Ancient fish with human-like hearing stuns scientists

Two-thirds of freshwater species today rely on a specialized middle ear known as the Weberian apparatus. This group spans more than 10,000 species, from catfish to aquarium favorites such as tetras and zebrafish. The Weberian system lets them detect much higher sound frequencies than most ocean fish, reaching a range close to human hearing.

University of California, Berkeley paleontologist Juan Liu examined the Weberian apparatus in a newly described fossil fish and used its anatomy to update the timeline for how freshwater fish evolved.

Fossil evidence revises the timeline

Otophysan fish, which possess a Weberian ear system, were long believed to have entered fresh water roughly 180 million years ago, before Pangea split into the continents we recognize today. Liu's work points to a later origin, about 154 million years ago in the late Jurassic Period, after Pangea had begun to break apart and as modern oceans were taking shape.

Analyses of fossils and genomic data indicate that precursors of the enhanced hearing bones first appeared while these fish still lived in the sea. Fully refined, sensitive hearing evolved after two separate lineages colonized fresh water: one that led to catfish, knife fish, and African and South American tetras, and another that produced carp, suckers, minnows, and zebrafish, the largest order of freshwater fish.

"The marine environment is the cradle of a lot of vertebrates," said Liu, an assistant adjunct professor of integrative biology and an assistant curator in the UC Museum of Paleontology. "A long time consensus was that these bony fish had a single freshwater origin in the large continent Pangea and then dispersed with the separation of different continents. My team's analysis of some fantastic fossils that shed new light on the evolutionary history of freshwater fish and found completely different results: the most recent common ancestor of otophysan fish was a marine lineage and there were at least two freshwater incursions after that lineage split up."

This reinterpretation reshapes how scientists view both the evolutionary history and the complex biogeography of this remarkably successful freshwater group, she added. "These repeated incursions into freshwater at the early divergence stage likely accelerated speciation, and are key factors in explaining the extraordinary hyper-diversity of otophysans in modern freshwater faunas."

Liu and her colleagues describe and name the 67 million-year-old fossil fish, Acronichthys maccagnoi, in a paper published on October 2 in the journal Science. In that paper, the researchers analyze 3D scans of the fossil's Weberian structure and the genomes and morphology of modern fish to revise the genealogy of freshwater fish, and also simulate the frequency response of the fossil fish's middle ear structure.

How underwater hearing works

Hearing in water relies on different structures than hearing in air. Many land vertebrates detect sound with an eardrum that vibrates and drives a chain of middle ear bones that amplify the signal before it reaches the fluid-filled inner ear; in humans these bones are the malleus, incus, and stapes.

Because a fish's body is close in density to water, sound waves pass through it. Many fish therefore evolved an internal air bladder that vibrates with passing sounds. In most saltwater species, vibrations reach the inner ear only weakly, which limits hearing to low frequencies below about 200 Hertz.

Otophysan fish improved this pathway by adding small bony "ossicles" that connect the air bladder, often mistakenly called the swim bladder, to the inner ear. This linkage boosts and broadens hearing sensitivity. Zebrafish, for instance, can detect sounds up to 15,000 Hz, approaching the 20,000 Hz upper limit in humans.

Why high-frequency hearing is useful remains an open question. It may reflect the variety of habitats these fish occupy, from fast streams to still lakes.

Liu studies the Weberian apparatus in living and fossil fish, and last year published a computational simulation of how the apparatus works. That simulation allows her to predict the frequency response of the bony ossicles, and thus the hearing sensitivity of fish.

A tiny Alberta fossil with outsized insight

Numerous specimens of the newly named fossil fish, a mere 2 inches long, were excavated and collected in Alberta, Canada, over six field seasons starting in 2009 by ichthyologist and co-author Michael Newbrey of Columbus State University in Georgia. The fossils are housed in the Royal Tyrrell Museum in Drumheller, Alberta. A couple of specimens were so well preserved that the bones in the middle ear were clearly Weberian. The fish is the oldest known North American fossil of an otophysan fish, or Otophysi, dating from the late Cretaceous Period, only a short time before the non-avian dinosaurs disappeared. Older specimens have been found elsewhere in the world, but none had a well-preserved Weberian apparatus, Liu said.

Technicians with the Canadian Light Source at the University of Saskatchewan in Saskatoon and at McGill University in Montreal captured 3D X-ray scans of the fish, and Liu modeled the ossicles of the Weberian apparatus in her laboratory. The model suggests that, even 67 million years ago, otophysan fish had nearly as sensitive hearing as zebrafish do today.

"We weren't sure if this was a fully functional Weberian apparatus, but it turns out the simulation worked," Liu said. "The Weberian apparatus has just a little bit lower output power, which means lower sensitivity, compared to a zebrafish. But the peak, the most sensitive frequency, is not too much lower than zebrafish -- between 500 and 1,000 Hertz -- which is not too bad at all and which means the higher frequency hearing should have been achieved in this old otophysan fish."

What this means for evolution and diversity

The results underscore a broader pattern in evolution: bursts of new species often follow repeated entries into new habitats, especially when organisms evolve innovations such as more sensitive hearing.

"For a long time, we presumed that the Otophysi probably had a freshwater origin because this group consisted almost exclusively of freshwater fishes," Newbrey said. "The new species provides crucial information for a new interpretation of the evolutionary pathways of the Otophysi with a marine origin. It just makes so much more sense."

Other coauthors of the paper are Donald Brinkman of the Royal Tyrrell Museum, Alison Murray of the University of Alberta, former UC Berkeley undergraduate Zehua Zhou, now a graduate student at Michigan State University, and Lisa Van Loon and Neil Banerjee of Western University in London, Ontario. Liu was funded by a Franklin Research Grant from the American Philosophical Society.