Who benefits?

There's an interesting idea from evolutionary theory called the cui bono principle.

Cui bono? is Latin for "who benefits?"  It started out as a legal concept; if a crime has been committed, and you're looking for the suspect, find out who benefitted.  That, very likely, will get you on the right path toward solving the mystery.

Cui bono in the evolutionary model has to do with explaining odd phenomena that seem to have no obvious underlying reason -- or which even induce organisms into self-destructive behavior.  One common example is the strange situation where certain ant species crawl up to the tops of blades of grass and basically just wait there to be eaten by herbivores.  It turns out that the bizarrely suicidal ants are infected with a parasite called a lancet worm that needs to complete its life cycle in the gut of a herbivorous mammal, so it damages the brain of the ant in just such a way as to turn its sense of direction upside down.  The parasitized ant then crawls upward instead of downward to safety, gets eaten -- and the lancet worm, of course, is the one who benefits.

Another, even creepier example, is Toxoplasma gondii, which I wrote about here at Skeptophilia a few years ago.  I encourage you to go back and read the post, but the upshot is this parasite -- which by some estimates infects half of the human population on Earth -- causes different symptoms in its three main hosts, cats, rats, and people.  Each set of symptoms is tailored to change behavior in very specific ways, with one end in mind; allowing the parasite to jump to its next host.

I just found out about another very peculiar (and convoluted) example of cui bono just yesterday, this one involving rice plants.  Many plants, it turns out, have pheromonal signaling, releasing chemicals into the air that then trigger responses in neighboring individuals, either of their own or of different species.  Acacia trees that are browsed by herbivores, for example, emit a signal that triggers nearby trees to produce bitter tannins, discouraging further snacking on the leaves.  Well, it turns out that rice plants have an even niftier strategy; attacked by insect pests, the rice plants emit a chemical called methyl salicylate (better known as oil of wintergreen), which attracts parasitoids -- insects like chalcid wasps that attack and kill the offending pests, usually by laying an egg in or on them and allowing the larvae to eat the pests for lunch.

Okay, but this has yet another layer of complexity, because there's a different set of organisms that have another take on cui bono.  Rice are subject to a group of plant viruses called tenuiviruses, which cause rice stripe disease, weakening or killing plants and severely reducing crop yield.  Tenuiviruses are spread by insect pests like planthoppers, which (much like mosquitoes with malaria, dengue fever, yellow fever, and chikungunya) suck up the sap of infected plants and the virus along with it, move on to an uninfected host, and spread the disease.

Rice stripe tenuivirus [Image credit: A. M. Espinoza]

And new research has found that the tenuiviruses, once in an infected plant's tissues, suppress the plant's ability to produce methyl salicylate.  The result?  The plant can't send a signal to the parasitoids, the planthoppers multiply, and the disease spreads.

The authors write:

[R]ice viruses inhibit methyl salicylate (MeSA) emission, impairing parasitoid recruitment and promoting vector persistence.  Field experiments demonstrate that MeSA, a key herbivore-induced volatile, suppresses vector populations by attracting egg parasitoids.  Viruses counter this by targeting basic-helix-loop-helix transcription factor OsMYC2, a jasmonic acid signaling hub, thereby down-regulating OsBSMT1 and MeSA biosynthesis, responses conserved across diverse rice viruses and vector species.

So once again, we have a parasitic microorganism that is engineering a response in its host that makes it more likely to be passed on, in this case by preventing the host from calling for help.

This kind of strategy brings Tennyson's observation that "nature is red in tooth and claw" to new heights, doesn't it?  Makes you wonder how many other examples there are out there of behavior being manipulated by parasites.  Further evidence that evolution is the Law of Whatever Works -- even if Whatever Works is kind of unsettling.

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