The skates developed their undulating wings thanks to the origami of the genome

A ray embryo

A skate embryo at an early stage of development

David Gold, Lynn Kee and Meghan Morrissey, Embryology Course, Marine Biology Laboratory

The skates got their wing-like fins using a genetic mix that folded different sections of their genomes into physical contact with each other. This created a new pattern of gene activity in the fins of stingray embryos, highlighting how changes in three-dimensional genomic architecture can drive the evolution of new body structures.

Evolutionary biologists are fascinated by the fins of fish because they represent one of the great innovations in vertebrates: paired appendages. These show an amazing variety of shapes, including our arms. In skates, the equivalent is their front, or pectoral, fins which have extended forward and fused with the head.

“One way or another, the pectoral fin and the head are completely combined and integrated in terms of function and structure,” explains Tetsuya Nakamura, a developmental biologist at Rutgers University in New Jersey. “It’s a pretty remarkable animal.”

To study the evolution of fins, Nakamura’s team, along with five other groups, looked at the 3D structure of the ray genome (Leucoraja erinacea).

They wanted to study rays because their genomes, like those of sharks and rays, evolved more slowly and resemble those of ancestral vertebrates more than other animals commonly used in research, such as zebrafish. This makes it easier to spot important changes and gives a perspective on the evolution of the genome spanning a longer time scale.

The researchers were looking for structures called topological association domains (TADs). They are large self-contained loops of DNA and protein that bring genes into contact with non-coding regions of DNA called activators that control where and when genes are active.

TADs are known to play a role in the development and disruption of their structure can cause congenital diseases in humans. Modified TADs have also been found to drive evolutionary innovations in other mammals, such as the gonads of female moles. A big question is whether they played a larger role in the evolution of vertebrates.

The teams deduced the 3D structure of the TADs skateboards, then compared them to those of their closest relatives, the sharks. They found sections of DNA that had been broken up and moved around in skate TADs involving planar cell polarity genes, which help cells all point in the same direction in the plane of a tissue. These genes explain why hairs in mammalian skin all point in a certain direction.

The team showed that one of these genes was now active in the development of pectoral fins in rays, but not in sharks. Nakamura thinks this could mean that ray fin cells can all elongate in the same direction, influencing the shape of the tissue.

This will not be the whole story of the evolution of skate fins. Other genes and activators will be involved, he says. “Evolution is really complicated. More than we expected.

The team found that TADs influenced which sections of DNA could be moved or lost and which should be kept intact during evolution. “I think it’s a completely different way of looking at how genomes evolve,” says a team member DarIoLupiAez at the Max Delbrück Center in Berlin, Germany.

Work shows the power of analyzing and comparing 3D genomic structures to reveal new mechanisms behind evolutionary innovations, says Matthew Harris at Harvard Medical School. Using this approach, rather than looking at how known genes are regulated, can yield big surprises, like this. “No one would have started the day thinking that planar cell polarity was involved in fin evolution,” he says.


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