Evolution and Ecology in Widespread Acoustic Signaling Behavior Across Fishes

Abstract

Acoustic signaling by fishes has been recognized for millennia, but is typically regarded as comparatively rare within ray-finned fishes; as such, it has yet to be integrated into broader concepts of vertebrate evolution. We map the most comprehensive data set of volitional sound production of ray-finned fishes (Actinopterygii) yet assembled onto a family level phylogeny of the group, a clade representing more than half of extant vertebrate species. Our choice of family-level rather than species-level analysis allows broad investigation of sonifery within actinopterygians and provides a conservative estimate of the distribution and ancestry of a character that is likely far more widespread than currently known. The results show that families with members exhibiting soniferous behavior contain nearly two-thirds of actinopterygian species, with potentially more than 20,000 species using acoustic communication. Sonic fish families also contain more extant species than those without sounds. Evolutionary analysis shows that sound production is an ancient behavior because it is present in a clade that originating circa 340 Ma, much earlier than any evidence for sound production within tetrapods. Ancestral state reconstruction indicates that sound production is not ancestral for actinopterygians; instead, it independently evolved at least 27 times, compared to six within tetrapods. This likely represents an underestimate for actinopterygians that will change as sonifery is recognized in ever more species of actinopterygians. Several important ecological factors are significantly correlated with sonifery; including physical attributes of the environment, predation by members of other vertebrate clades, and reproductive tactics; further demonstrating the broader importance of sound production in the life history evolution of fishes. These findings offer a new perspective on the role of sound production and acoustic communication during the evolution of Actinopterygii, a clade containing more than 34,000 species of extant vertebrates.

Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior

“…Bony vertebrates include the Sarcopterygii, the vast majority of which are tetrapods, and Actinopterygii, which represent more than half of living vertebrate species, close to 99% of which are teleosts, including toadfishes ( Nelson et al, 2016 ). Teleost families with evidence for soniferous behavior contain nearly two-thirds of actinopterygian species ( Rice et al, 2020 ). Concurrent activation of neurons required for rapid and precise activation of muscle groups underlying acoustic signaling in different lineages of fishes ( Chagnaud et al, 2012 ; Kéver et al, 2020 ) and in tetrapods ( Mead et al, 2017 ; Kwong-Brown et al, 2019 ) might all benefit from gap junction-mediated glycinergic inhibition.…”

Demonstration of subsurface passive acoustic monitoring (SPAM) to survey for and estimate populations of imperiled underwater-calling frogs

“…There is no doubt the list of frogs that call underwater will grow rapidly as biologists adopt and deploy SPAM (see Appendix B for DoD-relevant species known to call underwater). In addition, a growing body of literature is discovering a diversity of taxonomic groups that vocalize underwater, including turtles (Ferrara et al 2017;Ferrara et al 2014;Giles et al 2009) and fish (Rice et al 2020;Rountree, Bolgan, and Juanes 2019;Rountree et al 2006). In this demonstration, we documented nine species of anuran calling underwater on Fort Stewart, seven of which had not previously been reported vocalizing underwater.…”

“…The increases in technological capability (memory size, battery life, and computer processing speed) have led to massive increases in the spatial and temporal scale addressed by acoustic surveys (Clark et al 2011). Although marine mammal surveys have received the bulk of the attention for technological capability, there have been recent advances in applying these same methods to other species groups, such as birds (Celis-Murillo, Deppe, and Allen 2009), fishes (e.g., Rice et al 2020), bats (Stahlschmidt and Brühl 2012), elephants (Wrege et al 2010), and anurans (Willacy, Mahony, and Newell 2015) in terrestrial, freshwater, and marine habitats around the world (Linke et al 2018;Sueur et al 2012;Sugai et al 2018).…”

“…Emerging research is just now highlighting the wide range of taxa that vocalize underwater, from turtles to fish (Giles et al 2009;Linke et al 2018;Mann, Locascio, and Wall 2016;Rice et al 2020). With the rapidly increasing number of species being reviewed for addition to the list of federal TES, the DoD will need to rely on a wide range of survey technologies.…”

Vocal and Electric Fish: Revisiting a Comparison of Two Teleost Models in the Neuroethology of Social Behavior

“…Vocalization is widespread in teleost fishes ( Rice et al, 2020 ), including some species of African electric fish (mormyroids). Our understanding of the neural mechanism underlying fish vocalization comes largely from a single group that includes toadfish and midshipman ( Nelson et al, 2016 ).…”