Flying fish can glide over the surface of the ocean because of their body proportions. Surprisingly few genetic changes were required.
A flying fish is able to shoot out of the water and glide long distances because of its longer and more rigid fins than other fish. In a triumph of evolution, creatures that were once strictly aquatic were transformed into temporarily airborne ones through a few modifications in body shape.
Matthew Harris of Harvard Medical School and Boston Children's Hospital led a group of researchers who discovered that the distinctive body shape of flying fishes was due to changes in just two genes.
Harris said that when they first started out in evo-devo, they didn't think they would be able to make large jumps in form with such simple rules. The study was published in the November issue of Current Biology.
The findings suggest that bioelectric signals within developing tissues, not just chemical ones, can regulate the growth and shape of developing fins and possibly other structures. The study and earlier work show how small genetic changes can produce big changes in the body.
Natural selection has tinkered with the genetic programs that control development in order to create a wide range of animal forms. New niches for species can be created by tweaking the timing and speed of tissue growth. The study of this process has been going on for a long time, but recently researchers have been able to look for genes that are involved in certain changes.
Researchers in the Harris lab began by comparing the genomes of 35 species of flying fish and their close relatives to find the genetic basis of the flying fish. They found genes that seemed to have evolved under selection pressure by looking for regions of DNA that had changed quickly between species.
The main factors driving the formation of the new body type were looked at in the comparative analysis. How are you going to find out if the smoking gun is the genes? He said that you can't modify it in the flying fish. You have to find a way to do that.
Harris' team turned to zebra fish, a freshwater minnows widely kept as aquarium pets but also as research animals. His team used chemicals and rays to create random changes in zebra fish embryos. They searched for interesting adult characteristics in those that survived to adulthood. This approach was different because it focused on the early development of the animals.
Jacob Daane, a PhD student in the Harris lab, and his colleagues screened a collection of previously known zebra fish mutants with long fins to look for genes that might regulate the growth of the flying fishes fins. They homed in on two of them, kcnh2a and lat4a, which are loss-of-function and potassium channels, respectively.
In zebra fish, the loss of function in the leucine transporter causes all fins to be short, while the over expression of the potassium channels causes all fins to be long. A clumsy fish can be produced by either of those changes. The zebra fish has long and short median fins, the form of the flying fish, when the two mutations are combined.
Matthew Harris, a researcher at Boston Children's Hospital and Harvard Medical School, has created thousands of different types of zebra fish to study the evolution of fins and limbs. Aquarium pets are popular with studies of genetic and development.
Micheal Goderre is a doctor at the Boston Children's Hospital.
Daane said that a single point change can give you big fins. I don't know of any other system where there is that level of simplicity in terms of major scale changes to an organ's size.
The flying fish body plan always relied on the same types of mutations in the leucine transporter and the potassium channel. The leucine transporter changes in the different lineages are the same as the changes in the genetic trick to evolve this shape. Sarah McMenamin, a fish evolutionary developmental biologist at Boston College, said that nature has targeted the same specific gene in a couple of different contexts.
The cause of the extra growth in the fin is a mystery. Harris said that it is not like a receptor-ligand interaction where things are binding to the receptor on the inside of the cell. The cell is more active and responsive because of the changes in the resting and pH of the cytoplasm. The fin cells start to show signaling characteristics that are associated with stem cells. Harris said that it is possible that the changes in cell signaling might affect how the fin grows. He said that people don't really understand much about the new ground.
The researchers found that the growth of the fins was blocked because of the blocking of the potassium ion from passing between the fin cells. The cells of the fin are thought to be a single mass with many nuclei floating in it. Harris said that the electric field set up by the potassium ion could create more potential for long-range signaling coordination than a typical morphogen or secreted factor. Other researchers have seen evidence that electric fields may play a role in guiding the development of tissues.
The Harris lab made an exciting discovery about the evolution of appendages in February of 2021. The ancestors of zebra fish differed about 450 million years ago from the lineages that later gave rise to tetrapods, but a single mutation can awaken a potential for limb patterning in zebra fish fins. Two studies published online with this one in Cell looked at the genomes of early branching ray-finned fishes and African lungfish and suggested that a capacity to build limbs was present in the common ancestor of all bony fish.
The zebra fish has a pect fin that connects to the body with just one layer of bones. The Harris team found two new intermediate radial bones in the zebra fish that they discovered in their genetic screen. The muscles were attached to the bones.
With only one change, we are making a brand new structure that is well integrated and patterned. This kind of throwback shows how ancient and shared the genetic "grammar" for making fins and limbs was.
The Harris lab has shown that the genetic potential to make these elaborations in the endoskeleton are still retained in modern ray-finned fish, and they have the potential to build more elaborated structures.
Flying fish seem to have evolved their unusual form of locomotion as a strategy for evading the predatory fish that swim just beneath the waves.
The point that fins and limbs develop under the genetic influence of highly conserved mechanisms is reinforced by new studies. A paper published in November in the Proceedings of the National Academy of Sciences identified a gene that regulates the formation of digits in the limbs and the outer edges of fins. A study in Current Biology found that the hind feet of jerboas, tiny bipedal rodents that can hop, skip and run at extraordinary speeds, result from a gene that causes disproportionate bone growth in their limbs.
The most interesting question to Marcus Davis, an evolutionary developmental biologist at James Madison University, is where the original developmental program came from. The program for fins and limbs was probably modified from an older program for other parts of the body. He said that it had to come from somewhere. The appendage program was modified over time to build the other parts of the body.
The development of the dorsal and anal fins is more ancient than the pairs of fins, which is why Tetsuya believes the genetic program for building them is derived from that. The group of jawless fish that first evolved about half a billion years ago have no fins.
Even though appendages and body shapes have roots in the same ancient genetic networks, the changes between them were major. He believes that the limb is an evolutionary novelty. What enabled those changes to evolve is still being learned.
The unconventional approach used in the Harris laboratory, which Davis praised as "atypical and modern" and McMenamin hailed as "creative" and "a tour de force," points to one way that evo-devo researchers might find answers. Studies often look for genes that regulate limb and fin patterning in the hunt for genes that regulate development. The Harris team used comparative genomics and large-scale genetic screens to identify fish with interesting, relevant phenotypes. They had to be willing to follow where that led them.
Harris said that unexpected things come out when we start asking the right questions.
An injection of chaos solved a decades-old mystery.
