“We like to think of it as a baseball hitter that strikes out a lot, but when they do hit, it’s a home run,” said Douglas Soltis, a plant evolutionary geneticist at the Florida Museum of Natural History. “Polyploidy is the most important process on the planet that hardly anybody knows anything about.”
Advances in whole-genome sequencing are changing that. Studies across the tree of life are finding that genome duplication isn’t exactly an infrequent occurrence. Among plants, it’s hard to avoid, said Jonathan Wendel, an evolutionary biologist at Iowa State University: All seed plants living today have experienced at least one ancient whole-genome duplication, and many have undergone more. Barnacles, insects, trout, and arachnids carry evidence of ancient duplications in their genomes. Biologists hotly debate whether the significant evolutionary changes that led to jawed vertebrates, from hagfish to humans, are connected by ancient gene duplications hundreds of millions of years ago.
Like gene inversions and translocations or single-nucleotide point mutations, a whole-genome duplication is a type of genetic mutation that fuels evolutionary change. In fact, genome doubling is the single most radical mutation an organism can experience in a single generation. Researchers are analyzing the whole genomes of diverse species to find out how organisms manage not only to survive such a potentially lethal event, but also to thrive and adapt in its wake. “All these different interrogative tools have opened up this world to us that we could not see and hence did not know existed,” Wendel said.
A story of how this process unfolds is being written in potamo’s genome. Neiman’s team dated the snail’s genome duplication to less than a million years ago — incredibly recent in evolutionary terms, but long enough ago for the species to have begun the longer process of adjusting to its heavier genomic load. That recency is giving Neiman a close view of how potamo has managed its polyploid existence.
This is the latest evidence amid a growing awareness of polyploidy that is shifting science’s understanding of genome duplication’s evolutionary importance. The serene shores of Lake Alexandrina are about as far from the Las Vegas strip as you can get, but that didn’t stop potamos from taking one of evolution’s biggest gambles.
Genetic Backup
Until the advent of widespread DNA sequencing, polyploidy remained largely shrouded in mystery. Scientists knew that it happened: It was obvious to anyone in the habit of counting chromosomes under a microscope. But it wasn’t until researchers could analyze genomes, base pair by base pair, that they began to appreciate the full implications of whole-genome duplication.
Analyzing base pairs is how the evolutionary biologist Kenneth Wolfe at University College Dublin became interested in polyploidy. When he started his lab in the early 1990s, he took advantage of a European Union initiative that would pay scientists 2 euros per nucleotide to sequence the genome of baker’s yeast, Saccharomyces cerevisiae. (In 2022, sequencing cost roughly $0.000000006 per nucleotide in U.S. dollars.) Wolfe wasn’t especially interested in yeast, but his lab needed the money. Later, when he and other researchers with the Saccharomyces Genome Sequencing Project started sharing their results, they noticed something interesting.
“There just seemed to be an awful lot of duplicated genes in these genomes,” he recalled. As the genome project reached completion, Wolfe and his team found that yeast DNA was full of doubled regions. The duplicated segments were around 60% identical, and regions of closely related DNA were separated by far longer stretches of unique genes. “You could really see the history of what had happened,” he said. “You could track every gene and see what happened to it.”
Wolfe suspected that he was seeing evidence of a past genome duplication event alongside indications that the cells were in the process of pruning back excess DNA. Wolfe’s 1997 Nature paper on the subject helped turn increasing attention to both polyploidy and the inverse process, rediploidization, in which an organism retains some of its doubled genes and discards others, ultimately bringing the genome back to a streamlined diploid state.
As the complete genome sequences of other model organisms began trickling in, Wolfe used his bioinformatics expertise to look for genome duplications there. The roundworm Caenorhabditis elegans was devoid of polyploidy. So, too, was the fruit fly. Perhaps, Wolfe mused, what he saw in yeast was a fluke. Then, in 2000, the genome of the model plant Arabidopsis was published.
“There was a genome duplication in there screaming at us,” he said. “And it wasn’t just my lab — several labs discovered this genome duplication.”
Past biologists had theorized about the evolutionary benefit of doubled genes. In 1970, the Japanese American geneticist Susumu Ohno had published Evolution by Gene Duplication, which posited that the duplication of individual genes was an underappreciated source of evolutionary novelty. A doubling event on its own can result in novel traits. Plus, with two copies of each gene, evolution can tinker with one version while keeping the other as a backup; a new function could emerge without a gene losing its existing use. The same could potentially be true if the entire genome was doubled. In his treatise, Ohno hypothesized that all vertebrate genomes contained evidence of an ancient genome duplication event. Subsequent genome sequencing has shown this to be the case.
“You might think that the genome, the blueprint of life, would be a stable thing,” said Sarah Otto, an evolutionary biologist at the University of British Columbia. “It’s not. It’s all over the map.”
The challenge for biologists studying polyploidy was that the cellular shock of sudden genome doubling is often lethal. Even offspring that survive are usually sterile and have no way of passing on the extra DNA. To find out how a polyploidy event could be survivable, they would need input from plant biologists, who had myriad opportunities to watch it unfold.
Radical Change
Several decades ago, in the dry prairies of eastern Washington, Pamela Soltis and Douglas Soltis began tracking a polyploidy event. They knew almost exactly when it had happened: Several species of a plant known as goatsbeard were brought to the United States from Europe in the mid-1920s. They hybridized, and before long, two new species emerged with 24 chromosomes — twice as many as the original species. By growing the plants from seed and studying their genomes, the Soltises could see what happens to cells in the immediate aftermath of genome duplication.
What they found was chaos. Almost as soon as the goatsbeard acquired the extra DNA, the plants started to tinker with their surplus of genes — changing some genes, getting rid of others, keeping a few, Douglas Soltis said. “Immediately, in one generation, they’re already beginning to get rid of certain copies of genes [and] not expressing certain genes as much as other genes.”
