Abstract :
[en] During evolutionary processes, new capabilities can be acquired following morphological reorganizations from an ancestral form into a new morphotype allowing the entrance in a novel adaptive zone. Once this zone is reached, minor modifications to the morphotype could facilitate diversification through the acquisition of new adaptive behaviours or traits. In this study, we aimed to explore how acoustic communication is related to the evolutionary history and phylogenetic relationships of Holocentridae fish. For this purpose, we used a multidisciplinary approach that combined phylogenetics, comparative morphology, acoustics and ethology.
Conducting our study on a large vocal family was required to achieve our objective. We computed the largest acoustic dataset ever observed in teleosts by recording the hand-held sounds produced by 33 holocentrid species from 73 populations belonging to 5 genera in Guadeloupe, French Polynesia, Guam, Seychelles and Philippines. Furthermore, behavioural studies conducted in the wild and in aquariums were used to assess the ability of Holocentridae to produce different sound types and to determine their contexts of emission. Additionally, we investigated the variations in the morphology of the sound-producing mechanism in 17 species, covering all 9 holocentrid genera.
Our results support that all holocentrid species should be able to produce different types of sound in different social contexts. Besides, contrasting results between wild and experimental observations challenge the traditional view of fish acoustic signals being associated with specific behaviours. Sounds produced by hand-held fish, at night or those emitted towards predators in aquariums are stereotyped, whereas no acoustical stereotypy in sounds has been found during daylight. Acoustical events during this time are composed of one to several sounds of the same or different types, arranged randomly. This suggests that acoustic communication is less constrained during daylight supporting a more flexible, multimodal communication strategy that integrates at least acoustic signals with visual cues. This flexibility could also reflect that different sounds may represent varied emotional or motivational states, a hypothesis that remains open for further exploration.
Our study reveals a clear relationship between the phylogeny and acoustic signals within Holocentridae, though the strength of this relationship varies across taxonomic levels. Sounds serve as effective discriminators at higher levels such as subfamilies and genera. At the species level, differentiation based on sound becomes more complex. In parallel, while the anatomical structures involved in sound production delineate two broad taxonomic categories corresponding to the two subfamilies (Myripristinae and Holocentrinae), variations in the morphology of the sound-producing mechanism at genus and species level are minor. While anatomical traits are quite stable, the variety in acoustic features across Holocentridae indicates a certain versatility in physiological and neurological traits. We hypothesize that the morphological specializations in the sound-producing mechanism might have enabled the exploitation of a new adaptive zone, allowing for the production of distinct sound types. Smaller
acoustical variations observed at lower taxonomic levels in both the Holocentrinae and the Myripristinae likely result from the neurophysiology that governs the functionality of the sound-producing mechanism. This indicates that the diversity of sound types emitted by the holocentrids could result from the differentiated use of a common fundamental mechanism.
Overall, this research suggests an intricate relationship between morphological evolution and acoustic signalling within Holocentridae, demonstrating how modifications of the sound-producing mechanism and neurophysiology can interplay to enable diverse acoustic outputs across various taxonomic levels. By showing that the same basic mechanisms can be utilized differently to produce a spectrum of sounds, our study supports the adaptive versatility of acoustic communication.
