix (P) stability is sparse, and largely focused on morphological traits. Here we compared P for the structure of the complex sexual advertisement call of six divergent allopatric populations of the Australian black field cricket, Teleogryllus commodus. We measured a subset of calls from wild-caught crickets from each of the populations and then a second subset after rearing crickets under common-garden conditions for three generations. In a second experiment, crickets from each population were reared in the laboratory on high- and low-nutrient diets and their calls recorded. In both experiments, we estimated P for call traits and used multiple methods to compare them statistically (Flury hierarchy, geometric subspace comparisons and random skewers). Despite considerable variation in means and variances of individual call traits, the structure of P was largely conserved among populations, across generations and between our rearing diets. Our finding that P remains largely stable, among populations and between environmental conditions, suggests that selection has preserved the structure of call traits in order that they can function as an integrated unit.
PMCID: PMC3641675  PMID: 23530814
sexual selection; advertisement call; P matrix; phenotypic plasticity; phenotypic integration; common garden; diet; matrix comparison; field cricket
18.  Divergence of Acoustic Signals in a Widely Distributed Frog: Relevance of Inter-Male Interactions 
PLoS ONE  2014;9(1):e87732.
Divergence of acoustic signals in a geographic scale results from diverse evolutionary forces acting in parallel and affecting directly inter-male vocal interactions among disjunct populations. Pleurodema thaul is a frog having an extensive latitudinal distribution in Chile along which males' advertisement calls exhibit an important variation. Using the playback paradigm we studied the evoked vocal responses of males of three populations of P. thaul in Chile, from northern, central and southern distribution. In each population, males were stimulated with standard synthetic calls having the acoustic structure of local and foreign populations. Males of both northern and central populations displayed strong vocal responses when were confronted with the synthetic call of their own populations, giving weaker responses to the call of the southern population. The southern population gave stronger responses to calls of the northern population than to the local call. Furthermore, males in all populations were stimulated with synthetic calls for which the dominant frequency, pulse rate and modulation depth were varied parametrically. Individuals from the northern and central populations gave lower responses to a synthetic call devoid of amplitude modulation relative to stimuli containing modulation depths between 30–100%, whereas the southern population responded similarly to all stimuli in this series. Geographic variation in the evoked vocal responses of males of P. thaul underlines the importance of inter-male interactions in driving the divergence of the acoustic traits and contributes evidence for a role of intra-sexual selection in the evolution of the sound communication system of this anuran.
PMCID: PMC3905042  PMID: 24489957
19.  Inference of Cross-Level Interaction between Genes and Contextual Factors in a Matched Case-Control Metabolic Syndrome Study: A Bayesian Approach 
PLoS ONE  2013;8(2):e56693.
Genes, environment, and the interaction between them are each known to play an important role in the risk for developing complex diseases such as metabolic syndrome. For environmental factors, most studies focused on the measurements observed at the individual level, and therefore can only consider the gene-environment interaction at the same individual scale. Indeed the group-level (called contextual) environmental variables, such as community factors and the degree of local area development, may modify the genetic effect as well. To examine such cross-level interaction between genes and contextual factors, a flexible statistical model quantifying the variability of the genetic effects across different categories of the contextual variable is in need. With a Bayesian generalized linear mixed-effects model with an unconditional likelihood, we investigate whether the individual genetic effect is modified by the group-level residential environment factor in a matched case-control metabolic syndrome study. Such cross-level interaction is evaluated by examining the heterogeneity in allelic effects under various contextual categories, based on posterior samples from Markov chain Monte Carlo methods. The Bayesian analysis indicates that the effect of rs1801282 on metabolic syndrome development is modified by the contextual environmental factor. That is, even among individuals with the same genetic component of PPARG_Pro12Ala, living in a residential area with low availability of exercise facilities may result in higher risk. The modification of the group-level environment factors on the individual genetic attributes can be essential, and this Bayesian model is able to provide a quantitative assessment for such cross-level interaction. The Bayesian inference based on the full likelihood is flexible with any phenotype, and easy to implement computationally. This model has a wide applicability and may help unravel the complexity in development of complex diseases.
PMCID: PMC3577698  PMID: 23437214
20.  An interdomain sector mediating allostery in Hsp70 molecular chaperones 
The Hsp70 family of molecular chaperones provides a well defined and experimentally powerful model system for understanding allosteric coupling between different protein domains.New extensions to the statistical coupling analysis (SCA) method permit identification of a group of co-evolving amino-acid positions—a sector—in the Hsp70 that is associated with allosteric function.Literature-based and new experimental studies support the notion that the protein sector identified through SCA underlies the allosteric mechanism of Hsp70.This work extends the concept of protein sectors by showing that two non-homologous protein domains can share a single sector when the underlying biological function is defined by the coupled activity of the two domains.
Allostery is a biologically critical property by which distantly positioned functional surfaces on proteins functionally interact. This property remains difficult to elucidate at a mechanistic level (Smock and Gierasch, 2009) because long-range coupling within proteins arises from the cooperative action of groups of amino acids. As a case study, consider the Hsp70 molecular chaperones, a large and diverse family of two-domain allosteric proteins required for cellular viability in nearly every organism (Figure 1) (Mayer and Bukau, 2005). In the ADP-bound state, the two domains act independently, the C-terminal substrate-binding domain displays a stable configuration in which the so-called ‘lid' region is docked against the β-sandwich subdomain, and substrates bind with relatively high affinity (Figure 1A) (Moro et al, 2003; Swain et al, 2007; Bertelsen et al, 2009). Exchange of ADP for ATP in the N-terminal nucleotide-binding domain causes significant local and propagated conformational change, formation of an interface with the substrate-binding domain, opening of the lid subdomain, and a decrease in the binding affinity for substrates (Figure 1B) (Rist et al, 2006; Swain et al, 2007). Upon ATP hydrolysis by the nucleotide-binding domain, Hsp70 is returned to the ADP-bound configuration suitable for another round of substrate binding and release. This process of cyclical substrate binding and release underlies all biological functions of Hsp70 proteins.
What is the structural basis for the long-range functional coupling within Hsp70? When allostery is a conserved property of a protein family, one approach to this problem is to analyze the correlated evolution of amino acids in the family—the expected statistical signature of cooperative action of protein residues (Lockless and Ranganathan, 1999; Kass and Horovitz, 2002; Suel et al, 2003). Previous work using an implementation of this concept (the statistical coupling analysis or SCA) showed that proteins contain sparse networks of co-evolving amino acids termed ‘sectors' that link protein active sites with distinct functional surfaces through the protein core (Halabi et al, 2009). This architecture is consistent with known allosteric mechanisms in protein domains (Suel et al, 2003; Halabi et al, 2009).
However, the principle of co-evolution of protein residues need not be limited to the study of individual protein domains. Indeed, conserved allosteric coupling between two (or more) non-homologous domains implies the existence of shared sectors that span functional sites on different domains. Here, we test this concept by extending the SCA method to consider the allosteric mechanism acting between the two domains of the Hsp70 proteins. Hsp70-like proteins include not only the allosteric Hsp70s, but also the Hsp110s—homologs that contain both domains and are regarded as structural models for Hsp70s, but that do not exhibit allosteric coupling. In this study, we take advantage of the functional divergence between the Hsp70s and Hsp110s to reveal patterns of co-evolution between amino acids that are specifically associated with the allosteric mechanism.
To identify the allosteric sector in Hsp70, we used SCA to compute a weighted correlation matrix, C̃, that describes the co-evolution of every pair of amino-acids positions in a sequence alignment of 926 members of the Hsp70/110 family. We then applied a mathematical method known as singular value decomposition to simultaneously evaluate the pattern of divergence between sequences and the pattern of co-evolution between amino-acid positions. The basic idea is that if the pattern of sequence divergence is able to classify members of a protein family into distinct functional subgroups, then we can rigorously identify the group of co-evolving residues that correspond to the underlying mechanism. Figure 2A shows the principal axis of sequence variation in the Hsp70/110 family, showing a clear separation of the allosteric (Hsp70) and non-allosteric (Hsp110) members of this family. The corresponding axis of co-evolution between amino-acid positions reveals a subset of Hsp70/110 positions (∼20%, 115 residues out of 605 total) that underlie the divergence of Hsp70 and Hsp110 proteins (Figure 2B). These positions derive roughly equally from the nucleotide-binding domain (in blue, 56 positions) and the substrate-binding domain (in green, 59 positions) and are more conserved within the Hsp70 sub-family. These results define a protein sector that is predicted to underlie the allosteric mechanism of Hsp70.
What is the structural arrangement of the putative allosteric sector within the Hsp70 protein? Consistent with a function in allosteric coupling, the 115 sector residues form a physically contiguous network of atoms, linking the ATP-binding site on the nucleotide-binding domain to the substrate recognition site on the substrate-binding domain through the interdomain interface (Figure 2C). The physical connectivity is remarkable given that only ∼20% of overall Hsp70 residues is involved (Figure 2B). Thus, functionally coupled but non-homologous protein domains can share a single sector of co-evolving residues that connects their respective functional sites.
We compared the Hsp70 sector mapping with the large body of biochemical studies that have been carried out in this family. We find strong experimental support for the involvement of sector positions in the Hsp70 allosteric mechanism in several regions: (1) within the ATP-binding site, (2) at the interface linking the two domains, and (3) within the β-sandwich core of the substrate-binding domain. The sector analysis also makes predictions about the involvement of some previously untested residues; we show that mutations at two such sites in fact reduce the allosteric coupling within Hsp70 in vitro and fail to complement a DnaK knockout strain of E. coli in a stress-response assay. Taken together, we conclude that sector positions are associated with the allosteric mechanism of Hsp70.
This work also adds a new finding with regard to the concept of protein sectors. Previous work showed that multiple quasi-independent sectors, each of which contributes a different aspect of function, are possible within a single protein domain (Halabi et al, 2009). This work shows that a single sector can also span two different protein domains when biological function (here, nucleotide-dependent substrate binding) arises from their coupled action. This result emphasizes the point that sectors are units of functional selection and are not obviously related to traditional hierarchies of structural organization in proteins. An interesting possibility is that evolution of allostery between proteins might evolve through the joining of protein sectors, a conjecture that can be tested in future work.
Allosteric coupling between protein domains is fundamental to many cellular processes. For example, Hsp70 molecular chaperones use ATP binding by their actin-like N-terminal ATPase domain to control substrate interactions in their C-terminal substrate-binding domain, a reaction that is critical for protein folding in cells. Here, we generalize the statistical coupling analysis to simultaneously evaluate co-evolution between protein residues and functional divergence between sequences in protein sub-families. Applying this method in the Hsp70/110 protein family, we identify a sparse but structurally contiguous group of co-evolving residues called a ‘sector', which is an attribute of the allosteric Hsp70 sub-family that links the functional sites of the two domains across a specific interdomain interface. Mutagenesis of Escherichia coli DnaK supports the conclusion that this interdomain sector underlies the allosteric coupling in this protein family. The identification of the Hsp70 sector provides a basis for further experiments to understand the mechanism of allostery and introduces the idea that cooperativity between interacting proteins or protein domains can be mediated by shared sectors.
PMCID: PMC2964120  PMID: 20865007
allostery; chaperone; co-evolution; SCA; sector
21.  Echolocation calls and communication calls are controlled differentially in the brainstem of the bat Phyllostomus discolor 
BMC Biology  2005;3:17.
Echolocating bats emit vocalizations that can be classified either as echolocation calls or communication calls. Neural control of both types of calls must govern the same pool of motoneurons responsible for vocalizations. Electrical microstimulation in the periaqueductal gray matter (PAG) elicits both communication and echolocation calls, whereas stimulation of the paralemniscal area (PLA) induces only echolocation calls. In both the PAG and the PLA, the current thresholds for triggering natural vocalizations do not habituate to stimuli and remain low even for long stimulation periods, indicating that these structures have relative direct access to the final common pathway for vocalization. This study intended to clarify whether echolocation calls and communication calls are controlled differentially below the level of the PAG via separate vocal pathways before converging on the motoneurons used in vocalization.
Both structures were probed simultaneously in a single experimental approach. Two stimulation electrodes were chronically implanted within the PAG in order to elicit either echolocation or communication calls. Blockade of the ipsilateral PLA site with iontophoretically application of the glutamate antagonist kynurenic acid did not impede either echolocation or communication calls elicited from the PAG. However, blockade of the contralateral PLA suppresses PAG-elicited echolocation calls but not communication calls. In both cases the blockade was reversible.
The neural control of echolocation and communication calls seems to be differentially organized below the level of the PAG. The PLA is an essential functional unit for echolocation call control before the descending pathways share again the final common pathway for vocalization.
PMCID: PMC1190161  PMID: 16053533
22.  Single-Unit Responses to 22 kHz Ultrasonic Vocalizations in Rat Perirhinal Cortex 
Behavioural brain research  2007;182(2):327-336.
Rats emit ultrasonic vocalizations (USVs) as social signals in several situations. Lesion studies have shown that rat perirhinal cortex (PR), a polymodal sensory region that is reciprocally connected with the amygdala, is critical for normal fear conditioning to so-called “22 kHz USVs”. Here we evaluated single-unit responses in rat PR to 22 kHz USVs and other acoustic stimuli. One question was whether PR circuits are specifically and preferentially tuned, prior to fear conditioning, to respond to USVs and USV-like stimuli. Two 22 kHz USVs were pre-recorded from different conspecifics. Each USV consisted of a “bout” of several discrete calls. Using experimentally-naïve rats, single-unit responses to the USVs were compared with responses to continuous or discontinuous tones that had the same root frequency as the USVs (19 or 22 kHz). The on/off patterns of the discontinuous tones were temporally-matched to the call structure in the corresponding USVs. Compared to continuous tones, the USVs were no more likely to elicit single-unit firing changes in PR. On the other hand, the continuous tones and USVs clearly did elicit different firing patterns in many units. More specifically, the USVs sometimes elicited a transient increase in discharge frequency to each call in a bout of calls. Interestingly, the USVs and the temporally-matched tone segments usually elicited similar firing patterns. The USV-elicited firing pattern in PR thus appears to be controlled by the on/off temporal structure of the calls rather than by the frequency or amplitude modulations associated with each call in a bout of calls.
PMCID: PMC2040343  PMID: 17445914
species-specific behavior; biological preparedness; auditory social signals; alarm calls; rhinal cortex
23.  The role of nocturnal vision in mate choice: females prefer conspicuous males in the European tree frog (Hyla arborea) 
Nocturnal frog species rely extensively on vocalization for reproduction. But recent studies provide evidence for an important, though long overlooked, role of visual communication. In many species, calling males exhibit a conspicuous pulsing vocal sac, a signal bearing visually important dynamic components. Here, we investigate female preference for male vocal sac coloration—a question hitherto unexplored—and male colour pattern in the European tree frog (Hyla arborea). Under nocturnal conditions, we conducted two-choice experiments involving video playbacks of calling males with identical calls and showing various naturally encountered colour signals, differing in their chromatic and brightness components. We adjusted video colours to match the frogs' visual perception, a crucial aspect not considered in previous experiments. Females prefer males with a colourful sac and a pronounced flank stripe. Both signals probably enhance male conspicuousness and facilitate detection and localization by females. This study provides the first experimental evidence of a preference for specific vocal sac spectral properties in a nocturnal anuran species. Vocal sac coloration is based on carotenoids and may convey information about male quality worthwhile for females to assess. The informative content of the flank stripe remains to be demonstrated.
PMCID: PMC2690462  PMID: 19324736
mate choice; coloration; nocturnal vision; multimodal signalling; vocal sac; lateral stripe
24.  Larger Body Size at Metamorphosis Enhances Survival, Growth and Performance of Young Cane Toads (Rhinella marina) 
PLoS ONE  2013;8(7):e70121.
Body size at metamorphosis is a key trait in species (such as many anurans) with biphasic life-histories. Experimental studies have shown that metamorph size is highly plastic, depending upon larval density and environmental conditions (e.g. temperature, food supply, water quality, chemical cues from conspecifics, predators and competitors). To test the hypothesis that this developmental plasticity is adaptive, or to determine if inducing plasticity can be used to control an invasive species, we need to know whether or not a metamorphosing anuran’s body size influences its subsequent viability. For logistical reasons, there are few data on this topic under field conditions. We studied cane toads (Rhinella marina) within their invasive Australian range. Metamorph body size is highly plastic in this species, and our laboratory studies showed that larger metamorphs had better locomotor performance (both on land and in the water), and were more adept at catching and consuming prey. In mark-recapture trials in outdoor enclosures, larger body size enhanced metamorph survival and growth rate under some seasonal conditions. Larger metamorphs maintained their size advantage over smaller siblings for at least a month. Our data support the critical but rarely-tested assumption that all else being equal, larger body size at metamorphosis is likely to enhance an individual’s long term viability. Thus, manipulations to reduce body size at metamorphosis in cane toads may help to reduce the ecological impact of this invasive species.
PMCID: PMC3726449  PMID: 23922930
25.  Divergent Receiver Responses to Components of Multimodal Signals in Two Foot-Flagging Frog Species 
PLoS ONE  2013;8(1):e55367.
Multimodal communication of acoustic and visual signals serves a vital role in the mating system of anuran amphibians. To understand signal evolution and function in multimodal signal design it is critical to test receiver responses to unimodal signal components versus multimodal composite signals. We investigated two anuran species displaying a conspicuous foot-flagging behavior in addition to or in combination with advertisement calls while announcing their signaling sites to conspecifics. To investigate the conspicuousness of the foot-flagging signals, we measured and compared spectral reflectance of foot webbings of Micrixalus saxicola and Staurois parvus using a spectrophotometer. We performed behavioral field experiments using a model frog including an extendable leg combined with acoustic playbacks to test receiver responses to acoustic, visual and combined audio-visual stimuli. Our results indicated that the foot webbings of S. parvus achieved a 13 times higher contrast against their visual background than feet of M. saxicola. The main response to all experimental stimuli in S. parvus was foot flagging, whereas M. saxicola responded primarily with calls but never foot flagged. Together these across-species differences suggest that in S. parvus foot-flagging behavior is applied as a salient and frequently used communicative signal during agonistic behavior, whereas we propose it constitutes an evolutionary nascent state in ritualization of the current fighting behavior in M. saxicola.
PMCID: PMC3558420  PMID: 23383168

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