Imagine a half-ton tuna laid out on a dock next to a seahorse, a minnow, and a moray eel. That’s just a snapshot of the astonishing diversity found in the group of fishes called teleosts, or ray-finned fish, which today have 30,000 species—more than all living mammals, birds, reptiles, and amphibians combined. For more than a decade, many researchers have assumed that teleosts’ dizzying array of body types evolved because their immediate ancestor somehow duplicated its entire genome, leaving whole sets of genes free to take on other functions.
Now, an examination of the fish fossil record challenges that view. Despite duplicating their genome about 160 million years ago, teleost fish hewed to a few conventional body types for their first 150 million years. Meanwhile, the holostean fishes, a related group with genomes that never underwent a doubling, evolved a stunning diversity of body plans. The work "demonstrates beautifully how necessary it is to look at the fossil record when testing hypotheses about … large-scale evolutionary changes," says Robert Sansom, a paleontologist at the University of Manchester in the United Kingdom.
The link between genome duplication and diversification has seemed so intuitive that it has "almost become an urban legend," says Michael Lynch, an evolutionary biologist at Indiana University, Bloomington. The textbook case was the contrast between teleosts, with their spectacular diversification, and holosteans, which today have a mere eight species in just two body types (bowfins and gars). Flowering plants, too, are rife with such duplications and are champions of diversity among plants. In both cases, evolutionary biologists assumed that some DNA replication quirk doubled the genome. Then, while the pre-existing genes kept the species viable, the extra gene copies could evolve new functions, thus speeding evolutionary change.
John Clarke, now a paleontologist at the University of Pennsylvania, decided to test this “legend” by comparing the diversity of teleosts and holosteans in the fossil record. He visited 15 museums around the world measuring and photographing specimens from 250 million to 100 million years ago, then compared their rates of diversification. "Teleosts weren't always special," Clarke concludes. As he and his colleagues report online today in the Proceedings of the National Academy of Sciences, teleosts got off to a slow start in their first 150 million years. Meanwhile, the holosteans evolved diverse shapes and sizes, most of which have since gone extinct. "[Fish] without the duplicated genome are diversifying just fine," as fast or even faster than teleosts, notes Michael Alfaro, an evolutionary ichthyologist at the University of California, Los Angeles.
Other recent work has questioned the consequences of gene duplications in flowering plants as well. Given how often plants today undergo genome doubling and tripling, relatively few living species have multiple sets of DNA buried in their genomes, suggesting that such doubles often tend to be evolutionary dead ends.
Some evidence suggests that genome duplications may actually promote diversity, but not right away. In several groups of flowering plants, such as the Brassicales, which include cabbage and papaya, diversity seems to have exploded perhaps as many as 50 million years after the genomes doubled. "More and more examples from the plant field [show] a time lag," says Ingo Braasch, an evolutionary developmental geneticist at Michigan State University in East Lansing. Such a lag might also be at play in the teleost story, says Itay Mayrose, an evolutionary biologist at Tel Aviv University in Israel.
Others, however, think it’s time for evolutionary biologists to move on. Researchers have thoroughly documented that many species have arisen in the kind of evolutionary flowering seen in teleosts. "Genome duplication was such a nice, tidy explanation” for this extraordinary diversity, Sansom says. “Now we need to look for other explanations” for the mechanisms behind it.