What the Lungfish Heard: Clues to the ear’s evolution

November 9, 2010

African lungfish (credit: Christian Brandt)

For life on Earth, the successful transition from sea to land demanded adaptation: notably, legs (or at least the loss of flippers) and air-breathing lungs. It also put selective pressure on the ears. Sound propagates differently through air than it does through water, and it takes a certain kind of ear to detect it. That ear — the tympanic ear, featuring a membrane (or “eardrum”) that receives airborne vibrations and relays them to the bones of the inner ear — began to appear in four-legged vertebrates, or tetrapods, a little over 200 million years ago. Yet the tetrapods themselves had existed on land for more than 100 million years before that, ever since their divergence from lobe-finned fish. A hundred million years is a long time to go without a tympanum. What, if anything, could those earliest tetrapods hear?

A recent study offers a quiet answer. A team of Swedish biologists tested the hearing abilities of the West African lungfish, the closest living relative of tetrapods; the lungfish has an inner ear more like a tetrapod’s than a ray-finned fish’s, so presumably it’s a good stand-in for the earliest land-dwellers. The experiment was straightforward. The scientists put the lungfish in a water-filled tank and monitored the response of its auditory brainstem as the animal listened to clicks played through two hydrophones. Then the lungfish was put in a small, wet sandbox, and the scientists monitored again as the animal listened to airborne sounds emitted by a nearby loudspeaker.

Fishes have a couple of ways of sensing sound underwater. All can detect the motions of particles in the water that are triggered when sound waves pass through the medium; they detect these motions with specialized cells on the otolith, a dense, calcium-carbonate structure in the inner ear, or (at close range) with similar cells along the sides of the body. Some fish — notably the ray-finned fish — can also detect acoustic pressure waves. Basically, they have ears that are plugged into their swim bladders. The volume of the bladder, which is filled with air, varies with changes in pressure; those signals are sent to the otolith and are registered by the brain as sound. Fishes with this ability are known as hearing specialists, because they can hear sounds at higher frequencies, above 200 Hz.

The Swedish experiment was designed to ask whether the lungfish is a hearing specialist. It lacks a swim bladder, but maybe its lungs can serve similarly — as a “pressure-to-particle transducer” — to detect sound pressure underwater. And if the lungs detect sound pressure underwater, maybe they work above water too. That would make a certain sense, and would tell a neat evolutionary story: The first tetrapods didn’t have a tympanum, but maybe their predecessors, the tetrapodomorphs — the first fishes out of water, akin to the lungfish — came ashore already wired to register airborne sounds, via their lungs.

Alas, that story doesn’t quite pan out. The Swedish experiment found that lungfish hearing is based on the detection of particle motion, not pressure; the animal can hear underwater (no surprise there) but is largely insensitive to airborne sound. That means one of two things, the authors conclude: either the early lungfish (and, by extension, the early tetrapods) had a better inner ear, which has degraded in the epochs since; or the modern lungfish’s ear is similar to the ears of the first tetrapods, in which case they were all pretty much deaf to the wind. The latter seems more likely. The researchers did find that the lungfish can register some low-frequency sounds, both in and out of water, through the physical vibration of its skull, much as certain frogs do today. Small solace for our four-legged ancestors: For the first 100 million years, it seems, all they could hear was the rattling of bones.

Christensen-Dalsgaard, J., Brandt, C., Wilson, M., Wahlberg, M., & Madsen, P. (2010). Hearing in the African lungfish (Protopterus annectens): pre-adaptation to pressure hearing in tetrapods? Biology Letters DOI: 10.1098/rsbl.2010.0636

Note: This post is a proud entrant in the the ScienceOnline 2011 Travel Award Contest sponsored by NESCent, the National Evolutionary Synthesis Center.

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