Earthworms and their marine cousins, bloodworms, can look a lot alike. So much so that if you grab a container of bait worms from a tackle shop, you’d be forgiven for not knowing whether they came from soil or muddy seabed. But you’d scarcely think they were relatives from the arrangement of their genes, new research suggests. That’s because the group of earthworms that wiggled out of the ocean hundreds of millions of years ago—members of the class Clitellata—have completely reorganized their genes, landing many in new spots along their chromosomes. In terms of genome structure, a bloodworm looks more like a clam than its dirt-dwelling relatives.
“Clitellates have the most scrambled genomes among animals studied so far,” says Yi-Jyun Luo, an evolutionary biologist at the Biodiversity Research Center, Academia Sinica and leader of one of three groups that independently came to this conclusion this year when studying annelids, the phylum that includes all segmented worms.
How—and more intriguingly why—freshwater worms and their land-based relatives underwent such massive genetic rearrangements is a mystery for now, but there are hints it helped the invertebrates exit the sea. “There’s a clear correlation between all these changes and a habitat shift,” says Rosa Fernández, an evolutionary biologist at the Institute for Evolutionary Biology CSIC-UPF who led one of the teams, which posted their evidence in three preprints in May, one of which completed peer review and was published this month.
Joana Meier, an evolutionary biologist at the Wellcome Sanger Institute, calls the groups’ results “amazing” and “crazy.” Scientists have long believed in the importance of chromosomal stability for reproduction, says University of Vienna biologist Darrin Schultz, co–first author on one of the preprints. When the half-genomes from a sperm and egg come together, these chunks of DNA generally need to match up for an embryo to be viable. “It is very surprising that something like this would evolve,” Meier says. “You’d think there’d be very strong selection against it,” she says.
Early analyses of animal genome sequences supported that notion, says Thomas Lewin, the postdoc who spearheaded the work for Luo’s team and was first author on its paper in Molecular Biology and Evolution. Researchers observed that sets of genes stayed together on chromosomes in distantly related animals, a phenomenon called macrosynteny, roughly meaning “long together ribbons.” “If you look at the genome of anything from a sponge to a coral to a chordate, many of them have got this structure conserved almost perfectly,” Lewin says.
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But that’s not what the three groups saw when they applied new genome analysis methods to earthworms, leeches, and other clitellates. These worms have rejiggered their genomes so extensively that the ribbons of genes consistent across other worms and many groups of ancestral invertebrates were largely unrecognizable (see graphic, below).
“Everything broke and then rearranged completely randomly,” Fernández says. “I made my team repeat the analysis a thousand times.”
Going further than the other teams, her group suggests the genomes of early marine annelids may have been especially open to rearrangement, to judge from their descendants such as bloodworms and ragworms. Chromosomes in these modern worms are “floppy,” they found, allowing genes on separate chromosomes to coordinate by clustering together like the overlap of separate strands of spaghetti. That flexibility might have meant genes were freer to move around and still work together.
Scrambled genes
Certain sets (colors) of genes (individual threads) stay near one another on chromosomes even among distantly related animals. But new work shows the genes in these blocks became increasingly scrambled in earthworm species that moved into fresh water, and then onto land.
And the DNA scrambling in the past not only reorganized genes, it ripped many apart, including ones involved in genome stability and cell division. Fernández calls it a “genomic catastrophe,” which may have also facilitated genomic rearrangements by weakening the cell’s ability to spot and fix mistakes during DNA replication. Though it begs the question of how the animals survived at all.
But the clitellates not only survived the genomic catastrophe; she speculates it may even have enabled them to conquer new environments—first fresh water, giving rise to earthworms like leeches, and then land, leading to earthworms. Fernández’s team found that some genes specific to clitellate worms that are expressed when they are stressed by factors such as changes in oxygen, salinity, or ultraviolet light formed early in their lineage, when bits of once-distant genes became glued together—a hint that genetic pandemonium helped the worms handle the challenges of new environments.
Lewin and others in the field point out that the work can’t distinguish which came first: the genomic rearrangements or the transition to new habitats. “It’s a nice coincidence, and it’s a really nice idea that it might have been involved in the adaptation in some way,” he says. “But in our three papers right now, there’s no actual evidence for that at all. It’s pure speculation.”
The three research teams plan to continue to study the worms to see whether a causal connection holds up. What’s “really fabulous,” says Michigan State University symbiologist Elizabeth Heath-Heckman, who is one of Schultz’s co-authors, is that the tumult in these worms’ genomes hasn’t subsided. “From all three of these papers, you can see that these rearrangements are apparently ongoing,” she says. That means the animals are likely excellent models for uncovering the mechanisms behind genomic instability, as well as how it is tolerated.
Although clitellates’ chromosomal chaos is impressive, it may not be unique. Continuing work by Shultz and colleagues as well as Luo’s group suggests conserving genomic architecture isn’t as essential as previously assumed. Indeed, stability may actually be “the exception, not the rule” in animals, Luo says.
Wilcox, Ph.D. is a science journalist and author with more than a decade of experience telling life’s most compelling stories. As Science’s Newsletter Editor, Wilcox compiles and writes ScienceAdviser, providing readers with a daily distillation of the latest science news, commentary, and research as well as original reporting and analysis.
