Electric Fish Genomes Reveal How Evolution Repeats Itself
The electric eel is one of several species of freshwater fish in South America that generate electricity to navigate, communicate, hunt or defend themselves. Fish in Africa independently evolved electric organs that are strikingly similar, though the molecular details of their operation are different.
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Introduction
Along the murky bottom of the Amazon River, serpentine fish called electric eels scour the gloom for unwary frogs or other small prey. When one swims by, the fish unleash two 600-volt pulses of electricity to stun or kill it. This high-voltage hunting tactic is distinctive, but a handful of other fish species also use electricity: They generate and sense weaker voltages when navigating through muddy, slow-moving waters and when communicating with others of their species through gentle shocks akin to morse code.
Normally, when several species share an ability as unusual as generating electricity, it’s because they’re closely related. But the electric fish in the rivers of South America and Africa span six distinct taxonomic groups, and there are three other marine lineages of electric fish beyond them. Even Charles Darwin mused on both the novelty of their electrical abilities and the strange taxonomic and geographic distribution of them in On the Origin of Species, writing, “It is impossible to conceive by what steps these wondrous organs have been produced” — not just once, but repeatedly.
A recent paper published in Science Advances helps to unravel this evolutionary mystery. “We’re really just following up on Darwin, as most biologists do,” said Harold Zakon, an integrative biologist at the University of Texas, Austin and co-senior author of the study. By piecing together genomic clues, his team in Texas and colleagues at Michigan State University uncovered how a number of strikingly similar electric organs arose in electric fish lineages separated by roughly 120 million years of evolution and 1,600 miles of ocean. As it turns out, there’s more than one way to evolve an electric organ, but nature does have some favorite tricks to fall back on.
The South American and African fish that Zakon’s group studies get their zap from specialized electric organs extending along much of their body. Modified muscle cells called electrocytes in the organs create sodium ion gradients. When sodium-gate proteins in the membranes of the electrocytes open, this produces a burst of current. “It’s about the simplest signal you could imagine,” said Zakon.
In muscle, these electric signals flow through and between cells to help them contract for movements, but in the electric organs the voltage is directed outward. The strength of each shock depends on how many electrocytes fire at once. Most electric fish only fire a few at a time, but because electric eels pack an unusually high number of electric cells, they can unleash voltages powerful enough to kill small prey.
In the new work, Zakon, his former research technician Sarah LaPotin (now a doctoral candidate at the University of Utah) and his other colleagues reconstructed a key aspect of the evolution of these electric organs by tracing the fishes’ genomic history.
It began between 320 million and 400 million years ago, when the ancestor of all fish classified as teleosts survived a rare genetic accident that duplicated its entire genome. Whole-genome duplications are often deadly for vertebrates. But because they create redundant copies of everything in the genome, duplications can also open up previously untapped genetic possibilities. “Suddenly, you have the capacity to make a whole new pathway, instead of just one new gene,” said Gavin Conant, a systems biologist at North Carolina State University who was not involved in the study.
Harold Zakon, an integrative biologist at the University of Texas, Austin, was one of the leaders of the new study of electric fish evolution. “We’re really just following up on Darwin, as most biologists do,” he said.
For more recent ancestors of today’s freshwater electric fish, which are teleosts, the duplication meant that they had an extra copy of a gene for an important sodium pump. One copy continued to work in muscle cells; the second acquired mutations that conferred distinctive electrical properties on electrocytes.
But crucially, before any electric organ-specific adaptations could be adopted, that second copy of the gene first had to be deactivated in muscle cells — otherwise, the emerging electrocyte capabilities would have interfered with movement. And when Zakon and his colleagues looked at how the electric fish turned off the gene, they were surprised to discover that different lineages of electric fish did it differently.
In the muscle tissue of the African fish, sodium-pump gene was still functional, but like a lock with no key, it could not activate without helper molecules that muscle tissue did not make. In most of the South American fish, the pump was just missing from the muscles — the sodium-pump gene was largely inactive because it was missing an essential control element that specifically boosts the expression of the sodium pump in muscle. In one oddball lineage of South American fish, the gene did still function in muscle. It was temporarily inactive in young fish but turned back on when an entirely different set of genes took over control of the sodium channel in the electric organ as the fish matured.
So in a textbook case of convergent evolution, the various lineages of fish independently hit on the strategy of modifying their muscle tissue to create electrical organs, and they even did so by making their sodium pumps work selectively in different tissues. But they diverged in precisely how they regulated the pumps.
Oftentimes, when scientists investigate a case of convergent evolution, the traits turn out to arise by essentially the same mechanism, explained Johann Eberhart, a molecular biologist at the University of Texas, Austin and one of the new study’s co-authors. “But this was quite different,” he said. “And I think that’s exciting.”
Conant noted that the new findings “sort of mirrored what we’ve seen” in his own group’s research. His lab discovered that while other teleost fish had lost certain duplicate genes for sending signals between nerves and muscles, some electric fish lineages retained them. Without these key genes placing their electric organs under direct voluntary control, electric eels could not have developed their signature potent zap.
Zakon and his colleagues are also intrigued by the potential significance of the control region they found in the sodium pump genes, since it seems to determine precisely which tissues express the protein. The same control region appears in the sodium pumps of humans and other vertebrates. It’s possible that mutations affecting pump activity in our cells might cause or contribute to various health problems such as the muscle weakness condition called myotonia.
The new research touches on only a few of the examples of convergence and divergence on display in electric fish. Some South American lineages produce faint shocks using modified neurons instead of modified muscle cells. Some electric fish in the oceans have evolved more bizarre electrocution strategies; the stargazer, for example, administers shocks from modified muscles in its eyes.
But for Zakon, it’s the convergent solutions that are most helpful in addressing a fundamental puzzle of biology: If you could rewind the course of evolution, would it play back the same way? Seeing a unique innovation is “fascinating,” he said, but “it doesn’t answer the question, ‘Was there only one way to get there?’” The mix of convergence and divergence seen in organ systems like those of the diverse electric fish offers a much richer view of how predictable — and quirky — biology can be.
