Acoustical variations in sexually dimorphic features of distance calls in domesticated zebra finches (Taeniopygia guttata castanotis)

Species-specific distance calls (DCs) were recorded from Zebra finches (Taeniopygia guttata castanotis) obtained from three different breeding stocks: Japanese breeders that use Bengalese finches as fostering parents, and Japanese and American breeders that let natural parents rear Zebra finches. These calls were analyzed for five acoustic parameters that were shown to be sexually dimorphic in wild Zebra finches. Male Zebra finches had DCs that were variable among breeding stocks and among individuals. Female DCs recorded from Bengalese-fostered birds were generally longer in duration and higher in pitch than those recorded from Zebra-finch-reared birds, males and females in each breeding stock differed in at least one acoustic parameter, but that parameter was unique in each of the breeding stocks. These results suggest that although sexual dimorphism in Zebra finch DCs has gradually disappeared during the process of domestication, at least one acoustic attribute which allows discrimination between the calls of the sexes has been preserved.     

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.     

Neural function of the mesencephalic dorsomedial nucleus (DM) on distance call production in Bengalese finches

In sexually mature Bengalese finches, acoustic structures of distance calls show sexual difference. The dorsomedial nucleus (DM) of intercollicular complex is known as the midbrain vocal center of distance calls. Neural input from the robust nucleus of archistriatum (RA) was observed in the DM of sexually mature males, but not observed in that of sexually mature females. The purpose of this study is to clarify somo more details of physiological function of the neural system in the DM in distance call production. Electrical stimulation to the DM of both sexes induced a call acoustically similar to distance calls, whose duration depended on the number of the pulses/train of electrical stimulation; electrical stimulation in relatively large (or small) numbers of pulses/train induced calls with relatively long (or short) duration, respectively. Multi-unit spikes were recorded from neurons in the DM. The increment of the frequency of recorded spikos was large when the bird vocalized distance calls, and the number of the frequency decreased when the bird vocalized calls whose duration was shorter than that of distance calls. These results suggest that the neural system in the DM controls duration of distance calls in sexually mature males and females. Electrical stimulation to the DM under different pulse frequencies induced calls with different patterns of time-frequency characteristics. The relation between the pulse frequencies and time-frequency characteristics showed sexual difference. The relation between them in RA-lesioned males was similar to that in females. These results suggest that the neural circuit in the DM of sexually mature males is consisted of sexually common neural circuit controlled by the neural input from the RA, and that these sexually different neural system produce sexually different acoustic structures of distance calls.     

The response of adult orang-utans to flanged male long calls: inferences about their function

Flanged male orang-utans emit loud vocalizations called long calls. In this study, we examined the correlates of variation in long-calling rates among flanged male Sumatran orang-utans, as well as the ranging responses of adult females and flanged males to these long calls. Males that gave calls more often were more likely to approach calls by others. Results bolster a female attraction function of long calls. Flanged males did not significantly avoid or approach long calls. However, males called more when alone than when guarding a female mate, and adult females significantly approached long calls, especially those of the dominant male, and did so regardless of their reproductive state, allowing them to remain within earshot of calling males. The possible selective advantages of this response include avoidance of harassment and infanticide by males. These findings confirm the existence of some form of social organization above the mother-infant unit.     

Testosterone increases singing and aggression but not male-typical sexual partner preference in early estrogen treated female zebra finches

Female zebra finches given estradiol benzoate (EB) as nestlings and testosterone propionate (TP) as adults show masculinized sexual partner preference, preferring females instead of males. This suggests an organizational effect of EB on sexual partner preference in a socially monogamous species that pairs for life. It is not known whether there is an activational hormone effect on sexual partner preference in this species, or whether adult testosterone treatment is necessary for masculinized preference to be expressed. In this experiment females were injected with EB daily for the first 2 weeks posthatching. As adults they were given TP filled or empty implants. Subjects were then given two-choice preference tests with male vs female stimuli, in which singing as well as proximity to the stimuli was recorded, followed by tests in a group aviary for social behavior and pairing preference. Females with TP implants sang more than females with empty implants and were more aggressive toward other females. They did not, however, differ from females with empty implants in any measure of sexual partner preference. Neither group showed a marked preference for males; instead both groups were equally interested in males and females. Thus adult testosterone treatment is not necessary for early estrogen treated females to show a shift in sexual partner preference in the male-typical direction.     

Testosterone decreases the potential for song plasticity in adult male zebra finches

Zebra finches are age-limited learners; males crystallize their songs at 90 days and do not subsequently alter those songs. However, a variety of interventions, including deafening and syringeal denervation, result in long-term changes to the crystallized song. These changes can be prevented by lesioning nucleus LMAN. As different social contexts for song production result in differential activation of LMAN, we asked whether the social context experienced by adult males would affect their ability to alter their songs in response to syringeal denervation. Males able to see and direct their songs to females made fewer changes to their songs than did males that could hear but not see females, but this trend was not significant. The volume of a male's HVc, a forebrain song control nucleus, also failed to predict the degree to which a male would change his song. However, testis mass was significantly correlated with the number of changes made to the song, indicating that variations in testosterone modulate adult song plasticity. We directly tested the effect of circulating testosterone on adult song plasticity by implanting adult males with either testosterone or flutamide, a testosterone receptor blocker, and tracking song changes triggered by ts nerve injury. As predicted, males implanted with testosterone changed their songs less than did males that received flutamide implants. These results suggest that the high testosterone concentrations associated with sexual maturity and song crystallization in zebra finches continue to act in adult males to reduce the potential for vocal plasticity.     

Development in the Usage and Comprehension of Greeting Calls in a Free‐Ranging Group of Japanese Macaques (Macaca fuscata)

The main objective of this study is to clarify the developmental process involved in both the usage of greeting calls and the response to greeting calls by Japanese macaques. These greeting calls facilitate affiliative interactions by communicating benign intent. Specifically, individuals frequently emit greeting calls when interacting with less‐predictable individuals. Here, we examined whether the targets at which greeting calls are directed, along with associated behavioral responses, differed among the age classes, by conducting a cross‐sectional observation of females aged 0–5 yr and their mothers. We found that infant females showed a weak tendency to emit greeting calls at no specific receivers, unlike that by older females. Adult females emitted greeting calls more frequently when approaching unrelated females than related females. In contrast, young adult or juvenile females exhibited no significant difference in the proportion of the calls with related and unrelated conspecifics. Adult and young adult females were more likely to respond affiliatively to other individuals that approached using greeting calls compared with silent approaches, whereas juveniles did not exhibit different responses to the two types of approaches. This study showed that the target‐specific usage and affiliative response to greeting calls emerge with changes in the developmental stage. Furthermore, the fact that even young adults did not use greeting calls as adults indicates that the usage of greeting calls is modified in conjunction with the expansion of social relationships.     

The development of stimulus‐specific auditory responses requires song exposure in male but not female zebra finches

Juvenile male zebra finches develop their song by imitation. Females do not sing but are attracted to males' songs. With functional magnetic resonance imaging and event‐related potentials we tested how early auditory experience shapes responses in the auditory forebrain of the adult bird. Adult male birds kept in isolation over the sensitive period for song learning showed no consistency in auditory responses to conspecific songs, calls, and syllables. Thirty seconds of song playback each day over development, which is sufficient to induce song imitation, was also sufficient to shape stimulus‐specific responses. Strikingly, adult females kept in isolation over development showed responses similar to those of males that were exposed to songs. We suggest that early auditory experience with songs may be required to tune perception toward conspecific songs in males, whereas in females song selectivity develops even without prior exposure to song. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 2010     

Geographic and Temporal Variation of the Male Zebra Finch Distance Call

Temporal and geographic variation of acoustic signals can provide insights into dispersal patterns, population history and speciation. Vocalizations that are transmitted from one generation to the next are of particular value in this respect because they can reveal patterns of gene flow, effectively behaving as population markers. The male zebra finch Taeniopygia guttata distance call is one such vocalization; sons learn their father's distance call in the first 40 d of life and it is individually stereotyped thereafter. We investigated geographic variation in the zebra finch by comparing the structure of distance calls recorded from 61 males from six populations across the continent‐wide range of the Australian subspecies T. g. castanotis. Intra‐population variation was high, in many cases greater than the variation among all males recorded, possibly because of population interchange. However, three of six call variables measured, including the newly discovered modulated element, varied geographically although the pattern of distance call variation did not agree with that of geographic proximity of populations. The proportion of calls with a modulated element increased dramatically over 7 yr in central Australia but there was no change over a similar period of time in south‐eastern Australia where no calls contained the element. The findings suggest that interchange among widely separated populations may be commonplace in Australian zebra finches, with the possible exception of those from south‐eastern Australia.     

Acoustic Properties of Long Calls Given by Flanged Male Orang‐Utans (Pongo pygmaeus wurmbii) Reflect Both Individual Identity and Context

Long calls by flanged male Bornean orang‐utans (Pongo pygmaeus wurmbii) serve as a long‐distance communication signal in this semi‐solitary species and allow individuals to adjust their ranging behavior. Long calls can be heard up to circa 1 km in dense rainforest. Only flanged males emit them, in various contexts: spontaneously (where no disturbances from the environment are perceived by human observers), when highly aroused by another male’s long call or a falling tree nearby, or right after having pushed over a dead tree themselves. In this study, acoustic analyses of orang‐utan long calls at Tuanan in Central Kalimantan not only confirm the discrimination of individual males by their long calls but also demonstrate the discrimination of context based on the long calls’ acoustic structure, which is further supported by the females’ ranging responses according to long call contexts. Females with dependent offspring move away from spontaneous long call sources but appear to ignore long calls elicited by disturbance. Hence, Bornean orang‐utan females perceive measurable differences in acoustic characteristics of long calls given in different contexts. These findings concur with vocal discrimination of contexts in other non‐human primates.     

黄山短尾猴交配叫声及其影响因素

哺乳动物在交配过程中经常会发出独特且有节奏的交配叫声(Copulation call),这通常被认为是雌雄双方交配策略的一种体现.交配叫声的发生及其影响因素在不同物种间差异较大,对其深入研究有助于比较和揭示不同动物交配策略的差异及其适应性功能.为了阐明交配叫声的生物学和社会学因素,我们在安徽黄山记录了野生黄山短尾猴(M...     

Sex differences in the telencephalic song control circuitry in Bengalese finches (Lonchura striata var. domestica)

Bengalese finches, Lonchura striata, are extremely sexually dimorphic in their singing behavior; males sing complex songs, whereas females do not sing at all. This study describes the developmental differentiation of the brain song system in Bengalese finches. Nissl staining was used to measure the volumes of four telencephalic song nuclei: Area X, HVC, the robust nucleus of the arcopallium (RA), and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN). In juveniles (circa 35 days old), Area X and the HVC were well developed in males, while they were absent or not discernable in females. The RA was much larger in males but barely discernable in females. In males, the volumes of Area X and the RA increased further into adulthood, but that of the HVC remained unchanged. The LMAN volume was greater in juveniles than in adults, and there was no difference in the LMAN volume between the sexes. The overall tendency was similar to that described in zebra finches, except for the volume of the RA, where the degree of sexual dimorphism is larger and the timing of differentiation occurs earlier in Bengalese finches. Motor learning of the song continues until day 90 in zebra finches, but up to day 120 in Bengalese finches. Earlier neural differentiation and a longer learning period in Bengalese finches compared with zebra finches may be related to the more elaborate song structures of Bengalese finches.     

Female Iberian midwife toads (Alytes cisternasii) use call order to reach particular males in dense choruses

Call-timing mechanisms among anuran males calling within choruses are frequent, and previous studies have indicated that midwife toad females respond preferentially to these mechanisms. The results of multi-speaker tests performed here with midwife toads suggest that the temporal order of male calls within a dense chorus can determine the ability of females to locate the most attractive calls (in this instance the low-frequency calls emitted by larger males). When call emission was regular in the multi-speaker tests, most females chose the most attractive option (i.e., the speaker emitting the lower-frequency call). When call emission was not regular, however, most females failed to reach the most attractive option, selecting the speaker that emitted immediately after that emitting the most attractive call. These results support the idea that there may be benefits for smaller males that emit their less attractive calls close to those of larger, more attractive males in dense choruses. Less attractive males could exploit the attractiveness of nearby larger males calls by alternating their calls in an unordered sequence to reach receptive females.     

The calling song of the field cricket,Gryllus bimaculatus (de geer): constraints on transmission and its role in intermale competition and female choice

Field studies of calling male field crickets, Gryllus bimaculatus, showed that males formed calling aggregations. Within aggregations males appeared to maintain an exclusive female-attraction zone about their burrows; calling song may thus serve as an aggressive signal to neighbouring males to maintain spacing. Calling song attenuates with distance. Furthermore, calls became degraded with distance by the loss of low frequency components and a reduction in the interval between chirps and pulses due to reverberation. Playback experiments suggested that the predictable degrading properties of the call may serve as a distance-finding mechanism maintaining observed male spacing. The intensity of calls and the repetition rate of chirps and pulses was positively correlated with male size. While information contained within the intensity parameter of calls may prove unreliable due to unpredictable attenuation and irregular amplitude fluctuations, the repetition rate of chirps and pulses was not affected by distance degradation. Playback experiments in which intensity was controlled suggested that females orientate preferentially to the calls of large males.     

Mate recognition by female zebra finch: analysis of individuality in male call and first investigations on female decoding process

Zebra finches are monogamous birds living in large assemblies, which represent a source of confusion for recognition between mates. Because the members of a pair use distance calls to remain in contact, call-based mate recognition is highly probable in this species. Whereas it had been previously demonstrated in males [Vignal, C., Mathevon, N., Mottin, S., 2004. Audience drives male songbird response to mate's voice. Nature 430, 448-451], call-based mate recognition remained to be shown in females. By analysing the acoustic structure of male calls, we investigated the existence of an individual signature and identified the involved acoustic cues. We tested to see if females can identify their mates on the basis of their calls alone, and performed preliminary experiments using modified signals to investigate the acoustic basis of this recognition. Playback tests carried on six individuals showed that a female zebra finch is able to perform the call-based recognition of its mate. Our experiments suggested that the female uses both the energy spectrum and the frequency modulation of the male signal. More experiments are now needed to decipher precisely which acoustic cues are used by females for recognition.     

Behavioral discrimination of sexually dimorphic calls by male zebra finches requires an intact vocal motor pathway

Vocal communication between zebra finches includes the exchange of long calls (LCs) as well as song. By using this natural call behavior and quantifying the LCs emitted in response to playbacks of LCs of other birds, we have previously shown that adult male zebra finches have a categorical preference for the LCs of females over those of males. Female LCs are acoustically simpler than male LCs, which include complex acoustic features that are learned during development. Production of these male-typical features requires an intact nucleus RA, the sexually dimorphic source of the main telencephalic projection to brainstem vocal effectors. We have now made bilateral lesions of RA in 17 adult males and tested their discrimination behavior in the call response situation. Lesioned birds continue to call, but lose the male-typical preference for female LCs. The degree of loss is correlated with the extent of RA damage. Further, the simplified LCs of males with RA lesions have a variable duration that is correlated with stimulus features. In effect, the call response behavior of lesioned males becomes like that of females. Apparently, in the absence of RA, the remaining intact structures receive different call information than RA normally does, and/or process it differently. This suggests that the vocal motor nucleus RA could play a role in the transformation of a signal encoding the salience of stimulus parameters into a control signal that modulates the probability and strength of responding.     

Sex-dependent loss of projection neurons involved in avian song learning.

In zebra finches, only males sing, and the neural regions controlling song exhibit prominent, hormone-induced sex differences in neuron number. In order to understand how sexual differentiation regulates neuron number within one song nucleus, the lateral magnocellular nucleus of the anterior neostriatum (IMAN), we studied the development of sex differences among IMAN neurons that project to the robust nucleus of the archistriatum (RA). The IMAN is implicated in song learning, and previous ontogenetic studies have indicated that males lose over 50% of their IMAN neurons during the juvenile song learning period. Based on developmental changes in both the extent of androgen accumulation within the IMAN and its appearance in Nissl-stained tissue, it had been hypothesized that IMAN neuron loss was even greater in young females, resulting in sex differences in neuron number. However, this hypothesis has not been tested directly because the Nissl-stained boundaries of the IMAN sometimes are ambiguous in young animals, and are not evident at all in adult females. To circumvent these problems, we employed the retrograde tracer fast blue to study the development of IMAN neurons defined on the basis of their projections to the RA. We find that the number of these IMAN-RA projection neurons is much greater in adult males than in females, and that this sex difference develops during the juvenile period of sexual differentiation and song learning because a significant number of these neurons are lost in females but not in males. With respect to sexual differentiation, we conclude that masculinization (which is stimulated by the hormone estradiol) promotes the retention of IMAN-RA projection neurons. In addition, our results indicate that any loss of IMAN neurons that may occur in young males does not include cells projecting to the RA.     

Socially transmitted mate preferences in a monogamous bird: a non-genetic mechanism of sexual selection

There is increasing evidence that animals can acquire mate preferences through the use of public information, notably by observing (and copying) the mate preferences of others in the population. If females acquire preferences through social mechanisms, sexual selection could act very rapidly to spread the preference and drive elaboration of the preferred trait(s). Although there are reports of 'mate-choice copying' in polygynous species, there is no clear evidence for this process in monogamous species. Here, we investigated whether adult female zebra finches Taeniopygia guttata can socially acquire sexual preferences for individual males and, in a separate study, for a generalized trait (coloured leg bands) of males. In both studies, test females observed males in two simultaneous conditions: a ('chosen') mixed-sex situation in which a male was paired with a (model) female, and a ('unchosen') same-sex situation in which a male was paired with another male. In the first experiment, after two weeks of females observing males, test females significantly preferred individual males who had been paired with another female (i.e. chosen males). In the second experiment, test females significantly preferred novel males that were wearing the same leg band colour as the apparently chosen males. Our findings are consistent with the conclusion that female zebra finches' mate preferences are altered by public information. Our study implies that mate preferences can spread rapidly through populations by social mechanisms, affecting the strength of sexual selection in a monogamous species.     

Sex-dependent loss of projection neurons involved in avian song learning

In zebra finches, only males sing, and the neural regions controlling song exhibit prominent, hormone-induced sex diffences in neuron number. In order to understand how sexual differentiation regulates neuron number within one song nucleus, the lateral magnocellular nucleus of the anterior neostriatum (IMAN), we studied the development of sex differences among IMAN neurons that project to the robust nucleus of the archistriatum (RA). The IMAN is implicated in song learning, and previous ontogenetic studies have indicated that males lose over 50% of their IMAN neurons during the juvenile song learning period. Based on developmental changes in both the extent of androgen accumulation within the IMAN and its appearance in Nissl-stained tissue, it had been hypothesized that IMAN neuron loss was even greater in young females, resulting in sex differences in neuron number. However, this hypothesis has not been tested directly because the Nissl-stained boundaries of the IMAN sometimes are ambiguous in young animals, and are not evident at all in adult females. To circumvent these problems, we employed the retrograde tracer fast blue to study the development of IMAN neurons defined on the basis of their projections to the RA. We find that the number of these IMAN-RA projection neurons is much greater in adult males than in females, and that this sex difference develops during the juvenile period of sexual differentiation and song learning because a significant number of these neurons are lost in females but not in males. With respect to sexual differentiation, we conclude that masculinization (which is stimulated by the hormone estradiol) promotes the retention of IMAN-RA projection neurons. In addition, our results indicate that any loss of IMAN neurons that may occur in young males does not include cells projecting to the RA. © 1992 John Wiley & Sons, Inc.     

Mate sampling by female barking treefrogs (Hyla gratiosa)

Despite intense interest in mate choice, relatively little isknown about how individuals sample prospective mates. Indeed,a key issue is whether females sample males or simply matewith the first male encountered. We investigated mate samplingby female barking treefrogs (Hyla gratiosa). Females choosingmates in natural choruses did not move between males but insteadmated with the first male they approached closely. Most femalesmated with the male closest to them at the start of their mate-choiceprocess, and females were more likely to mate with the closest male when the distance to other males was large. These observationsare consistent with the hypothesis that females do not samplepotential mates but instead mate with the first male they distinguishfrom the rest of the chorus. To test this initial detectionhypothesis, we conducted a playback experiment in which weoffered females a choice between two calls, one of which was detectable above the background chorus sound at the female'srelease point, and one of which became detectable only as femalesmoved toward the initially detectable call. Females did notprefer the initially detectable call, thus ruling out the initialdetection hypothesis and implicating sampling of potentialmates by females. Based on the behavior of females in natural choruses, we hypothesize that females approach the chorus, moveto locations where they are able to detect the calls of severalmales simultaneously, and choose a mate from among these malesat some distance from the males. Such simultaneous samplingmay be common in lekking and chorusing species, which havebeen the subjects of many studies of sexual selection.