Around 400 million years ago, the ancestor of all four-limbed creatures took its first steps onto dry land. Fast-forward about 350 million years, and a descendant of these early landlubbers did an about-face: It waded back into the water. With time, the back-to-the-sea creatures would give rise to animals vastly different from their land-trotting kin: They became the magnificent whales, dolphins, and porpoises that glide through the oceans today.
Going back to being aquatic was a drastic move that would change the animals inside and out, in the space of about 10 million years an eyeblink in evolutionary terms. Members of this group, now called cetaceans, dropped their hind limbs for powerful flukes and lost nearly all their hair. For decades, their bizarre body plans perplexed paleontologists, who speculated they might have arisen from creatures as varied as marine reptiles, seals, marsupials like kangaroos, and even a now-extinct group of wolf-like carnivores.
The cetaceans are on the whole the most peculiar and aberrant of mammals, one scientist wrote in 1945.
Then, in the late 1990s, genetic data confirmed that whales were part of the same evolutionary line that spawned cows, pigs, and camels a branch called artiodactyla. Fossils from modern-day India and Pakistan later fleshed out that family tree, identifying the closest ancient relatives of cetaceans as small, wading deer-like creatures.
But their body plans are just the start of cetaceans weirdness. To survive in the sea, they also had to make internal modifications, altering their blood, saliva, lungs, and skin. Many of those changes arent obvious in fossils, and cetaceans arent easily studied in the lab. Instead, it was, once again, genetics that brought them to light.
With the increasing availability of cetacean genomes, geneticists can now look for the molecular changes that accompanied the back-to-water transition. While its impossible to be certain about the influence of any particular mutation, scientists suspect that many of the ones they see correspond to adaptations that allow cetaceans to dive and thrive in the deep blue sea.
Convergent evolution left whales and dolphins with fish-like features at least superficially. Ron Sanford/Corbis Documentary/Getty Images
The first cetaceans lost a lot more than legs when they went back to the water: Entire genes became nonfunctional. In the vast book of genetic letters that make up a genome, these defunct genes are among the easiest changes to detect. They stand out like garbled or fragmented sentences and no longer encode a full protein.
Such a loss could happen in two ways. Perhaps having a particular gene was somehow detrimental for cetaceans, so animals that lost it gained a survival edge. Or it could be a use it or lose it situation, says genomicist Michael Hiller of the Senckenberg Research Institute in Frankfurt, Germany. If the gene had no purpose in the water, it would randomly accumulate mutations and the animals would be no worse off when it didnt function anymore.
Hiller and colleagues dove into the back-to-water transition by comparing the genomes of four cetaceans dolphin, orca, sperm whale, and minke whale with those of 55 terrestrial mammals plus a manatee, a walrus, and the Weddell seal. Some 85 genes became nonfunctional when cetaceans ancestors adapted to the sea, the team reported in Science Advances in 2019. In many cases, Hiller says, they could guess why those genes became defunct.
For example, cetaceans no longer possess a particular gene SLC4A9 involved in making saliva. That makes sense: What good is spit when your mouth is already full of water?
Cetaceans also lost four genes involved in the synthesis of and response to melatonin, a hormone that regulates sleep. The ancestors of whales probably discovered pretty quickly that they couldnt surface to breathe if they shut off their brains for hours at a time. Modern cetaceans sleep one brain hemisphere at a time, with the other hemisphere staying alert. If you dont have the regular sleep as we know it anymore, then you probably do not need melatonin, says Hiller.
The long periods of time that whales must hold their breath to dive and hunt also seem to have spurred genetic changes. Diving deep, as scuba divers know, means little bubbles of nitrogen can form in the blood and seed clots something that was probably detrimental to early cetaceans. As it happens, two genes (F12 and KLKB1) that normally help kick off blood clotting are no longer functional in cetaceans, presumably lowering this risk. The rest of the clotting machinery remains intact so whales and dolphins can still seal up injuries.
Another lost gene and this one surprised Hiller encodes an enzyme that repairs damaged DNA. He thinks this change has to do with deep dives as well. When cetaceans come up for a breath, oxygen suddenly floods their bloodstreams, and as a result, so do reactive oxygen molecules that can break DNA apart. The missing enzyme DNA polymerase mu normally repairs this kind of damage, but it does so sloppily, often leaving mutations in its wake. Other enzymes are more accurate. Perhaps, Hiller thinks, mu was just too sloppy for the cetacean lifestyle, unable to handle the volume of reactive oxygen molecules produced by the constant diving and resurfacing. Dropping the inaccurate enzyme and leaving the repair job to more accurate ones that cetaceans also possess may have boosted the chances that oxygen damage was repaired correctly.
Cetaceans arent the only mammals that returned to the water, and the genetic losses in other aquatic mammals often parallel those in whales and dolphins. For example, both cetaceans and manatees have deactivated a gene called MMP12, which normally degrades the stretchy lung protein called elastin. Maybe that deactivation helped both groups of animals develop highly elastic lungs, allowing them to quickly exhale and inhale some 90 percent of their lungs volume when they surface.
Deep-diving adaptations arent all about loss, though. One conspicuous gain is in the gene that carries instructions for myoglobin, a protein that supplies oxygen to muscles. Scientists have examined myoglobin genes in diving animals from tiny water shrews all the way up to giant whales, and discovered a pattern: In many divers, the surface of the protein has a more positive charge. That would make the myoglobin molecules repel each other like two north magnets. This, researchers suspect, allows diving mammals to maintain high concentrations of myoglobin without the proteins glomming together, and thus high concentrations of muscle oxygen when they dive.
Conveergent evolution left many animals across classes with similar features despite only distant relations. Heraldo Mussolini/Stocktrek Images/Stocktrek Images/Getty Images
Early cetaceans faced another challenge when they started swimming: billions of tiny germs. Compared with air, aquatic habitats are a funky stew of viruses, bacteria, and other pathogens that try to sneak into whales bodies through their skin and lungs. Its a living environment, says Nathan Clark, an evolutionary geneticist at the University of Utah in Salt Lake City. Everything facing the external environment is getting hit harder by pathogens. He thinks those sea germs spurred genetic changes affecting the skin and lungs of mammals that returned to the sea.
Clark and colleagues found these skin and lung alterations when they examined the DNA of cetaceans, sirens (manatees and dugongs), and pinnipeds (seals, walruses, and sea lions). They looked for cases where, in all the aquatic mammals, a certain gene seemed to have accumulated DNA changes more rapidly, or more slowly, than the same gene in terrestrial mammals. That pattern would tell them that a gene was under strong evolutionary pressure as the aquatic creatures adapted to the ocean.
The researchers reported in 2016 that they found hundreds of genes that showed just this pattern in members of these three different aquatic groups. Genes under such dialed-up evolutionary pressure included ones that code for proteins in the skin, and a gene encoding the liquid surfactant that coats the inside of the lungs. Its difficult to know exactly how those genetic changes altered the animals physiology for the better, but protection from germs is Clarks best guess.
Not surprisingly, then, genes of the immune system also changed when cetaceans went back underwater. In fact, thats a common evolutionary pattern, says Andrea Cabrera, an evolutionary biologist at the University of Copenhagen who coauthored a 2021 perspective on genetics and cetacean evolution in the Annual Review of Ecology, Evolution, and Systematics. Every time you change the environment, you have to adapt to the new composition of pathogens and microbes, Cabrera says. Scientists in China even discovered that the dolphin version of a particular sensor for bacteria is less efficient at responding to land-based germs than its counterpart protein from cows.
When Clark screened specifically for genes that were lost when cetaceans, sirenians, and pinnipeds went back to the water, his No. 1 hit was a gene called PON1. The function of the protein it encodes isnt entirely understood, but Clark suspects that deactivating it protected cetaceans from inflammation that would otherwise occur when they held their breaths for a long time.
Deactivating the PON1 gene was all well and good when cetaceans first slipped back into the sea. But today, a functional PON1 gene might come in handy. In mammals, it encodes the primary enzyme that can degrade toxic organophosphate pesticides. Insects lack PON1, so theyre susceptible; we humans and other land mammals are somewhat protected. If these marine mammals are missing it, if theyre hanging out near agricultural runoff and canals like manatees do, it could be a concern, Clark says.
Blubber and skin from a bottlenose dolphin. Jason Edwards 972332/51C CrRM/The Image Bank Unreleased/Getty Images
Clark and other scientists have also observed a big reduction in functional cetacean genes for smell by nearly 80 percent among toothed whales, in one study and for taste. Terrestrial mammals have hundreds of olfactory receptors that allow them to distinguish a panoply of odors, but the receptors work in the air, not water. (Theyre different from the underwater sensory systems that fish such as sharks use.)
Presumably, cetaceans werent getting any benefit from the receptors, so they lost them. This squares with changes in anatomy. Baleen whales such as humpbacks have very reduced olfactory structures, and toothed whales such as orcas have none at all. And it seems that taste isnt so useful, either, if youre swallowing dinner whole. Cetaceans no longer possess the genes to sense sour, sweet, umami or most bitter tastes.
They arent the only ones with such a bland experience of seafood. Other marine mammals, and even non-mammals, that returned to water experienced similar genetic losses. Penguins have fewer intact olfactory receptor genes than other water birds, and their taste receptor genes suggest theyve lost the ability to sense sweet, bitter and umami, leaving them with nothing but sour and salty. Takushi Kishida, an evolutionary geneticist at the Museum of Natural and Environmental History in Shizuoka, Japan, has even found that sea snakes lost several olfactory receptor genes when they wriggled back into the water.
Not only is there no way to smell in the deep, but its dark. So its no surprise that cetaceans changed some genes for vision, too. Most mammal eyes have light sensors called rods for low-light, colorless vision, plus two kinds of cones, one for green light and one for blue light. (Humans have a bonus cone for red.) As cetaceans evolved, the gene for the rod sensors morphed to be more sensitive to blue light perfect for the inky blue deep. Then there were several instances when the animals lost one or both cones. Some cetaceans, like belugas and orcas, still retain the blue cones. Others, such as sperm whales, have neither cone and, thus, fully monochromatic vision.
Scientists know they are only just beginning to plumb the genetic depths of cetacean evolution. Now, with dozens of cetacean genomes available to study, and with new analytic techniques under development, they are poised to further probe the aquatic transition, along with other exciting moments in cetacean evolutionary history. Dolphins alone offer a wealth of questions: How did they diversify into so many types? They make up nearly half of cetacean species today. How did they and other toothed whales pick up the skill of echolocation, navigating the ocean via sound? And how did dolphin brains get so large, with a brain-to-body-size ratio to rival that of great apes?
Most of the important problems, says Kishida, are still unsolved.
This article originally appeared in Knowable Magazine, an independent journalistic endeavor from Annual Reviews. Sign up for the newsletter.
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