It sounds like a bad monster movie plot: A 10-legged mutant creature that reproduces asexually, escapes from confinement in Germany, and quietly begins a global invasion. Within 2 decades, clones of the voracious animal spread through Europe and Africa, bringing devastation to ecosystems and threatening native species.
That appears to be the strange-but-true story of the marbled crayfish, an invasive freshwater species suspected to have been created through a reproductive accident in an aquarium around 1995. A new analysis of the crustacean’s genome supports this unlikely origin and may help explain how the animal has subsequently spread and adapted to so many new environments.
The crayfish’s unusual evolution could also suggest a strategy to tackle a more infamous clonal monster: cancer. “In many ways, the invasive expansion of [the marbled crayfish] is analogous to a cancerous lineage spreading asexually at the expense of its host,” says Jean-François Flot, an evolutionary genomicist at the Free University of Brussels who was not involved with the work.
The marbled crayfish is the only decapod crustacean that reproduces asexually, with the all-female species making clones of itself from eggs unfertilized by sperm. It has been thought to have arisen when two slough crayfish, imported from Florida for the aquarium trade in Germany, mated.
Since its discovery in 1995 in Germany, the marbled crayfish has spread across Europe and into Africa in huge numbers. “They eat anything—rotten leaves, snails or fish broods, small fish, small insects," says Frank Lyko, a molecular geneticist at the German Cancer Research Center in Heidelberg. “This crayfish is a serious pest,” adds Gerhard Scholtz, an evolutionary biologist at Humboldt University in Berlin, who has tracked its rapid spread across the globe, including Madagascar, where its success threatens the existence of the seven crayfish native to that island country. The European Union banned the species: It must not be sold, kept, distributed, or released to the wild.
Five years ago, Lyko became interested in the marbled crayfish, now called Procambarus virginalis, because he thought its newly evolved asexual nature might parallel how a normal cell turns cancerous and begins generating clones of itself. In particular, he wanted to study the genomes of marbled crayfish to uncover basic mechanisms underlying epigenetics, the binding of molecules to DNA that can drive tumor growth and help cancer spread.
So, Lyko and his colleagues sequenced genomes of about a dozen marbled crayfish from different parts of the world and performed less detailed genetic analyses of two dozen more from across Madagascar. At 3.5 billion DNA bases in length, the crustacean’s genome is bigger than the human genome, but contains about the same number of genes, 21,000, they report today in Nature Ecology & Evolution.
This is the first genome of a decapod, a group of 10-legged crustaceans that includes shrimp, lobsters, prawns, and crabs, as well as crayfish. “This [work] opens the way for comparative genomics and identification of [unique features] in this group of ecological and economically important species,” says Etienne Danchin, an evolutionary biologist at the National Institute of Agricultural Research in Sophia-Antipolis, France, who was not involved with the research.
The study also “provides clues about how this genome arose and may help conservationists better track the spread of this invasive species,” Shotz says.
As suggested by some preliminary evidence, the marbled crayfish has three sets of 92 chromosomes, not the usual two, and each set is essentially a version of the chromosomes belonging to the slough crayfish (P. fallax). Two of the three sets of chromosomes are virtually identical, but the third is different enough that Lyko’s team concludes the marbled crayfish likely arose from the mating of two slough crayfish from different regions of the world thrown together in an aquarium. One must have had an abnormal egg or sperm that retained two copies of its chromosomes instead of the usual single set that is in such germ cells, Lyko explains. The bringing together of the two distant slough crayfish enhanced the genetic variation within the new clonal “species.” Such a union “would never happen in the wild,” he asserts.
Schotz isn’t totally persuaded that the genomic pile-up happened inside an aquarium, versus two slough crayfish meeting in the wild. “It is mere speculation that it originated in captivity,” he says. But the analysis of marbled crayfish DNA from across Europe and Africa, he says, ”shows that all these crayfish are clones—with identical genomes the world over.”
More important than the crustacean’s origin may be that this clone thrives in a wide variety of freshwater habitats, with different temperatures, salinities, and acidity. Clones are supposed to be at a disadvantage because they lack the genetic variation to adapt to new situations. But, “This paper suggests that an animal species can rapidly invade a large geographical area despite reproducing without sex and being clonal,” Danchin says.
The marbled crayfish’s three sets of chromosomes may be key, containing enough variety for adapting to different conditions. Danchin studies a very successful plant parasite, a nematode that reproduces asexually and also has three sets of chromosomes.
Susan Adams, an aquatic ecologist with the U.S. Forest Service's Southern Research Station in Oxford, Mississippi, agrees. Work in other organisms shows that having an extra set of chromosomes can boost the number of young and may help the clones adjust to new environments. “Greater adaptability is expected to enhance invasion success,” she says.
A further advantage, Adams says: A clone can establish a new population starting with just one individual. “It is interesting to contemplate the global, ecological implications of an exceedingly rare evolutionary event arising in someone’s aquarium.”
*Correction, 6 February, 10:20 a.m.: An earlier version of this story incorrectly stated that the marbled crayfish is the only crustacean that reproduces asexually.