Male mate preferences in mutual mate choice: finches modulate their songs across and within male-female interactions.
ABSTRACT: Male songbirds use song to advertise their attractiveness as potential mates, and the properties of those songs have a powerful influence on female mate preferences. One idea is that males may exert themselves maximally in each song performance, consistent with female evaluation and formation of mate preferences being the primary contributors to mate choice. Alternatively, males may modulate their song behaviour to different degrees in the presence of different females, consistent with both male and female mate preferences contributing to mutual mate choice. Here we consider whether male Bengalese finches, Lonchura striata domestica, express mate preferences at the level of individual females, and whether those preferences are manifest as changes in song behaviour that are sufficient to influence female mate choice. We tested this idea by recording songs performed by individual unmated males during a series of 1 h interactions with each of many unmated females. Across recording sessions, males systematically varied both the quantity and the quality of the songs that they performed to different females. Males also varied their song properties throughout the course of each interaction, and behavioural tests using female birds revealed that songs performed at the onset of each interaction were significantly more attractive than songs performed by the same male later during the same interaction. This demonstration of context-specific variation in the properties of male reproductive signals and a role for that variation in shaping female mate preference reveals that male mate preferences play an important role in mutual mate choice in this species. Because these birds thrive so well in the laboratory and are so amenable to observation and experimentation across generations, these results yield a new model system that may prove especially advantageous in disentangling the role of male and female mate preferences in shaping mutual mate choice and its long-term benefits or consequences.
Project description:BACKGROUND: Sexual imprinting is important for kin recognition and for promoting outbreeding, and has been a driving force for evolution; however, little is known about sexual imprinting by auditory cues in mammals. Male mice emit song-like ultrasonic vocalizations that possess strain-specific characteristics. OBJECTIVES: In this study, we asked whether female mice imprint and prefer specific characteristics in male songs. METHODS AND FINDINGS: We used the two-choice test to determine the song preference of female C57BL/6 and BALB/c mice. By assessing the time engaged in searching behavior towards songs played back to females, we found that female mice displayed an innate preference for the songs of males from different strains. Moreover, this song preference was regulated by female reproductive status and by male sexual cues such as the pheromone ESP1. Finally, we revealed that this preference was reversed by cross-fostering and disappeared under fatherless conditions, indicating that the behavior was learned by exposure to the father's song. CONCLUSIONS: Our results suggest that female mice can discriminate among male song characteristics and prefer songs of mice from strains that are different from their parents, and that these preferences are based on their early social experiences. This is the first study in mammals to demonstrate that male songs contribute to kin recognition and mate choice by females, thus helping to avoid inbreeding and to facilitate offspring heterozygosity.
Project description:Courtship songs have undergone a spectacular diversification in the Drosophila buzzatii cluster. Accordingly, it has been suggested that sexual selection has played a significant role in promoting rapid diversification, reproductive isolation and speciation. However, there is no direct evidence (i.e., song playback experiments with wingless males) supporting this tenet. Moreover, several studies have showed that the courtship song in the genus Drosophila is not always used in female mate choice decisions, nor plays the same role when it is taken into account. In this vein, we use an approach that combines manipulative and playback experiments to explore the importance and the role of courtship song in female mate choice in four species of the D. buzzatii cluster and one species of the closely related D. martensis cluster for outgroup comparison. We also investigate the importance of courtship song in sexual isolation in sympatry between the only semi-cosmopolitan species, D. buzzatii, and the other species of the D. buzzatii cluster. Our study revealed that the courtship song is used by females of the D. buzzatii cluster as a criterion for male acceptance or influences the speed with which males are chosen. In contrast, we showed that this characteristic is not shared by D. venezolana, the representative species of the D. martensis cluster. We also found that the studied species of the D. buzzatii cluster differ in the role that conspecific and heterospecific songs have in female mate choice and in sexual isolation. Our findings support the hypothesis that divergence in female preferences for courtship songs has played a significant role in promoting rapid diversification and reproductive isolation in the D. buzzatii cluster. However, evidence from D. venezolana suggests that the use of the courtship song in female mate choice is not a conserved feature in the D. buzzatii complex.
Project description:Models of indirect (genetic) benefits sexual selection predict linkage disequilibria between genes that influence male traits and female preferences, owing to non-random mate choice or physical linkage. Such linkage disequilibria can accelerate the evolution of traits and preferences to exaggerated levels. Both theory and recent empirical findings on species recognition suggest that such linkage disequilibria may result from physical linkage or pleiotropy, but very little work has addressed this possibility within the context of sexual selection. We studied the genetic architecture of sexually selected traits by analyzing signals and preferences in an acoustic moth, Achroia grisella, in which males attract females with a train of ultrasound pulses and females prefer loud songs and a fast pulse rhythm. Both male signal characters and female preferences are repeatable and heritable traits. Moreover, female choice is based largely on male song, while males do not appear to provide direct benefits at mating. Thus, some genetic correlation between song and preference traits is expected. We employed a standard crossing design between inbred lines and used AFLP markers to build a linkage map for this species and locate quantitative trait loci (QTL) that influence male song and female preference. Our analyses mostly revealed QTLs of moderate strength that influence various male signal and female receiver traits, but one QTL was found that exerts a major influence on the pulse-pair rate of male song, a critical trait in female attraction. However, we found no evidence of specific co-localization of QTLs influencing male signal and female receiver traits on the same linkage groups. This finding suggests that the sexual selection process would proceed at a modest rate in A. grisella and that evolution toward exaggerated character states may be tempered. We suggest that this equilibrium state may be more the norm than the exception among animal species.
Project description:Sexual interactions play an important role in the evolution of reproductive isolation, with important consequences for speciation. Theoretical studies have focused on the evolution of mate preferences in each sex separately. However, mounting empirical evidence suggests that premating isolation often involves mutual mate choice. Here, using a population genetic model, we investigate how female and male mate choice coevolve under a phenotype matching rule and how this affects reproductive isolation. We show that the evolution of female preferences increases the mating success of males with reciprocal preferences, favouring mutual mate choice. However, the evolution of male preferences weakens indirect selection on female preferences and, with weak genetic drift, the coevolution of female and male mate choice leads to periodic episodes of random mating with increased hybridization (deterministic 'preference cycling' triggered by stochasticity). Thus, counterintuitively, the process of establishing premating isolation proves rather fragile if both male and female mate choice contribute to assortative mating.
Project description:The performance of courtship signals provides information about the behavioural state and quality of the signaller, and females can use such information for social decision-making (e.g. mate choice). However, relatively little is known about the degree to which the perception of and preference for differences in motor performance are shaped by developmental experiences. Furthermore, the neural substrates that development could act upon to influence the processing of performance features remains largely unknown. In songbirds, females use song to identify males and select mates. Moreover, female songbirds are often sensitive to variation in male song performance. Consequently, we investigated how developmental exposure to adult male song affected behavioural and neural responses to song in a small, gregarious songbird, the zebra finch. Zebra finch males modulate their song performance when courting females, and previous work has shown that females prefer the high-performance, female-directed courtship song. However, unlike females allowed to hear and interact with an adult male during development, females reared without developmental song exposure did not demonstrate behavioural preferences for high-performance courtship songs. Additionally, auditory responses to courtship and non-courtship song were altered in adult females raised without developmental song exposure. These data highlight the critical role of developmental auditory experience in shaping the perception and processing of song performance.
Project description:Mutual interactions between sexes have multiple signalling functions. Duet singing in songbirds is related to mutual mate guarding, joint resource defence, and signalling commitment. Coordinated visual displays of mating pairs are thought to perform similar functions, but are less well understood. The current study evaluated mutual interactions in an Estrildid species to explore the relative importance of duet dancing and male singing in mating success of pairs in a first encounter. When Java sparrows (Lonchura oryzivora) court prospective mates, only males sing. However, both males and females perform courtship dances, often in a duet-like manner. These dances are typically terminated by female copulation solicitation displays (CSDs). In the current study, we observed higher mating success when courtship dances were mutually exchanged, and when males sang. However, the sex initiating the courtship did not affect mating success. Most females produced CSDs after duet dancing but before hearing the entire song, indicating that duet dancing played a crucial role in mating. This finding highlights an unexplored aspect of duetting behaviour in the process of mutual mate choice. These results conflict with the majority of past songbird research, which has interpreted songs as primary behavioural sexual signals.
Project description:Female songbirds use male song to discriminate among individuals and evaluate their quality as potential mates. Previous behavioral experiments in many species, including the species studied here, have shown that females will solicit copulation in response to song even if no male is present. Those data demonstrate that female mate choice is closely tied to song features, but they leave open the question of which song parameters are most influential in female mate selection. We sought to identify features of male song that are salient for mate choice in female Bengalese finches. Using a novel experimental approach, we simultaneously tested the possible influence of specific notes or note transitions, the number of different note types in the male's repertoire, the complexity of note content and note sequence, and the stereotypy of note content and note sequence. In additional experiments, we also tested the influence of the pitch and tempo of note production. Our results demonstrate that females generally preferred songs containing increased tempo in the context of species-typical frequency bandwidth, consistent with the idea that females prefer songs that are especially challenging to produce. Female preference for song features that pose a neuromuscular challenge has also been reported in other species. Our data extend those observations into a species that thrives in a laboratory setting and is commonly used in studies of the neural basis of behavior. These results provide an excellent new model system in which to study female preference and the neural mechanisms that underlie signal evaluation and mate choice.
Project description:Abstract Correlative evidence suggests that high problem?solving and foraging abilities in a mate are associated with direct fitness advantages, so it would benefit females to prefer problem?solving males. Recent work has also shown that females of several bird species who directly observe males prefer those that can solve a novel foraging task over those that cannot. In addition to or instead of direct observation of cognitive skills, many species utilize assessment signals when choosing a mate. Here, we test whether females can select a problem?solving male over a non?solving male when presented only with a signal known to be used in mate assessment: song. Using an operant conditioning assay, we compared female zebra finch (Taeniopygia guttata) preference for the songs of males that could quickly solve a novel foraging task to the songs of males that could not solve the task. Females were never housed with the test subject males whose song they heard, and the only information provided about the males was their song. We found that females elicited more songs of problem?solving males than of non?solvers, indicating that song may contain information about a male’s ability to solve a novel foraging task and that naïve females prefer the songs of problem?solving males. Birdsong is known to be an indicator of overall brain function and developmental conditions, but it is unknown whether song can reflect cognitive or personality traits that specifically affect foraging tasks. Here, we tested female preference for song from males who could quickly solve or could not solve an artificial novel foraging task. Although females had no prior knowledge of males, they solicited more song from males who could quickly solve the novel foraging task.
Project description:Male song in birds and mammals is important for repelling rivals, stimulating mates or attracting them to a specific location. Nevertheless, direct experimental evidence for the mate attraction function of male song is limited to a few studies. Here, we provide strong experimental evidence that male songs attract wild female bats (Saccopteryx bilineata). Playbacks of territorial songs reliably elicited phonotaxis in females but not males. Most females captured during playbacks were subadults searching for new colonies to settle in. In S. bilineata, multiple males sing simultaneously at dawn and dusk, thereby creating a conspicuous chorus which encodes information on colony identity and size. Since territorial songs have a large signalling range, male songs constitute acoustic beacons which enable females to localize new colonies. In our playbacks, females strongly preferred local territorial songs over foreign territorial songs from two different locations, indicating that song familiarity influences phonotaxis. Our study provides the first clear experimental evidence that male song elicits female phonotaxis in a non-human mammal. Bats are an especially promising taxon for studying mammalian song since male song has been described in different species with diverse social organisations and natural histories, thus providing exciting opportunities for phylogenetically controlled comparative studies.
Project description:Animals modify acoustic communication signals in response to noise pollution, but consequences of these modifications are unknown. Vocalizations that transmit best in noise may not be those that best signal male quality, leading to potential conflict between selection pressures. For example, slow paced, narrow bandwidth songs transmit better in noise but are less effective in mate choice and competition than fast paced, wide bandwidth songs. We test the hypothesis that noise affects response to song pace and bandwidth in the context of competition using white-crowned sparrows (Zonotrichia leucophrys). We measure male response to song variation along a gradient of ambient noise levels in San Francisco, CA. We find that males discriminate between wide and narrow bandwidth songs but not between slow and fast paced songs. These findings are biologically relevant because songs in noisy areas tend to have narrow bandwidths. Therefore, this song phenotype potentially increases transmission distance in noise, but elicits weaker responses from competitors. Further, we find that males respond more strongly to stimuli in noisier conditions, supporting the 'urban anger' hypothesis. We suggest that noise affects male responsiveness to song, possibly leading to more territorial conflict in urban areas.