Parasitic Worms Might Manipulate Insect Behavior Through ‘Borrowed’ Genes

Adult horsehair worms, aptly named due to their long, noodle-like appearance, inhabit aquatic environments. They reproduce in water, yet their offspring only mature within the bodies of various animals, often terrestrial insects like praying mantises. When these parasites have fully developed inside their unwitting hosts, they face the peculiar task of compelling their hosts to drown themselves to fulfill their life cycle. The exact method through which these parasites manipulate their hosts has confounded scientists for a long time. However, the researchers of a recent study, published in Current Biology, propose that horsehair worms possess a multitude of genes that enable them to control a mantis’s movements. Intriguingly, these genes might have been acquired directly from their unfortunate hosts.

“The results are amazing,” remarks Clément Gilbert, an evolutionary biologist at the University of Paris-Saclay, who was not part of the study. If indeed it is confirmed that a substantial portion of the mantises’ genes made the leap to the parasitic worms, a phenomenon known as horizontal gene transfer, then, as he notes, “this is by far the highest number of horizontally transferred genes that have been reported between two species of animals”

The eerie phenomenon of parasites manipulating their hosts into self-destructive behavior has long captivated Tappei Mishina, an evolutionary biologist affiliated with Kyushu University and the RIKEN Center for Biosystems Dynamics Research. He notes that “For more than 100 years, there have been horrifying observations of terrestrial insects jumping into water right before our eyes all over the world”

Collaborating on the endeavor, he joined forces with ecologist Takuya Sato from Kyoto University’s Center for Ecological Research to delve into the genetic underpinnings of this parasitic behavior.

Their research was centered on horsehair worms, a category of parasitic creatures with close ties to nematodes. This particular group often follows intricate life cycles that encompass multiple hosts. Those residing in freshwater typically require an insect host to complete their transformation into adults. The scientists’ attention was drawn to the Chordodes genus, specifically known for its parasitic relationship with mantises. Within the relatively compact confines of these palm-sized insects, these worms can grow to lengths approaching one meter.

The process through which these worms coerced their hosts into self-destructive water dives had remained shrouded in mystery. “The mechanism was a complete mystery,” noted Mishina. With the assumption that the worms might be manipulating the mantids’ brains, the research team delved into sequencing messenger RNA (mRNA) – the molecules responsible for conveying instructions for protein production when a gene is active. This sequencing was conducted on both the parasites and the mantids’ brains, both before and after these insects submerged themselves.

In total, the research uncovered over 3,100 parasite genes that experienced heightened activity during their manipulation of the hosts. What’s astonishing is that more than 1,400 of these parasitic genes bore a striking resemblance to genes found in the mantises they infested. This implies that this particular cluster of genes had made an unconventional journey from the host’s genetic code to the parasite’s genome, a phenomenon known as horizontal gene transfer. “At first, I couldn’t believe the results and double-checked for errors,” Mishina recalls. “I was genuinely amazed by the sheer number of transferred genes.”

The phenomenon of horizontal gene transfer remains somewhat enigmatic. While viruses, mobile genetic elements, and a few other mechanisms are believed to play a role, the process has been largely shrouded in mystery. Previous instances of gene transfer have typically left behind ambiguous clues. In the case of the worms, certain transfers seemed to have occurred in the distant past, leading to a divergence of 5% or more between the worm and mantid sequences. However, other instances revealed nearly or completely identical sequences, indicating that these gene transfers were comparatively recent.

Jeff Doherty, a postdoctoral fellow delving into host-parasite interactions at the University of British Columbia, points out that the results are intriguing. However, he highlights that the researchers have not definitively eliminated another potential scenario: that the mantids might have acquired these genes from the worms instead.

The researchers acknowledge the possibility that the gene sequences could be a result of mantis tissues contaminating the worm samples. Nonetheless, Mishina underscores that they discovered RNA resembling mantis genetic material in adult worms that had been isolated in water for a period of up to 3 days, longer than typical contaminant RNA longevity. Furthermore, the researchers point out that the variations in many of the mRNA sequences wouldn’t align with what’s expected in a contamination scenario.

Even if the worms did acquire genes from the mantids, it remains uncertain how these genes could influence the mantids’ behavior. One possibility is that the worms’ proteins might imitate those of their hosts, effectively allowing them to take control of the mantids’ bodies by triggering behavioral patterns that serve their purposes. Jeff Doherty, a postdoctoral fellow studying host-parasite interactions, suggests that “Protein mimicry may only be a part of the puzzle here.” In essence, this research marks just the beginning of a complex and intricate exploration into this phenomenon.

The sheer quantity of potentially transferred genes is astounding, according to Gilbert. However, he believes the authors could have undertaken further steps to eliminate contamination as a possibility. He notes that in the past, remarkable claims of extensive gene transfers have later been debunked. Mishina’s team is actively engaged in sequencing the complete genomes of both the worms and mantises. This is a step that Gilbert and Doherty deem necessary to resolve any doubts about contamination and to provide answers regarding the direction and timing of these transfers. Gilbert expresses his desire to believe it’s true, as it would be an astonishing scientific revelation.

Resources

1. ^DATASET Wilcox, C. (2023). Parasitic worms may control minds of insects with ‘borrowed’ genes [Dataset]. In AAAS Articles DO Group. [Science]
2. ^JOURNAL Mishina, T., Chiu, M., Hashiguchi, Y., Oishi, S., Sasaki, A., Okada, R., Uchiyama, H., Sasaki, T., Sakura, M., Takeshima, H., & Sato, T. (2023). Massive horizontal gene transfer and the evolution of nematomorph-driven behavioral manipulation of mantids. Current Biology. [Current Biology]