Is sex overrated? It depends on who you ask. In the case of the asexual root-knot nematode, the answer would probably be "yes". Unlike animals such as the American cockroach and leopard shark, which are able to produce offspring asexually when the need arises, these parasitic worms have no choice in the matter – they can only reproduce without sex. While this might not sound like a life worth living, nature has given them an edge by turning them into efficient crop-killing machines that outperform their sexually reproducing cousins.

Ranked among the top five major plant pathogens in the world, root-knot nematodes are microscopic roundworms that infect the roots of more than 2,000 fruit, vegetable and ornamental crops, such as lettuce, tomatoes, strawberries and carnations, across the world. When they infiltrate a plant, they release an enzyme that causes the surrounding tissues to swell into giant cells, draining the plant's strength and leading to symptoms such as stunted growth and wilting.

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The female worms then gorge on these cells till they become swollen pear-shaped balloons before depositing their eggs in a gelatinous mass, which can contain up to 1,000 eggs. In regions such as South and Central America, they've been known to destroy entire coffee plantations, driving farmers to shift to other crops, such as sugar cane.

There are 98 species of root-knot nematodes (genus Meloidogyne) and while not all of them reproduce asexually, the most destructive ones are those that do, a development that has long puzzled biologists since these asexual worms should be on their way out the evolutionary trapdoor according to conventional wisdom about sexual reproduction.

"For a long time, the root-knot nematodes have remained an evolutionary puzzle because the most devastating agricultural parasites are those that have abandoned sex and meiosis," explains scientist Etienne Danchin of the French National Institute for Agricultural Research. "Being unable to combine beneficial mutations from different individuals and unable to purge progressive accumulation of deleterious mutations, they are expected to represent evolutionary dead ends."

Unfortunately for farmers, these asexual nematodes have proven to be a devastating exception. Not only do they cause more damage than their sexual relatives, they also infect more plants and have a greater geographical footprint. According to a study published by Danchin and his colleagues, the reason for their success is apparently hardwired in their genes.

The researchers studied the genomes of the three most damaging root-knot nematodes – M. incognita (Southern root-knot nematode); M. javanica (Sugarcane eelworm) and M. arenaria (Peanut root-knot nematode) – and compared them to a sexual relative.

According to the study, these asexual worms are likely the recent result of a series of interspecific hybridization encounters between a closely related maternal lineage and different male donors (the exact parental genealogy remains a mystery). Just like the unisexual Ambystoma salamander, these asexual worms are polyploid, meaning that unlike us they have more than two sets of chromosomes, a trait that allows them to maintain a rich genetic diversity. As the authors note, "the presence of duplicated and diverged genomic regions probably promotes functional novelty between resulting gene copies, following positive selection."

Another interesting feature in their genomes is the abundance of transposable elements, "jumping genes" that can move to different parts of the genome to cause mutations or supply new elements to protein-coding genes. The researchers suspect that these transposons could be playing a role in helping them adapt to new environments and outperform their sexual cousins. And since it takes only the female to reproduce, this could also explain why these asexual parasitic nematodes have been able to infect more hosts on a wider geographical scale.

"Their duplicated hybrid genome architectures provide these nematodes with multi-copy genes showing diverged sequence and expression patterns where their sexual relatives have very closely related alleles," says Danchin. "We suspect these multiple copies provide a reservoir to adapt to different environments and plant hosts, and constitute an evolutionary advantage over their sexual relatives (at least in the short term). Their intriguing parasitic success despite absence of sex could thus be due to their hybrid origin where they combined multiple genomes of adapted parasitic nematodes in one single species."

That said, there is much about these tiny parasitic worms that remains unknown and understanding the conditions leading to their development could help scientists breed resistant plant varieties as well as guard against the emergence of even more aggressive and devastating new hybrids, conclude the researchers.

The study was published in PLOS.

Source: PLOS via EurekAlert

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