Acoustic signatures in Mexican cavefish populations inhabiting different caves

PLOS ONE RESEARCH ARTICLE Acoustic signatures in Mexican cavefish populations inhabiting different caves Carole Hyacinthe1,2☯*, Joël Attia3☯*, Elisa Schutz3, Lény Lego3, Didier Casane4,5, Sylvie Rétaux ID1* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Paris-Saclay Institute of Neuroscience, CNRS, Université Paris-Saclay, 91400, Saclay, France, 2 Department of Genetics, Harvard Medical School, Blavatnik Institute, Boston, MA, United States of America, 3 Equipe de Neuro-Ethologie Sensorielle, CRNL, CNRS and Université de St Etienne, SaintÉtienne, France, 4 Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, 91190, Gif-sur-Yvette, France, 5 Université Paris Cité, UFR Sciences du Vivant, 75013, Paris, France ☯ These authors contributed equally to this work. * (CH); (JA); (SR) Abstract OPEN ACCESS Citation: Hyacinthe C, Attia J, Schutz E, Lego L, Casane D, Rétaux S (2023) Acoustic signatures in Mexican cavefish populations inhabiting different caves. PLoS ONE 18(8): e0289574. https://doi.org/ 10.1371/journal.pone.0289574 Editor: Hector Escriva, Laboratoire Arago, FRANCE Received: June 21, 2023 Accepted: July 21, 2023 Published: August 3, 2023 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0289574 Copyright: © 2023 Hyacinthe et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: Work supported by: a Lidex Neuro-Saclay collaborative grant to SR and JA (no website), an Equipe FRM grant (DEQ20150331745) to SR Complex patterns of acoustic communication exist throughout the animal kingdom, including underwater. The river-dwelling and the Pachón cave-adapted morphotypes of the fish Astyanax mexicanus are soniferous and share a repertoire of sounds. Their function and significance is mostly unknown. Here, we explored whether and how sounds produced by blind cavefishes inhabiting different Mexican caves may vary. We compared “Clicks” and “Serial Clicks” produced by cavefish in six different caves distributed in three mountain ranges in Mexico. We also sampled laboratory-bred cavefish lines originating from four of these caves. Sounds were extracted and analyzed using both a manual method and a machine learning-based automation tool developed in-house. Multi-parametric analyses suggest wild cave-specific acoustic signatures, or “accents”. An acoustic code also existed in laboratory cavefish lines, suggesting a genetic basis for the evolution of this trait. The variations in acoustic parameters between caves of origin did not seem related to fish phenotypes, phylogeography or ecological conditions. We propose that the evolution of such acoustic signatures would progressively lead to the differentiation of local accents that may prevent interbreeding and thus contribute to speciation. Introduction Animal communication brings together all the information exchanged between individuals of the same or different species. The emitter produces a signal encoding an information, which causes a change in behavior or physiological state of the recipient [1]. In the aquatic environment, where the speed of sound propagation is approximately four times faster than in the air and travels long distances, mammalian and non-mammalian vertebrates such as teleosts largely rely on acoustic communication. In fishes, acoustic signals are mainly produced by stridulation, swim bladder pulsation, hydrodynamic movement, tendon vibration and air PLOS ONE | https://doi.org/10.1371/journal.pone.0289574 August 3, 2023 1 / 13 PLOS ONE (https://www.frm.org/), an Ecos-Nord exchange Program (M15A03) to SR and Patricia OrnelasGarcia (https://www.univ-spn.fr/ecos-nord/). a Fondation des Treilles prize fellowship to CH (https://www.les-treilles.com/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Acoustic signatures in Mexican cavefish release [2]. They play key roles in basic and complex behaviors such as feeding, reproduction, hierarchy, predator detection, orientation and habitat selection [3–5]. Sonic animals have their own sound repertoires. The underwater soundscape is extraordinarily diverse and representative of species such as the emblematic dolphin’s clicks, baleen’s songs, or toadfish’s boat-whistles. The acoustic repertoire of some species can further be refined to individual signature level. Unlike voice cues that affect all calls of an animal, signature whistles in bottlenose dolphins are distinct whistle types carrying an individual’s identity, as well as motivational, stress or socialization information encoded in their frequency modulation pattern [6]. Likewise, Lusitanian toadfish males demonstrate their quality to females through their calling rate [7]. Acoustic signatures are also species-specific. Their evolution has a suggested role in the speciation process, as proposed in cichlids [8,9] or pipefishes [10]. In the latter, differences in the structure of sound producing apparatus including cranial bone morphology may explain the unique acoustic signatures of the feeding clicks produced by closely related species. Furthermore, within the piranha species Serrasalmus marginatus, red- and yellow-eyed morphs produce sounds with different amplitude features [11]. Genetic or hormonal differences could explain both the sound amplitude and the eye color, playing a role in communication. This is, to our knowledge, a rare case of within-species acoustic signature in fish. Thus, the evolutionary processes of acoustic signatures establishment within groups and in a speciation context remain largely unknown. The teleost Astyanax mexicanus is widely used to investigate evolutionary genetic processes [12] and is a soniferous species [13]. Remarkably, acoustic communication has evolved between Astyanax surface-dwelling and blind cave-adapted morphotypes, which have diverged about 20.000 years ago [14,15]. Astyanax cavefish and surface fish share a repertoire of six sounds, but functionally the trigger, the use, and the meaning of one of these sounds, the “Sharp Click”, has changed between surface fish and cavefish originating from La Cueva de El Pachón [13]. Therefore, acoustic communication seems to have evolved after the colonization of the subterranean habitat. The sound producing mechanisms in Astyanax are no (...truncated)