Environmental and morphological constraints interact to drive the evolution of communication signals in frogs

Animals show a rich diversity of signals and displays. Among the many selective forces driving the evolution of communication between individuals, one widely recognized factor is the structure of the environment in which signals are produced, transmitted and received. In particular, animals communicating by sounds often emit acoustic signals from specific locations, such as high up in the air, from the ground or in the water. The properties of these different display sites will impose different constraints on sound production and transmission and may therefore drive signal evolution. Here, we used comparative phylogenetic analyses to assess the relationship between the display site properties and the structure of reproductive calls from 161 frog species from the frog families Ranidae, Leptodactylidae and Hylidae. Specifically, we compared the dominant frequency of species that vocalize from aquatic versus non-aquatic sites, and its relation with body size. We found that the dominant frequency of frogs calling from the water was lower than that of species calling outside of the water, a trend that was consistent across the three families studied. Furthermore, phylogenetic path analysis revealed that the call site had both direct and indirect effects on the dominant frequency. Indirect effects were mediated by call site influencing male body size, which in turn was negatively associated to call dominant frequency. Our results suggest that properties of display sites can drive signal evolution, most likely through morphological constraints, in particular the ones imposed on the sound production mechanism. Also, variation in body size between calling sites explained some of the differences we found in call frequency, highlighting the relevance of the interplay between morphological adaptation and signal evolution. Changes of display site may therefore have important evolutionary consequences, as it may influence sexual selection processes and ultimately may even promote speciation.动物展现出丰富多样的信号与展示行为。在推动个体间通信演化的诸多选择压力中，一项被广泛认可的影响因素是信号产生、传递与接收所处的环境结构。具体而言，依靠声音开展交流的动物，通常会从特定位置发出声学信号，例如高空、地面或水域中。这些不同展示位点的属性会对声音的产生与传递施加差异化限制，进而可能推动信号演化。 本研究采用比较系统发育分析方法，评估了来自蛙科（Ranidae）、细趾蟾科（Leptodactylidae）和雨蛙科（Hylidae）的161个蛙类物种的展示位点属性与繁殖鸣声结构之间的关联。具体来说，我们对比了从水生位点与非水生位点鸣叫的物种的鸣声主频，及其与体型大小的关系。 研究结果显示，从水中鸣叫的蛙类，其鸣声主频低于在水体外鸣叫的物种，这一趋势在上述三个研究蛙科中均保持一致。此外，系统发育路径分析表明，鸣叫位点对鸣声主频同时存在直接与间接影响：间接影响由鸣叫位点通过影响雄性体型大小所介导，而雄性体型大小与鸣声主频呈负相关关系。 我们的研究结果表明，展示位点的属性能够推动信号演化，这一过程大概率通过形态学限制实现，尤其是那些作用于声音产生机制的限制。此外，不同鸣叫位点间的体型差异，解释了本次研究中观测到的鸣声频率差异的部分成因，凸显了形态适应与信号演化之间相互作用的重要性。因此，展示位点的改变可能产生重要的演化后果——其可影响性选择过程，甚至最终推动物种形成。