Electric fish genome; How does evolution repeat itself?

In the muddy bed of the Amazon River, snake-like fish called electric eels search for frogs and other small prey in the dark. When a prey swims by a fish, the fish releases two pulses of 600 volts of electricity to stun or kill it.

This high-voltage hunting tactic is a distinctive tactic, but a handful of other fish species also use electricity. They generate and sense weaker voltages when moving in muddy, slow-moving waters and when communicating with other members of their species.

When several species have unusual abilities such as generating electricity, it is usually because they are closely related. But the electric fish in the rivers of South America and Africa include six distinct taxonomic groups, and apart from them there are three other marine lineages of electric fish.

Even Charles Darwin thought about the novelty of electrical abilities and the strange taxonomy and unusual geographical distribution of fish with these abilities, and wrote in his book On the Origin of Species: “It is impossible to imagine that these strange members have not only once, but many times.” were created, during what stages were they produced.

A recent article in the magazine Science Advances published, will help unravel this evolutionary mystery. “We, like most biologists, are just following Darwin,” says Harold Zaccone, a biologist at the University of Texas at Austin and one of the authors of the new study.

By piecing together genomic clues, Zaccone’s team in Texas and colleagues at Michigan State University discovered how similar electric organs appeared separately in different lineages of electric fish over about 120 million years of evolution and 1,600 miles of ocean apart.

Researchers’ studies show that there is more than one way to evolve electrical organs. The South American and African fish Zaccone’s group studies get their electricity from specialized electrical organs that run along their bodies.

Altered muscle cells called electrocytes create a sodium ion gradient in these organs. When the sodium channel proteins in the electrocyte membrane open, a sudden current occurs. “This ability is connected to the simplest signal you can imagine,” Zaccone says.

In muscle, these electrical signals flow in and between cells to help the muscles contract for movement, but in electrical organs, the voltage is directed outward. The intensity of each shock depends on the number of electrocytes that are fired at any given time.

In most electric fish, only a few electrocytes fire at a time, but because electric eels have so many electric cells, they can release voltages powerful enough to kill small prey.

electric eel

The electric eel is one of several freshwater fish species in South America that generate electricity for navigation, communication, hunting, or self-defense. Fish in Africa have independently evolved electrical organs that are strikingly similar, although the molecular details of their function differ.

In their new work, Zaccone and his colleagues reconstructed a key aspect of the evolution of electric organs by tracing the genomic history of these fishes. The evolution of these organs began between 320 and 400 million years ago. At that time, the ancestor of all fish classified as teleosts survived a rare genetic accident that duplicated its entire genome.

Whole genome duplication is often fatal for vertebrates. But since this phenomenon creates extra copies of everything in the genome, genetic duplication can also open up new genetic possibilities that have not been exploited before.

“Suddenly, instead of just having a new gene, you have the capacity to make a whole new pathway,” said North Carolina State University biologist Gavin Conant, who was not involved in the study.

Harold Zakon / Harold Zakon

Harold Zaccone, a biologist at the University of Texas at Austin, was one of the leaders of the new study on the evolution of electric fish. “Like most biologists, we just follow Darwin,” he said.

For the more recent ancestors of today’s freshwater electric fish, which belong to the teleost group, doubling up meant they had an extra copy of a gene important for the sodium pump. One version continued to work in muscle cells, and the other version acquired mutations that gave electrocytes distinct electrical properties.

Crucially, before any electrical organ-specific adaptations could be achieved, the second version of the gene had to be inactivated in the muscle cells. Otherwise, emerging electrocytic capabilities would interfere with movement.

When Zaccone and his colleagues looked at how genes were switched off in electric fish, they were surprised to discover that different lines of electric fish did it differently. In the muscle tissue of the African fish, the sodium pump gene was still functional, but like a lock without a key, it could not be activated without special helper molecules that were not produced in the muscle tissue.

In most South American fishes, this pump was not present in the muscles. The sodium pump gene was largely inactive because it lacked one of the essential control elements that specifically increases sodium pump expression in muscle. In one of the strange lineages of South American fish, this gene was still active in the muscles.

The gene was effectively inactive in young fish, but was reactivated as the fish matured, when a different set of genes took over control of the sodium channel in the electroorgan. Thus, in a clear example of convergent evolution, different lineages of fish had independently developed strategies to modify their muscle tissue to produce electric organs. They had done this by selectively activating the sodium pumps in different tissues, but they differed on how the pumps were regulated.

Inside the zebrafish muscle (left), the fluorescent green label shows a strong wave of electrical activity caused by the sodium pump inside the cells. In the muscle of the South American electric fish (right), the activity is much weaker, because in this fish, the evolution of electric organs began by suppressing the sodium pump in the muscles.

More often than not, when scientists study a case of convergent evolution, it turns out that the traits were created by a similar mechanism, explains Johan Eberhart, a molecular biologist at the University of Texas at Austin and one of the authors of the new study. “But this one was completely different, and I think it’s exciting,” he says.

Conant noted that the new findings somewhat mirror what he has seen in his research group’s research. His lab discovered that while other teleost fish had lost some of the duplicate genes for sending signals between nerves and muscles, some electric fish lineages had retained it. Without these key genes that put electric organs under direct voluntary control, electric eels could not have developed their own electricity.

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Zaccone and his colleagues are also intrigued by the possible importance of this control region they found in sodium pump genes, since it appears to specify with high precision which tissues express the protein. The same control region is seen in the sodium pumps of humans and other vertebrates. Mutations that affect the pump’s activity in our cells may cause various health problems, such as a type of muscle weakness called myotonia.

The new research points to just a few examples of convergence and divergence seen in electric fish. Some South American lineages produce weak shocks using modified neurons instead of modified muscle cells. Some electric fish in the oceans have evolved even more bizarre electrocution strategies. For example, the Uranus fish shocks from modified muscles inside its eye.

For Zaccone, it’s these convergent solutions that are most useful in solving one of biology’s fundamental puzzles: If you could reverse the course of evolution, would it go the same way again? He said it’s amazing to see unique innovation, but he doesn’t answer the question of whether there was only one way to get there.

The combination of convergence and divergence seen in organ systems such as those of diverse electric fishes provides a much richer view of how predictable and how unpredictable biology is.

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