Female presence and estrous state influence mouse ultrasonic courtship vocalizations

The laboratory mouse is an emerging model for context-dependent vocal signaling and reception. Mouse ultrasonic vocalizations are robustly produced in social contexts. In adults, male vocalization during courtship has become a model of interest for signal-receiver interactions. These vocalizations can be grouped into syllable types that are consistently produced by different subspecies and strains of mice. Vocalizations are unique to individuals, vary across development, and depend on social housing conditions. The behavioral significance of different syllable types, including the contexts in which different vocalizations are made and the responses listeners have to different types of vocalizations, is not well understood. We examined the effect of female presence and estrous state on male vocalizations by exploring the use of syllable types and the parameters of syllables during courtship. We also explored correlations between vocalizations and other behaviors. These experimental manipulations produced four main findings: 1) vocalizations varied among males, 2) the production of USVs and an increase in the use of a specific syllable type were temporally related to mounting behavior, 3) the frequency (kHz), bandwidth, and duration of syllables produced by males were influenced by the estrous phase of female partners, and 4) syllable types changed when females were removed. These findings show that mouse ultrasonic courtship vocalizations are sensitive to changes in female phase and presence, further demonstrating the context-sensitivity of these calls.     

Coos,booms, and hoots: The evolution of closed‐mouth vocal behavior in birds

Most birds vocalize with an open beak, but vocalization with a closed beak into an inflating cavity occurs in territorial or courtship displays in disparate species throughout birds. Closed‐mouth vocalizations generate resonance conditions that favor low‐frequency sounds. By contrast, open‐mouth vocalizations cover a wider frequency range. Here we describe closed‐mouth vocalizations of birds from functional and morphological perspectives and assess the distribution of closed‐mouth vocalizations in birds and related outgroups. Ancestral‐state optimizations of body size and vocal behavior indicate that closed‐mouth vocalizations are unlikely to be ancestral in birds and have evolved independently at least 16 times within Aves, predominantly in large‐bodied lineages. Closed‐mouth vocalizations are rare in the small‐bodied passerines. In light of these results and body size trends in nonavian dinosaurs, we suggest that the capacity for closed‐mouth vocalization was present in at least some extinct nonavian dinosaurs. As in birds, this behavior may have been limited to sexually selected vocal displays, and hence would have co‐occurred with open‐mouthed vocalizations.     

DEVELOPMENT OF DISPLAY BEHAVIOR IN YOUNG CAPTIVE BEARDED SEALS

In this study of the ontogeny of vocal behavior in captive bearded seals, Erignathus barbatus , (three males and three females), only males exhibited vocal displays. The onset of display behavior coincided with sexual maturity. Males exhibited three types of dive displays associated with the performance of vocalizations. Vocalizing individuals were frequently attended by another male that maintained passive muzzle contact with the vocalizing male. These interactions were non-aggressive and might play a role in the establishment of a social hierarchy or they might allow the attendee to obtain "near-field" vocal information from the displaying male. Captive males' vocalizations resembled those of males in the wild. However, display dives were shorter, and fewer vocalization types were documented among the captive males compared to bearded seals in the wild. The capacity of the captive males for producing well-formed, long calls with large frequency changes was also significantly less than for wild males. These capacities will likely develop further as the males grow older. Individual capacity for vocal production appears to develop gradually, showing plasticity in form development over time.     

Behavioural responses of male ruffed grouse (Bonasa umbellus,L.) to playbacks of drumming displays

Birds use a variety of sounds in their courtship displays, but the majority of behavioural studies have focused on vocalizations. In contrast, little is known about how non‐vocal sounds, or sonations, are used, even though many avian species produce them. The ruffed grouse (Bonasa umbellus) is a useful species to examine non‐vocal sounds because they lack vocal components in their courtship and rely on a non‐vocal sound to attract mates and defend their territory. Their courtship display, known as “drumming,” is created by the wings, and the number of pulses and speed (pulse rate) varies significantly among males. Anecdotal evidence suggested that males can affect the drumming behaviour of neighbouring males in drumming “duels” in an analogous way to song contests. Here, we test whether males do respond to the playback of drumming sounds of an unfamiliar male. Using a portable speaker system, we played recordings of drumming displays to males that were actively drumming themselves. Throughout each playback, we recorded the drumming behaviour of target males so that we could assess whether drumming activity changes following a playback as well as whether males change the speed of their display. Overall, male grouse were equally likely to approach the speaker or continue drumming following a playback. For those males that continued drumming, their drumming pulse rate was significantly faster following playbacks, but they drummed less often. These results indicate that male ruffed grouse do respond to drumming sounds, but the specific response differs among males. Because the differential response was not related to colour phase or whether a male was drumming in proximity to other males, we suggest that the response of individuals likely varies with other traits, such as hormone levels or behavioural syndrome.     

Defects in Ultrasonic Vocalization of Cadherin-6 Knockout Mice

Background

Although some molecules have been identified as responsible for human language disorders, there is still little information about what molecular mechanisms establish the faculty of human language. Since mice, like songbirds, produce complex ultrasonic vocalizations for intraspecific communication in several social contexts, they can be good mammalian models for studying the molecular basis of human language. Having found that cadherins are involved in the vocal development of the Bengalese finch, a songbird, we expected cadherins to also be involved in mouse vocalizations.

Methodology/Principal Findings

To examine whether similar molecular mechanisms underlie the vocalizations of songbirds and mammals, we categorized behavioral deficits including vocalization in cadherin-6 knockout mice. Comparing the ultrasonic vocalizations of cadherin-6 knockout mice with those of wild-type controls, we found that the peak frequency and variations of syllables were differed between the mutant and wild–type mice in both pup-isolation and adult-courtship contexts. Vocalizations during male-male aggression behavior, in contrast, did not differ between mutant and wild–type mice. Open-field tests revealed differences in locomotors activity in both heterozygote and homozygote animals and no difference in anxiety behavior.

Conclusions/Significance

Our results suggest that cadherin-6 plays essential roles in locomotor activity and ultrasonic vocalization. These findings also support the idea that different species share some of the molecular mechanisms underlying vocal behavior.     

Ultrasonic Reaction of Bank Vole Males to the Presence of Females Varying in Hormonal Activity

Rodents are known to emit ultrasounds during social interactions. Despite the evidence that ultrasonic vocalizations are emitted during sexual encounters and may play a certain role in sexual selection, only a few studies have investigated this phenomenon, mainly in laboratory rodents. We analysed the ultrasonic calls of bank vole (Myodes glareolus) males from an outbred colony in the presence of females differing in hormonal activity. Sexually experienced males were tested during interactions with naive, ovariectomized, pregnant and post‐partum oestrous females. We found that the males’ ultrasound vocalizations depend on the phase of the bank vole females’ reproductive cycle. During encounters with post‐partum oestrous females the males emitted significantly more ultrasounds, and the total duration of ultrasound vocalization was longer. The presence of post‐partum oestrous females also influenced the type of ultrasounds: the most typical constant‐frequency sounds were significantly shorter, and two additional types of ultrasounds were presented during interactions with females ready to mate: U‐shaped frequency‐modulated sounds and frequency‐modulated upsweep sounds. To our knowledge this is the first evidence that male voles of the subfamily Arvicolinae emit different types of ultrasounds in the presence of females depending on their reproductive stage. We suggest that these ultrasounds may be employed as an attractant during reproductive behaviour and that they are potentially an element of sexual selection.     

Underwater vocalizations and associated behavior in captive ringed seals (<Emphasis Type="Italic">Pusa hispida</Emphasis>)

In pinniped species, especially those that mate in the water, acoustic communication is suggested to play an important role in various aspects of behavior. However, little is known about the behavioral context or function of vocalization, principally because direct observation is difficult in the wild. In the present study, we analyzed the seasonality, sexual differences, and behavioral contexts of the vocalizations of captive ringed seals to explore the function of such communication. The behavior of and underwater sounds made by three ringed seals (an adult male, an adult female, and a subadult female) living in Otaru Aquarium, Japan, were recorded for 19 days between August 2011 and April 2012. Six call types (long snort, knock, yelp, bark, click, and woof) were identified in the recordings. The 12 observed social behaviors could be categorized into three categories (male courtship, aggression, and submission). All call types except clicks were vocalized during social behavior. Vocalizations of all types increased during the breeding season. The long snorts were only produced by the adult male toward an adult female during his courtship behavior. All three individuals emitted knocks, yelps, and bark sounds. Of these three call types, knocks were associated with aggressive behavior or the male’s courtship behavior. In contrast, alternate series of yelps and barks were vocalized by the recipients of aggressive behaviors, suggesting their function as submissive signals. This study could be applied to the monitoring of wild ringed seals with passive acoustic recordings to assess not only their distribution but also their behavior.     

High-Pitched Notes during Vocal Contests Signal Genetic Diversity in Ocellated Antbirds

Animals use honest signals to assess the quality of competitors during aggressive interactions. Current theory predicts that honest signals should be costly to produce and thus reveal some aspects of the phenotypic or genetic quality of the sender. In songbirds, research indicates that biomechanical constraints make the production of some acoustic features costly. Furthermore, recent studies have found that vocal features are related to genetic diversity. We linked these two lines of research by evaluating if constrained acoustic features reveal male genetic diversity during aggressive interactions in ocellated antbirds (Phaenostictus mcleannani). We recorded the aggressive vocalizations of radiotagged males at La Selva Biological Station in Costa Rica, and found significant variation in the highest frequency produced among individuals. Moreover, we detected a negative relationship between the frequency of the highest pitched note and vocalization duration, suggesting that high pitched notes might constrain the duration of vocalizations through biomechanical and/or energetic limitations. When we experimentally exposed wild radiotagged males to simulated acoustic challenges, the birds increased the pitch of their vocalization. We also found that individuals with higher genetic diversity (as measured by zygosity across 9 microsatellite loci) produced notes of higher pitch during aggressive interactions. Overall, our results suggest that the ability to produce high pitched notes is an honest indicator of male genetic diversity in male-male aggressive interactions.     

Dynamics of crowing development in the domestic Japanese quail (Coturnix coturnix japonica)

Species-specific behaviours gradually emerge, via incomplete patterns, to the final complete adult form. A classical example is birdsong, a learned behaviour ideally suited for studying the neural and molecular substrates of vocal learning. Young songbirds gradually transform primitive unstructured vocalizations (subsong, akin to human babbling) into complex, stereotyped sequences of syllables that constitute adult song. In comparison with birdsong, territorial and mating calls of vocal non-learner species are thought to exhibit little change during development. We revisited this issue using the crowing behaviour of domestic Japanese quail (Coturnix coturnix japonica). Crowing activity was continuously recorded in young males maintained in social isolation from the age of three weeks to four months. We observed developmental changes in crow structure, both the temporal and the spectral levels. Speed and trajectories of these developmental changes exhibited an unexpected high inter-individual variability. Mechanisms used by quails to transform sounds during ontogeny resemble those described in oscines during the sensorimotor phase of song learning. Studies on vocal non-learners could shed light on the specificity and evolution of vocal learning.     

Context, Structural Variability and Distinctiveness of California Towhee (Pipilo crissalis) Vocal Duets

Avian vocal duets occur when paired birds produce temporally and structurally coordinated vocalizations. Duets are given by members of many species from taxonomically distinct lineages and show great variety in form that often reflects function. By describing the structure of vocal duets we can learn about the diversity of communication signals present in nature and also gain insight into the evolution and operation of those signals. This study quantified the usage patterns and acoustic structure of California towhee duet vocalizations, and tested the distinctiveness of duets among different pairs. California towhee duets consist of a 'squeal' vocalization that is highly unlike the species-typical call note or male advertizement song. California towhees duet an average of three times per hour during the breeding season, and all duets are accompanied by an approach response that brings duetting partners into close spatial proximity. Males and females produce duet contributions with the same syllabic structure. Individual birds produce highly variable squeal vocalizations that are distinctive enough to signal identity. California towhee duet characteristics indicate that the squeal vocalization has evolved separately from other vocal traits in this species and was promoted by natural selection as a duet-specific vocalization. Duet usage patterns and structure suggest that these communication signals function in a cooperative context.     

Development of social vocalizations in mice

Adult mice are highly vocal animals, with both males and females vocalizing in same sex and cross sex social encounters. Mouse pups are also highly vocal, producing isolation vocalizations when they are cold or removed from the nest. This study examined patterns in the development of pup isolation vocalizations, and compared these to adult vocalizations. In three litters of CBA/CaJ mice, we recorded isolation vocalizations at ages postnatal day 5 (p5), p7, p9, p11, and p13. Adult vocalizations were obtained in a variety of social situations. Altogether, 28,384 discrete vocal signals were recorded using high-frequency-sensitive equipment and analyzed for syllable type, spectral and temporal features, and the temporal sequencing within bouts. We found that pups produced all but one of the 11 syllable types recorded from adults. The proportions of syllable types changed developmentally, but even the youngest pups produced complex syllables with frequency-time variations. When all syllable types were pooled together for analysis, changes in the peak frequency or the duration of syllables were small, although significant, from p5 through p13. However, individual syllable types showed different, large patterns of change over development, requiring analysis of each syllable type separately. Most adult syllables were substantially lower in frequency and shorter in duration. As pups aged, the complexity of vocal bouts increased, with a greater tendency to switch between syllable types. Vocal bouts from older animals, p13 and adult, had significantly more sequential structure than those from younger mice. Overall, these results demonstrate substantial changes in social vocalizations with age. Future studies are required to identify whether these changes result from developmental processes affecting the vocal tract or control of vocalization, or from vocal learning. To provide a tool for further research, we developed a MATLAB program that generates bouts of vocalizations that correspond to mice of different ages.     

Role of vocalizations in the reproductive cycle of ring doves (Streptopelia risoria): effects of hypoglossal nerve section on the reproductive behavior and physiology of the female

The role of vocalizations in the reproductive cycle of female ring doves was investigated. Two-stage bilateral hypoglossal nerve section (HNS) was performed on adult females to alter their cooing and they were observed for courtship behavior with the same stimulus males used in preoperation behavioral tests. The HNS females showed a reduction in both the vocalization and wing flipping components of nest-coos but no changes in other female courtship behaviors. In addition, the HNS females failed to show the typical male courtship-induced follicular growth observed in sham-operated females. The behavior of stimulus males did not differ between groups and therefore could not account for the failure of follicular growth in the HNS females. These data suggest that the female's performance of nest-coos, or factors associated with it, may stimulate her own follicular growth.     

Of Mice,Birds, and Men: The Mouse Ultrasonic Song System Has Some Features Similar to Humans and Song-Learning Birds

Humans and song-learning birds communicate acoustically using learned vocalizations. The characteristic features of this social communication behavior include vocal control by forebrain motor areas, a direct cortical projection to brainstem vocal motor neurons, and dependence on auditory feedback to develop and maintain learned vocalizations. These features have so far not been found in closely related primate and avian species that do not learn vocalizations. Male mice produce courtship ultrasonic vocalizations with acoustic features similar to songs of song-learning birds. However, it is assumed that mice lack a forebrain system for vocal modification and that their ultrasonic vocalizations are innate. Here we investigated the mouse song system and discovered that it includes a motor cortex region active during singing, that projects directly to brainstem vocal motor neurons and is necessary for keeping song more stereotyped and on pitch. We also discovered that male mice depend on auditory feedback to maintain some ultrasonic song features, and that sub-strains with differences in their songs can match each other''s pitch when cross-housed under competitive social conditions. We conclude that male mice have some limited vocal modification abilities with at least some neuroanatomical features thought to be unique to humans and song-learning birds. To explain our findings, we propose a continuum hypothesis of vocal learning.     

Cross fostering experiments suggest that mice songs are innate

Background

Vocal learning is a central functional constituent of human speech, and recent studies showing that adult male mice emit ultrasonic sound sequences characterized as “songs” have suggested that the ultrasonic courtship sounds of mice provide a mammalian model of vocal learning.

Objectives

We tested whether mouse songs are learned, by examining the relative role of rearing environment in a cross-fostering experiment.

Methods and Findings

We found that C57BL/6 and BALB/c males emit a clearly different pattern of songs with different frequency and syllable compositions; C57BL/6 males showed a higher peak frequency of syllables, shorter intervals between syllables, and more upward frequency modulations with jumps, whereas BALB/c males produced more “chevron” and “harmonics” syllables. To establish the degree of environmental influences in mouse song development, sons of these two strains were cross-fostered to another strain of parents. Songs were recorded when these cross-fostered pups were fully developed and their songs were compared with those of male mice reared by the genetic parents. The cross-fostered animals sang songs with acoustic characteristics - including syllable interval, peak frequency, and modulation patterns - similar to those of their genetic parents. In addition their song elements retained sequential characteristics similar to those of their genetic parents'' songs.

Conclusion

These results do not support the hypothesis that mouse “song” is learned; we found no evidence for vocal learning of any sort under the conditions of this experiment. Our observation that the strain-specific character of the song profile persisted even after changing the developmental auditory environment suggests that the structure of these courtship sound sequences is under strong genetic control. Thus, the usefulness of mouse “song” as a model of mammalian vocal learning is limited, but mouse song has the potential to be an indispensable model to study genetic mechanisms for vocal patterning and behavioral sequences.     

The relationship between ambient noise and dominant frequency of vocalizations in two species of darters (Percidae: <Emphasis Type="Italic">Etheostoma</Emphasis>)

Acoustic communication is used by many freshwater fishes for both courtship and aggressive interactions. Fish that live in shallow streams with fast moving water are often exposed to high levels of ambient noise, which could have an effect on the characteristics of their vocalizations. This paper investigates the aggressive vocalizations produced by two closely related species of darters. We measured ambient noise in their respective microhabitats, and found that both species produce aggressive drum vocalizations with a dominant frequency that corresponds to areas of low ambient noise. Previous studies have found quiet windows in shallow streams that have correlated to the dominant frequency of sounds made by fish that inhabit the streams. This is the first study, however, to show how the dominant frequencies of vocalizations of two closely related species occur in areas of low ambient noise within their respective microhabitats. This study supports other studies which show that ambient noise along with other physical features of the environment can affect vocal characteristics and behaviors in freshwater fish.     

鸟类鸣声与个体适合度关系的研究进展

鸣声蕴藏着丰富的生物学信息,是鸟类间信息交流最主要的方式之一.本文综述了鸟类鸣声行为与包括个体状态(体征、激素水平和健康状况)、社会等级及繁殖(性选择和成效)在内的个体适合度关系的研究进展.文章总结发现,鸟类的鸣声水平与单一体征参数关系的研究结果不稳定,鸣声可能受个体内部的多种激素调控,并与个体的社会等级有直接关系.雌...     

白腹管鼻蝠成体交流声波多样性

小蝙蝠亚目即通常所说的蝙蝠,是哺乳动物中群居程度最高的类群之一,主要依靠声学信号在黑暗环境中进行交流并维持社群结构,很多蝙蝠种类的交流声波具有极高的多样性,但是目前关于特定种类蝙蝠交流声波的研究还比较缺乏。我们通过录制白腹管鼻蝠(Murina leucogaster)成体的声波,深入研究其交流声波声谱特征,根据交流声波在声谱图上的形状对声波类型进行初步划分,并利用主成分分析(PCA)和判别分析(DFAs)进行验证。结果表明,其交流声波在声谱结构上具有较高多样性,分为16种不同的音节类型,其中包括13种简单音节和3种组合音节,大多数音节都具有多谐波结构。简单音节可分为9种调频音节、2种准恒频音节和2种噪音,组合音节由简单音节无间隔地组合而成。第一谐波最大频率、第一谐波带宽、持续时间为与调频音节类型相关的主要参数。本研究结果为今后进一步开展研究蝙蝠发声行为的行为学意义和声波交流的神经生理学机制方面的研究奠定了基础。     

Sound production during courtship and spawning of Oreochromis mossambicus: male–female and male–male interactions

The role of sound production of the Mozambique tilapia Oreochromis mossambicus in agonistic and mating interactions observed during hierarchy formation and in established groups was examined. Only territorial males produced sounds, during male–female and male–male courtship interactions and during pit-related activities ( e.g. dig, hover and still in the nest). Sound production rate was positively correlated with courting rate. Although sounds in other cichlids are typically emitted in early stages of courtship, O. mossambicus produced sounds in all phases, but especially during late stages of courtship, including spawning. It is suggested that the acoustic emissions in this species may play a role in advertising the presence and spawning readiness of males and in synchronizing gamete release.