Flying fish may have taken to the air when evolution tweaked electrical signals that control the size of their fins. This discovery suggests the existence of a previously unknown mechanism by which animals can change the relative size of specific body parts.

“How organs and tissues know when to stop growing at a certain size and stay there is a major mystery,” says Jake Daane at Northeastern University in Massachusetts. This scaling, known as allometry, is also a key driver of evolutionary change. The stunning variation in the fins of bony fish are a classic example, from the billowing veils of the tropical betta fish to the stumpy appendages of a mackerel.

Most dramatic of all are the wings of flying fish, which allow some species to leap from the sea and glide for 400 metres, the length of eight Olympic swimming pools. This helps fish evade underwater predators, a tactic so successful that it has evolved independently several times.

In comparisons of the genomes of nine species of flying fish and some non-flying relatives, Daane and his colleagues spotted genetic changes consistently associated with gliding, and uncovered sections of the genome being conserved by natural selection.

The team also studied mutations affecting fin size in zebrafish, which have short fins suited to streams and ponds. This is unlike flying fish, which have expanded their paired fins – equivalents of our arms and legs – into wings to take flight.

The zebrafish work revealed two interesting gene variants: one affecting how potassium ions flow into cells, which made all the fins larger; the other affecting how cells absorb compounds called amino acids, which made all the fins smaller. Neither affected the overall body size of the fish.

Similar genes and cellular processes involving them showed up in the flying fish genomes. But this didn’t explain why only their paired fins are overgrown.

So the team combined both gene variants in one zebrafish, and found that only the paired fins were overgrown, transforming the zebrafish into a copy of a flying fish.

Potassium ion flow affects how electrical charge moves over tissues, which affects embryonic development – including fin growth – and tissue regeneration. But the exact mechanism is poorly understood, and it is unclear how amino acid uptake could tweak bioelectricity to create such specific changes in fin size.

Combining lab genetics with the comparison of genomes is a very creative approach to unpick the mechanisms behind allometry, says Peter Currie at the Australian Regenerative Medicine Institute in Melbourne. Understanding how evolution generates shape and form will aid research into how tissues regenerate, he says. “The more you understand about the evolutionary processes that guide the formation of structures, the more you’ll be able to understand and to use in [medicine].”

Journal reference: BioRxiv, DOI: 10.1101/2021.03.05.434157