The African Cichlid Fish Astatotilapia burtoni Uses Acoustic Communication for Reproduction: Sound Production, Hearing, and Behavioral Significance

Sexual reproduction in all animals depends on effective communication between signalers and receivers. Many fish species, especially the African cichlids, are well known for their bright coloration and the importance of visual signaling during courtship and mate choice, but little is known about what role acoustic communication plays during mating and how it contributes to sexual selection in this phenotypically diverse group of vertebrates. Here we examined acoustic communication during reproduction in the social cichlid fish, Astatotilapia burtoni. We characterized the sounds and associated behaviors produced by dominant males during courtship, tested for differences in hearing ability associated with female reproductive state and male social status, and then tested the hypothesis that female mate preference is influenced by male sound production. We show that dominant males produce intentional courtship sounds in close proximity to females, and that sounds are spectrally similar to their hearing abilities. Females were 2–5-fold more sensitive to low frequency sounds in the spectral range of male courtship sounds when they were sexually-receptive compared to during the mouthbrooding parental phase. Hearing thresholds were also negatively correlated with circulating sex-steroid levels in females but positively correlated in males, suggesting a potential role for steroids in reproductive-state auditory plasticity. Behavioral experiments showed that receptive females preferred to affiliate with males that were associated with playback of courtship sounds compared to noise controls, indicating that acoustic information is likely important for female mate choice. These data show for the first time in a Tanganyikan cichlid that acoustic communication is important during reproduction as part of a multimodal signaling repertoire, and that perception of auditory information changes depending on the animal's internal physiological state. Our results highlight the importance of examining non-visual sensory modalities as potential substrates for sexual selection contributing to the incredible phenotypic diversity of African cichlid fishes.所有动物的有性生殖均依赖于信号发送者与接收者之间的有效通信。诸多鱼类，尤其是非洲慈鲷（African cichlids），以其艳丽的体色以及求偶与配偶选择过程中视觉信号的关键作用而广为人知，但学界对该表型多样的脊椎动物类群在交配过程中声学通讯发挥的作用，以及其如何参与性选择，仍知之甚少。本研究以社会性慈鲷鱼类布氏桨鳍丽鱼（Astatotilapia burtoni）为对象，探究其繁殖过程中的声学通讯行为。我们对优势雄性在求偶过程中发出的声音及其伴随行为进行了特征描述，检测了与雌性生殖状态、雄性社会地位相关的听觉能力差异，并验证了“雌性配偶偏好受雄性发声行为影响”这一假说。研究结果表明，优势雄性会在雌性附近主动发出求偶声音，且这些声音的频谱特征与它们的听觉能力相匹配。与口育育幼期相比，处于性接受期的雌性对雄性求偶声音频谱范围内的低频声音的敏感性高出2至5倍。雌性的听觉阈值与循环性类固醇激素水平呈负相关，而雄性则呈正相关，这表明类固醇激素可能在生殖状态相关的听觉可塑性中发挥潜在作用。行为实验结果显示，与噪声对照组相比，性接受期雌性更愿意与播放求偶声音的雄性建立关联，这表明声学信息可能对雌性配偶选择具有重要意义。本研究首次在坦噶尼喀湖慈鲷（Tanganyikan cichlid）中证实，声学通讯作为多模态信号组合的一部分，在繁殖过程中发挥重要作用，且动物对听觉信息的感知会随其内部生理状态而变化。本研究结果凸显了探究非视觉感官模态作为性选择潜在底物的重要性，而这一过程正是造就非洲慈鲷惊人表型多样性的原因之一。