Sound production and hearing

Which evolved first – sound production or hearing? When I was young, my aunt, who had founded a finishing school in Oxford for girls from overseas, lamented my poor language skills: “Of course there’s no point in speaking a foreign language unless you have something interesting to say.”1 Dim as I was, I lacked the wits to call out her imperialist mindset. Surely, I later reflected, the virtue in learning a foreign tongue comes from having someone interesting to hear or read in the language.

It seems logical that hearing should have evolved before sound production for signalling and display – which can bring no benefit without an audience. Sensitivity to sound waves probably first functioned for surveillance, to detect predators, competitors or food. All organisms sense the mechanical world around them. Bacteria and yeasts respond to human-audible vibrations, which can stimulate growth and production of metabolites2. Vascular plants respond to acoustic cues from predators and from pollinators3.

A wide diversity of marine invertebrates have cilia with acoustic sensitivity, and many possess mechanisms for sound production4. Amongst terrestrial invertebrates, hairs in the cuticles of spiders respond to airborne sounds; the antennae of male mosquitoes are sensitive to the tone of female wingbeats; many Orthoptera and Hemiptera have tympanal membranes, which for cicadas allow synchronisation of their loud stridulations5.

All vertebrate skulls possess fluid-filled canals with hair-cell patches that detect acceleration and, in most species, particle motion or sound pressure. More specialised hearing organs – ears – probably evolved after the first vertebrates had begun to communicate acoustically by using lungs to produce simple grunts and clicks shaped by the mouth6. The tympanic middle ear characteristic of almost all modern tetrapods likely first appeared during the Triassic Period7. The cartilaginous external ear characteristic only of mammals evolved from a repurposing of gill tissues, which may itself have had invertebrate origins8.

The mutual action of information broadcast and detection has propagated through geological time in continuously evolving mechanisms of communication, and specifically for humans, through cultural revolutions in rapidly developing communication networks. Sound production creates opportunities – the explosive clicks of a snapping shrimp stun competitors and prey, the melodious song of a male blackbird attracts receptive females – but it also carries risks in self-advertisement to potential predators. Although listening risks nothing, neither does it actively benefit anyone.

My aunt wins the moral high ground, then, gifted teacher that she was: her words in any language, and always with a delightfully cultivated accent, stimulated conversation. She relished any exchange of interesting intelligence, and most of all, as I remember, at dinner parties around her banquet table. Conversation eddied and swirled across the table, while I prised lead shot from the blood-clotted meat of my roast pheasant. Contributor and conveyor merged in the festival of chatter. Information burned on a pyre of gossip, and from the ashes rose a living narrative, borne aloft on hot winds of pleasure by wings formed of bigger pinions.

• My aunt was born at the zenith of the British Empire in 1918, when it covered one-quarter of Earth's total land area; her grandfather had been a Major-General in the British East India Company. She devoted her life to European cultural integration. She liked to declare her aphorism at social gatherings, and as it happened in the hearing of the person who would go on to write her obituary, repeating it there for the benefit of all Daily Telegraph readers – another reason for not speaking unless you are sure of the message you are communicating.
• Indian classical music enhances growth and metabolite production in various bacteria and yeasts (Sarvaiya, N. & Kothari, V. 2015 Microbiology). Some biotic responses may amount to no more than physical reactions. For example, acoustic fields cause bacteria in aqueous suspension to cluster together, just as they cluster inert particles in Brownian motion (Gutiérez-Ramos, S. et al. 2018 Scientific Reports). The bacterium Escherichia coli, however, changes its swimming behaviour when played Nikolai Rimsky-Korsakov’s Flight of the Bumblebee, increasing motility at higher sound frequencies and tempos (Ku, H.-N. et al. 2020 Applied Acoustics).
• The thale cress Arabidopsis thaliana primes its defences in response to high-amplitude vibrations produced by feeding caterpillars; the evening-primrose Oenothera drummondii produces sweeter nectar when exposed to the sound of bee wingbeats (Karban, R. 2021 Annual Review of Ecology, Evolution, and Systematics).
• Solé, M. et al. (2023) Marine invertebrates and noise. Frontiers in Marine Science.
• Römer, H. & Tautz, J. (1992) Invertebrate auditory receptors. In: Ito, F. (ed.) Comparative Aspects of mechanoreceptor Systems. Springer Nature.
• For modern choanate vertebrates – having lungs and internal nostrils – sound-production capability is widespread across all branches of the evolutionary tree reaching back to their last common ancestor, which lived some 407 million years ago (Jorgewich-Cohen, G. et al. 2022 Nature Communications). Sound production by that ancestal lungfish will have long pre-dated possession of well-developed ears.
• Sobral, G. & Müller, J. (2016) Archosaurs and their kin: the ruling reptiles. In: Clack, J. et al. (eds) Evolution of the Vertebrate Ear. Springer Nature.
• Thiruppathy, M. et al. (2025) Repurposing of a gill gene regulatory program for outer-ear evolution. Nature.

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