In soldierfish and squirrelfish, evolution diversifies sounds without reinventing the instrument

Does every new sound require a new apparatus? In the Holocentridae, the answer is no. These reef-dwelling fish first developed a common anatomical structure, then learnt to use it in different ways - much like musicians each playing their own rhythm on the same drum. This is demonstrated by an international study led by researchers from the Laboratory of Functional and Evolutionary Morphology at the University of Liège.

Fish produce sounds in many situations: defending their territory, encountering a predator, social interactions or interactions with other species. Many sound-production mechanisms have already been described, but little was yet known about how these systems have changed and diversified over the course of evolution. Comparative studies have most often focused on a small number of closely related species, providing isolated pieces of a jigsaw puzzle without allowing a complete evolutionary history to be pieced together.

The Holocentridae provide a case study well suited to this question. This family of mainly nocturnal reef fish comprises two subfamilies, the soldierfish (Myripristinae) and the squirrelfish (Holocentrinae), which exhibit marked differences in their sound-producing apparatus, their sounds and their hearing abilities. All produce sounds using fast-twitch muscles connected to the skeleton and the swim bladder.

“We compared, on a single evolutionary tree, the morphology of the sound-producing apparatus, the characteristics of the sounds and the phylogenetic relationships between species,” explains Marine Banse, a researcher at the Laboratory of Functional and Evolutionary Morphology at ULiège. “Our work is based on genetic data covering 53 species, on the anatomical analysis of the sound-producing apparatus in 17 species, and on a vast set of acoustic data. In total, 388 fish from 73 populations and belonging to 33 species were individually recorded, yielding a total of over 7,500 sounds!”

This comparison reveals a three-stage scenario. It suggests an evolutionary scenario in three stages. A structure combining the swim bladder, specialised muscles and the first ribs would first have developed in the common ancestor. It would then have diversified following the separation of the two subfamilies. In soldierfish, the swim bladder has developed two anterior extensions that bring it into extensive contact with the rear of the skull. In squirrelfish, it has remained simpler and is still separate from the skull in most genera. Finally, within each lineage, species continue to diversify their sounds whilst the mechanism remains broadly conserved, notably by varying the number and rhythm of sound pulses, differences that likely relate to neuromuscular control rather than anatomy.

“In other words, evolution did not create a new instrument for every new signal; it first established different architectures, then diversified the way they function,” explains Éric Parmentier, director of the laboratory. “The sounds make it possible to distinguish between the major lineages and most of the species studied, but their characteristics overlap more between closely related species. A fish’s sound is therefore not necessarily a ‘unique identifier’ specific to a species, but it nevertheless retains information about the lineage, the production mechanism and its neural control.”

This work forms part of Marine Banse’s PhD thesis and a research project funded by the FNRS. It was based on field campaigns of an unusual scale, carried out in Guadeloupe, the Seychelles, the Philippines, Guam and French Polynesia. As Holocentridae are primarily nocturnal, the fish were caught by swimming or diving after dark, with each individual then recorded as quickly as possible. Additional recordings were made at the Okinawa Churaumi Aquarium in Japan for species that usually live at depth and are very difficult to observe in their natural habitat.

“By linking anatomy, acoustics and phylogeny, this study illustrates one way in which evolution can generate diversity,” concludes the young researcher. “A morphological innovation establishes the conditions for sound production, and the diversification of signals then occurs primarily through changes in the use and control of an architecture that is already in place. This mode of evolution, in which the same structure is reused in different ways, could be found in other vocal fish.”