Earthworms and Leeches Have the Most Scrambled Genomes Known

Clitellate genomes underwent a genetic upheaval

When worms first moved from saltwater into freshwater, their genetic material appears to have been catastrophically reorganised.

The event tore apart previously functional genes, including genes involved in essential cell-division mechanisms. It left earthworms, leeches and their other clitellate relatives with the most scrambled genomes yet identified.

"Everything broke and then rearranged completely randomly," Rosa Fernández, of Spain's Institute of Evolutionary Biology (CSIC-UPF), told Christie Wilcox at Science. "I made my team repeat the analysis a thousand times."

Three separate research groups have independently arrived at the same finding. Their work challenges the long-held idea that animal species need a degree of genetic stability to avoid extinction.

Evolutionary biologist Carlos Vargas-Chávez, also at CSIC-UPF, and his colleagues found that gene loss is roughly 25 percent greater in the worm lineage that became clitellata than in its other relatives.

Freshwater and land may have driven chromosome change

The researchers suspect that the worms' genomes became scrambled as they adapted to new environments. However, they have not yet established whether the worms' moves into freshwater and onto land happened first, or whether their genes first shifted to new locations on their chromosomes.

"While the timing of this genomic rearrangement remains unclear, we argue that the genomic hallmarks observed in clitellates are highly unlikely to have arisen via… rearrangements over time," the researchers write in their paper.

Rather, the patterns identified by Vargas-Chávez and his team point to a "single cellular catastrophe" that effectively shattered a worm genome over a brief period. They propose that severe environmental shifts, such as sudden exposure to higher oxygen levels or radiation, may have caused it.

The authors compare the scale of the worms' genomic transformation with processes observed in cancer cells.

Earthworms and leeches lost ancient genome architecture

Most bilaterians - animals, including humans, with left and right sides that mirror one another - were believed to retain highly conserved chromosome sections. That stability is important for correctly lining up the two DNA strands within them as they separate and then pair, with one strand inherited from each parent during reproduction.

From sponges to monkeys, genomes contain long stretches of genes that retain a particular order among distantly related species. These gene ribbons have been conserved for hundreds of millions of years.

Although such ribbons can shift position to a degree, the sequences within each section generally remain largely preserved. Leeches and earthworms are an exception.

"Overall, the ancient bilaterian genome architecture has been completely lost within the clitellates," found a second team led by evolutionary genomicist Thomas Lewin of Taiwan's Biodiversity Research Center.

Lewin's group is examining how these unexpectedly extreme chromosomal alterations have influenced animal evolution.

"Cases of genome structure conservation are exceptionally rare," Lewin and colleagues state in another study, maintaining that, contrary to earlier assumptions, they are "the exception rather than the rule".

Chromosome scrambling and extinction risk

Large-scale genetic reorganisation may be more widespread than scientists once believed, but it carries the expected dangers. A third group studied the genomes of 2,291 species from every major animal clade and found that extreme chromosomal alterations can be linked to major extinction events.

"One outstanding question is how this profound genome reshaping event did not result in extinction," Vargas-Chávez and colleagues write.

They found that ancestral marine worm genomes do not appear to be arranged into compartments, making them "much more floppy" than those of other animals.

This "may have resulted in a high resilience to the deep genome reshaping occurring after chromosome scrambling," the team concludes. The finding also indicates that similarly dramatic genetic rearrangements may still be taking place in these species.

This research is available on the bioRxiv preprint server alongside two related papers, while another study has been published in Molecular Biology and Evolution.