Female sexual arousal in amphibians

Rather than being a static, species specific trait, reproductive behavior in female amphibians is variable within an individual during the breeding season when females are capable of reproductive activity. Changes in receptivity coincide with changes in circulating estrogen. Estrogen is highest at the point when females are ready to choose a male and lay eggs. At this time female receptivity (her probability of responding to a male vocal signal) is highest and her selectivity among conspecific calls (measured by her probability of responding to a degraded or otherwise usually unattractive male signal) is lowest. These changes occur even though females retain the ability to discriminate different acoustic characteristics of various conspecific calls. After releasing her eggs, female amphibians quickly become less receptive and more choosy in terms of their responses to male sexual advertisement signals. Male vocal signals stimulate both behavior and estrogen changes in amphibian females making mating more probable. The changes in female reproductive behavior are the same as those generally accepted as indicative of a change in female sexual arousal leading to copulation. They are situationally triggered, gated by interactions with males, and decline with the consummation of sexual reproduction with a chosen male. The changes can be triggered by either internal physiological state or by the presence of stimuli presented by males, and the same stimuli change both behavior and physiological (endocrine) state in such a way as to make acceptance of a male more likely. Thus amphibian females demonstrate many of the same general characteristics of changing female sexual state that in mammals indicate sexual arousal.     

Information content of female copulation calls in yellow baboons.

In a wide variety of animal species, females produce vocalizations just before, during, or immediately after copulation. Observational and experimental evidence indicates that these copulation calls are sexually selected traits, functioning to promote competition between males for access to the calling female. In this paper, we present an acoustic analysis of variation in the form of copulation calls of female yellow baboons, Papio cynocephalus cynocephalus. In particular, we examine whether information about three factors-the calling female's reproductive state, the occurrence or absence of ejaculation, and the dominance rank of the mating male-is encoded in call structure and hence is potentially available to male receivers attending to the signal. Although several features of copulation calls were correlated with each of these factors, when all three were included in multiple regressions only reproductive state and rank of the mating male had independent effects on call form. These findings indicate that female copulation calls in this species signal information about the proximity to ovulation of the calling female and also the relative competitive strength of her mating partner.     

Calling,Courtship, and Condition in the Fall Field Cricket,Gryllus pennsylvanicus

Theoretically, sexual signals should provide honest information about mating benefits and many sexually reproducing species use honest signals when signalling to potential mates. Male crickets produce two types of acoustic mating signals: a long-distance mate attraction call and a short-range courtship call. We tested whether wild-caught fall field cricket (Gryllus pennsylvanicus) males in high condition (high residual mass or large body size) produce higher effort calls (in support of the honest signalling hypothesis). We also tested an alternative hypothesis, whether low condition males produce higher effort calls (in support of the terminal investment hypothesis). Several components of long-distance mate attraction calls honestly reflected male body size, with larger males producing louder mate attraction calls at lower carrier frequencies. Long-distance mate attraction chirp rate dishonestly signalled body size, with small males producing faster chirp rates. Short-range courtship calls dishonestly reflected male residual mass, as chirp rate and pulse rate were best explained by a curvilinear function of residual mass. By producing long-distance mate attraction calls and courtship calls with similar or higher effort compared to high condition males, low condition males (low residual mass or small body size) may increase their effort in current reproductive success at the expense of their future reproductive success, suggesting that not all sexual signals are honest.     

Function of male song in the greater white-lined bat, Saccopteryx bilineata

The use of vocalizations by males to attract mates and defend territories is widespread in birds but uncommon in mammals. In the greater white-lined bat, males defend small territories in tree buttresses and produce complex audible vocalizations. During the day, females roost within these territories, and males with females in their territories have higher reproductive success than males without females. To determine call function, we recorded male vocalizations on the island of Trinidad and made behavioural observations of the focal male and nearby bats at the time the calls were given. Noisy broadband calls were directed mainly at other males whereas tonal calls were used primarily in interactions with females. Two other types of calls were given independently of any observable context and may be involved in territorial defence or conspecific notification. Poisson regression showed that males with song repertoires that contained more unique types of composite syllables had more females in their territories. In addition, several acoustic features of one common call type significantly correlated with the number of females on a territory. Male vocalizations may, therefore, transfer information to colony members about male quality or fighting ability.     

The Structure of Bonobo Copulation Calls During Reproductive and Non‐Reproductive Sex

Copulation calls in primates are usually identified as sexually selected signals that promote the reproductive success of the caller. In this study, we investigated the acoustic structure of copulation calls in bonobos (Pan paniscus), a great ape known for its heightened socio‐sexuality. Throughout their cycles, females engage in sexual relations with both males and other females and produce copulation calls with both partners. We found that calls produced during sexual interactions with male and female partners could not be reliably distinguished in terms of their acoustic structure, despite major differences in mating behaviour and social context. Call structure was equally unaffected by the size of a female’s sexual swelling and by the rank of her mating partner. Rank of the partner did affect call delivery although only with male, but not female partners. The only strong effect on call structure was because of caller identity, suggesting that these signals primarily function to broadcast individual identity during sexual interactions. This primarily social use of an evolved reproductive signal is consistent with a broader trend seen in this species, namely a transition of sexual behaviour to social functions.     

Female Sexual Preferences Toward Conspecific and Hybrid Male Mating Calls in Two Species of Polygynous Deer, <Emphasis Type="Italic">Cervus elaphu</Emphasis>s and <Emphasis Type="Italic">C. nippon</Emphasis>

The behavioral processes at the basis of hybridization and introgression are understudied in terrestrial mammals. We use a unique model to test the role of sexual signals as a reproductive barrier to introgression by investigating behavioral responses to male sexual calls in estrous females of two naturally allopatric but reproductively compatible deer species, red deer and sika deer. Previous studies demonstrated asymmetries in acoustic species discrimination between these species: most but not all female red deer prefer conspecific over sika deer male calls while female sika deer exhibit no preference differences. Here, we extend this examination of acoustic species discrimination to the role of male sexual calls in introgression between parent species and hybrids. Using two-speaker playback experiments, we compared the preference responses of estrous female red and sika deer to male sexual calls from conspecifics versus red × sika hybrids. These playbacks simulate early secondary contact between previously allopatric species after hybridization has occurred. Based on previous conspecific versus heterospecific playbacks, we predicted that most female red deer would prefer conspecific calls while female sika deer would show no difference in their preference behaviors toward conspecific and hybrid calls. However, results show that previous asymmetries did not persist as neither species exhibited more preferences for conspecific over hybrid calls. Thus, vocal behavior is not likely to deter introgression between these species during the early stages of sympatry. On a wider scale, weak discrimination against hybrid sexual signals could substantially contribute to this important evolutionary process in mammals and other taxa.     

Multimodal Signaling in Male and Female Foot-Flagging Frogs Staurois guttatus (Ranidae): An Alerting Function of Calling

In multimodal communication, individuals use several sensory modalities for information transfer. We report on novel observations of foot‐flagging in the Bornean ranid frog Staurois guttatus that is temporally linked to advertisement calling. In addition, we document the first case of foot‐flagging in a female anuran as well as additional visual displays in both males and females including arm‐waving, vocal‐sac pumping and open‐mouth display. In males, advertisement calls and foot‐flags were given throughout most of the day, suggesting that acoustic and visual signals form a multicomponent and multimodal display. We tested the efficacy‐based alerting signal hypothesis of multimodal communication using acoustic playback experiments with males. This hypothesis predicts that an initial signal draws the receiver's attention to the location of a subsequent more informative signal. Several lines of evidence supported the alerting hypothesis. First, the latency between foot‐flags and advertisement calls was significantly higher than that between advertisement calls and foot‐flags, suggesting a functional linkage with calls drawing attention to foot‐flags. Secondly, advertisement calling had a signaling function with males responding significantly more often with both calls and foot‐flags compared with pre‐ and post‐playback control periods. Finally, and most notably, all males tested turned towards the playback stimulus, suggesting that the advertisement call serves to focus their attention on subsequent signals. We discuss the potential of multimodal signaling for conspecific and heterospecific communication and the circumstances under which such a multimodal communication system could evolve.     

The structure and usage of female and male mouse ultrasonic vocalizations reveal only minor differences

Ultrasonic vocalizations (USV) of mice are increasingly recognized as informative dependent variables in studies using mouse models of human diseases. While pup vocalizations primarily serve to re-establish contact with the mother, adult male "songs" were considered to be courtship signals. Alternatively, mouse USVs may generally function as territorial signals. To distinguish between these two hypotheses, we compared the structure and usage of adult male and female USVs in staged resident-intruder encounters. If calls function primarily as courtship signals, males should respond stronger than females, specifically when presented with a female intruder. Refuting this hypothesis, we found that in response to female intruders, females called more than males (228±32 calls/min vs. 71±15 calls/min), and males called more to female than to male intruders (14±7.5 calls/min). There were no significant differences in the acoustic characteristics of the calls given by females and males. To control for the influence of the intruder's behavior on calling, we repeated the experiments using anaesthetized intruders. Again, females produced more calls to female than male intruders (173±17 calls/min vs. 71±15 calls/min), while males called more in response to female than male intruders (39±17 calls/min), and there were no acoustic differences in female and male calls. The vocal activity did not differ significantly with regard to intruder state (awake or anaesthetized), while the acoustic structure exhibited significant differences. Taken together, our findings support the view that calls do not mainly function as courtship signals, although they might serve both a territorial (sex-independent) and a courtship function. The comparison of responses to awake vs. anaesthetized intruders suggests that the latter are sufficient to elicit vocal activity. The subtle acoustic differences, however, indicate that the subject differentiates between intruder states.     

Physiological resonance between mates through calls as possible evidence of empathic processes in songbirds

Physiological resonance – where the physiological state of a subject generates the same state in a perceiver – has been proposed as a proximate mechanism facilitating pro-social behaviours. While mainly described in mammals, state matching in physiology and behaviour could be a phylogenetically shared trait among social vertebrates. Birds show complex social lives and cognitive abilities, and their monogamous pair-bond is a highly coordinated partnership, therefore we hypothesised that birds express state matching between mates. We show that calls of male zebra finches Taeniopygia guttata produced during corticosterone treatment (after oral administration of exogenous corticosterone and during visual separation from the partner) provoke both an increase in corticosterone concentrations and behavioural changes in their female partner compared to control calls (regular calls emitted by the same male during visual separation from the partner only), whereas calls produced during corticosterone treatment by unfamiliar males have no such effect. Irrespective of the caller status (mate/non-mate), calls' acoustic properties were predictive of female corticosterone concentration after playback, but the identity of mate calls was necessary to fully explain female responses. Female responses were unlikely due to a failure of the call-based mate recognition system: in a discrimination task, females perceive calls produced during corticosterone treatment as being more similar to the control calls of the same male than to control calls of other males, even after taking acoustical differences into account. These results constitute the first evidence of physiological resonance solely on acoustic cues in birds, and support the presence of empathic processes.     

Female reproductive state influences the auditory midbrain response

Female behavioral responses to sensory stimuli can be highly variable across the reproductive cycle. Female green treefrogs (Hyla cinerea) use the male vocal signal to locate and choose a mate. Gravid females approach a vocalizing male to mate but do not approach if they have recently mated. Such differences in behavioral response may be due in part to shifts in the neural representation of auditory information in the brain. In this study, we investigated the influence of female reproductive state on neural responses in the auditory midbrain to both communication signals (advertisement calls) and non-communication sounds (band limited noise bursts). Recently mated females exhibited significantly reduced response strengths compared to females not recently mated. Reduced response strengths in post-mated females were in response to both noise bursts and male advertisement calls but were limited to the lower frequency range corresponding to the amphibian papilla of the peripheral auditory system. Our results therefore show that the ability of social signals to stimulate the auditory system differs in females depending on their reproductive state, and that the differential effect on low versus high spectral sensitivities may influence the way the two spectral peaks of male advertisement calls are represented.     

Wake up and smell the conflict: odour signals in female competition

Odour signals used in competitive and aggressive interactions between males are well studied in the context of sexual selection. By contrast, relatively little is known about comparable signals used by females, despite current interest in the evolution of female ornaments and weaponry. Available evidence suggests that odour signals are important in competitive interactions between female mammals, with reductions or reversals of male-biased sexual dimorphism in signalling where female competition is intense. Scent marking is often associated with conflict between females over access to resources or reproductive opportunities. Female scent marks may therefore provide reliable signals of competitive ability that could be used both by competitors and potential mates. Consistent with this hypothesis, we report that aggressive behaviour of female house mice is correlated with the amount of major urinary protein (MUP) excreted in their urine, a polymorphic set of proteins that are used in scent mark signalling. Under semi-natural conditions, females with high MUP output are more likely to produce offspring sired by males that have high reproductive success, and less likely to produce offspring by multiple different sires, suggesting that females with strong MUP signals are monopolized by males of particularly high quality. We conclude that odour signals are worthy of more detailed investigation as mediators of female competition.     

The Acoustic Structure and Information Content of Female Koala Vocal Signals

Determining the information content of animal vocalisations can give valuable insights into the potential functions of vocal signals. The source-filter theory of vocal production allows researchers to examine the information content of mammal vocalisations by linking variation in acoustic features with variation in relevant physical characteristics of the caller. Here I used a source-filter theory approach to classify female koala vocalisations into different call-types, and determine which acoustic features have the potential to convey important information about the caller to other conspecifics. A two-step cluster analysis classified female calls into bellows, snarls and tonal rejection calls. Additional results revealed that female koala vocalisations differed in their potential to provide information about a given caller’s phenotype that may be of importance to receivers. Female snarls did not contain reliable acoustic cues to the caller’s identity and age. In contrast, female bellows and tonal rejection calls were individually distinctive, and the tonal rejection calls of older female koalas had consistently lower mean, minimum and maximum fundamental frequency. In addition, female bellows were significantly shorter in duration and had higher fundamental frequency, formant frequencies, and formant frequency spacing than male bellows. These results indicate that female koala vocalisations have the potential to signal the caller’s identity, age and sex. I go on to discuss the anatomical basis for these findings, and consider the possible functional relevance of signalling this type of information in the koala’s natural habitat.     

Parasite infection has little effect on sexual signals and reproductive behaviour in strawberry poison frogs

Acoustic and visual signals like mating calls or colour patterns, which are involved in courtship displays, can be affected by the health status of an individual. For example, infection with parasites can result in sexual signals that are less intense or conspicuous than in healthy individuals; thus it is generally assumed that sexual signals indicate the quality of the holder. We use strawberry poison frogs from Costa Rica to find out (1) whether there is variation in the parasite load among individuals, (2) whether the parasite load varies over time, (3) whether the parasite load has an effect on acoustic and visual signals, which are supposed to be important for female mate choice and (4) whether the parasite load influences the reproductive behaviour. We found that 60 % of our focal males were infested with an intestinal nematode of the genus Cosmocerca while the parasite load changed considerably over time. We found slight associations between the intensity of acoustic signals (advertisement calls), visual signals (colour and brightness contrasts) and parasite load. Non-infected males produced significantly lower pulse rates than parasitised males. As pulse rate has been shown to decrease with age, we suggest that males without parasites become older than infected males. Moreover, the visual contrasts of the frogs varied across natural backgrounds. An interaction between parasite infection and the background of the calling place affected the ventral colour contrast. This finding suggests that at least some males without parasites defend calling places that render them more conspicuousness to conspecifics than other potential positions would. There were no differences in several elements of reproductive behaviour between parasitised and healthy males. Further studies are necessary to find out whether parasite infection varies among populations, and whether at higher levels it would have a stronger influence on sexual signals, behaviour and lifetime fitness.     

Acoustic and Temporal Variation in Gelada (<Emphasis Type="Italic">Theropithecus gelada</Emphasis>) Loud Calls Advertise Male Quality

Many animals rely on information from vocal signals to assess potential competitors and mates. For example, in primates, males use loud calls to assess rivals when the acoustic properties of the calls reliably indicate the condition or quality of the sender. Here, we investigate whether the loud calls of male geladas (Theropithecus gelada) function as a quality signal. Gelada males produce loud calls during ritualistic chases with rival males. Given the physically taxing nature of these displays, we hypothesize that variation in the acoustic properties of loud calls reliably signal male stamina or competitive ability. To test this hypothesis, we examined whether the acoustic properties of the gelada loud call varied in relation to individual, age, status, and exhaustion. Specifically, we examined 12 call parameters (e.g., fundamental frequency) and 3 bout parameters (e.g., number of calls per bout), that have been previously shown to vary across condition in male primates. We found that several acoustic features varied consistently across age and status such that males deemed higher quality in gelada society (e.g., high status) produced more calls per bout, produced calls that were lower in overall frequency measures, and exhibited a greater vocal range. In addition, we found that similar acoustic features varied with exhaustion; after a long chase event, males produced both fewer calls per bout and calls with higher spectral measures. Results from this study are consistent with the hypothesis that gelada loud calls are quality signals, contributing to the growing evidence that primates may use acoustic information to assess the quality of a rival or a potential mate.     

Size-dependent response to conspecific mating calls by male crickets.

Male sexual displays provide females with information that is crucial to their reproductive decisions. That same information is available to eavesdroppers, with potential consequences for both signaller and receiver. We present empirical evidence for size-dependent responses to intersexual communication by conspecific rivals. Acoustic features of a male house cricket's (Acheta domesticus) mating call are positively associated with its size, with females preferring the calls of larger males. In order to investigate whether conspecific males make use of the information content of mating calls, we examined their phonotactic responses to call recordings that differ in attractiveness to females. Males of all sizes exhibited positive phonotaxis, with smaller males showing a clear preference for female-preferred calls. Smaller males were also less likely to seek contact with the speaker playing their chosen call. We discuss possible explanations for this size-dependent male behaviour.     

Female Barbary macaque (Macaca sylvanus) copulation calls do not reveal the fertile phase but influence mating outcome

In a number of primate species, females utter loud and distinctive calls during mating. Here we aim to clarify the information content and function of Barbary macaque (Macaca sylvanus) copulation calls by testing (i) whether or not copulation calls advertise the female fertile phase and (ii) whether and how copulation calls influence male ejaculatory behaviour. In order to do this, we combined hormone measurements with acoustic analysis and behavioural observations. In contrast to a previous study implying that the structure of copulation calls indicates the timing of the fertile phase, our results, using objective endocrine criteria for assessing ovulation, provide evidence that the structure of copulation calls of female Barbary macaques does not reveal the timing of the fertile phase. More importantly, females seem to influence the likelihood of ejaculation by calling versus remaining silent and by adjusting the timing of call onset. Females make use of this ability to influence mating outcome to ensure ejaculatory matings with almost all males in the group. In addition, calls given during ejaculatory copulations differ from those during non-ejaculatory copulations, providing information about mating outcome for listeners. We conclude that in this species, copulation calls apparently serve to enhance sperm competition and maximize paternity confusion.     

Reproductive state affects reliance on public information in sticklebacks

The degree to which animals use public and private sources of information has important implications for research in both evolutionary ecology and cultural evolution. While researchers are increasingly interested in the factors that lead individuals to vary in the manner in which they use different sources of information, to date little is known about how an animal''s reproductive state might affect its reliance on social learning. Here, we provide experimental evidence that in foraging ninespine sticklebacks (Pungitius pungitius), gravid females increase their reliance on public information generated by feeding demonstrators in choosing the richer of two prey patches than non-reproductive fish, while, in contrast, reproductive males stop using public information. Subsequent experiments revealed reproductive males to be more efficient asocial foragers, less risk-averse and generally less social than both reproductive females and non-reproductives. These findings are suggestive of adaptive switches in reliance on social and asocial sources of information with reproductive condition, and we discuss the differing costs of reproduction and the proximate mechanisms that may underlie these differences in information use. Our findings have important implications for our understanding of adaptive foraging strategies in animals and for understanding the way information diffuses through populations.     

Multimodal Advertisement of Pregnancy in Free-Ranging Female Japanese Macaques (Macaca fuscata)

The role of multiple sexual signals in indicating the timing of female ovulation, and discrimination of this timing by males, has been particularly well studied among primates. However the exhibition of pregnancy signals, and how such signals might modulate male post-conception mating decisions, is still poorly understood. Here we aimed to determine if Japanese macaque males use changes in female sexual signals (behavioral, visual and auditory) to discriminate pregnancy and adjust their socio-sexual behaviors. We combined behavioral observations, digital photography and endocrinological (progestogen and estrogen) data, collected systematically during three one-month periods: the pre-conceptive period, the 1^st month of pregnancy and the 2^nd month of pregnancy. We analyzed variation in the probability of detecting male and female socio-sexual behaviors and estrus calls, as well as changes in female face color parameters, in relation to female reproductive state. Based on our focal observations, we found that males did not copulate during the pregnancy period, and that female socio-sexual behaviors generally decreased from the pre-conceptive to post-conceptive periods. Female face luminance decreased from the pre-conceptive month to the pregnancy period whereas face color only varied between the 1^st and 2^nd month of gestation. Our results suggest that Japanese macaque females display sexual cues of pregnancy that males might use to reduce energy wasted on non-reproductive copulations with pregnant females. We hypothesize that females advertize their pregnancy through changes in behavioral, visual and potential auditory signals that males can use to adjust their mating behaviors. We finish by discussing implications for male and female post-conception strategies.     

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

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

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.