Fate or Feedback: is the microbiome driving our behavior?

Once upon a time there was an unsuspecting ant on the rainforest floor somewhere in Thailand. Marching along single-file between his brothers he was minding his own business, when he suddenly cocked his head and sniffed a moldy kind of smell. Thinking nothing of it, he kept on walking but soon found himself compelled to get out of line and began wandering off into the forest alone. He felt disoriented, confused, not knowing what was happening to him. 

Our tiny friend then found himself at the base of a towering leafy plant. Looking up at the massive translucent leaves he began to climb. Higher and higher he climbed up the central trunk, passing branch after branch, all the while loosing any idea of where he was or what he was doing. Once he reached a height where the air was thick with humidity he stopped climbing and began to walk out onto a leaf. Over the edge of the leaf he could see the long homeward-bound procession of his brothers far below. But before he could make another move he felt an overwhelming urge to bite down on the central vein of the leaf where he found himself perched. As he bit down he felt all the energy in his tiny body flow to the muscles in his head and mandibles and he bit harder than he had ever bit before. His life flashed before his eyes and in an instant he was dead, frozen. 

What has happened to our little ant friend?

Just a few days after the ant's demise a long grey tube began to grow from inside his head, eventually puncturing the top of his ant-skull it continued to grow into a large mushroom. As soon as the fruiting body had fully unfurled tiny spores were released from the cap and sprinkled like snow, slowly down over a fresh line of brother ants where the entire sordid tale began anew.

This is a true story. As you can see, this fungus has hijacked the ant's body turning it into a zombie of sorts, bending the ant's behavior to work exclusively for the benefit of the fungus.This is not the only example of this kind of fucked up relationship in nature. There is nematode worm that lives part of it's life cycle inside the guts of birds. When the birds poop in the jungle, ants eat the poo and with it the nematode larva. Inside the ant's stomach the nematode enters the next phase of its life cycle causing the ant's abdomen to swell and turn bright red. The round red ants look like ripe local berries to hungry birds and the cycle starts again.  Crazy!

Humans are still plagued by extreme parasites as well. The killer gut bacteria Clostridium difficile (widely known as C. diff) causes 14,000 deaths in the US annually according to the Centers for Disease Control. The extreme diarrhea symptomatic of C.diff.  can cause patients to loose a third of their body weight or more. As C.diff usually proliferates in the wake of long antibiotic regimes it is often resistant to antibiotics.  At the same time C. diff. ferociously out-competes the diversity of benign bacteria (part of the microbiome) that regularly inhabit the ecosystem inside the human gut. 

Fear not! A radically simple and effective treatment has emerged for this problem. Fecal transplants! That's right, people get so desperate when they have lost 80+ lbs and are too weak to walk they will try anything. But this shit actually works! Doctors get a "donor" to poop into a container, then they mix it up into a slurry with some water, and deliver the slurry to the colon with a colonoscopy-style tube, or... the doctors can also deposit the donor's poop slurry through a nose-tube into the stomach. I almost just barfed typing that out.  Usually the fecal "donor" is a spouse or a parent, and four out of five patients who receive this poop infusion are cured on the first go!

It is hard to think of near-fatal diarrhea as a behavior but, strictly speaking, it is. The point I want to make by bringing up C.diff infection is that a human behavior - extreme diarrehea - can be changed by a fecal transplant. A transfer of the microbial garden from one field to another can literally change the culture.

So far I have examined extreme examples of behavior modification by parasites. They are extreme in the sense that the victims pay with their lives, but what if there were a whole lot more of these relationships than we ever thought? Relationships in which the host's behavior only had to be manipulated slightly to help the parasite. What if much of human behavior is largely dictated by the the non-human denizens of our bodies? One out of ten cells making up  a person's body are actually of the species Homo sapiens. The rest? Fungus, bacteria, mites, protozoa and a whole ecosystem of diverse fauna. The question is, how democratic is the human body in decision making? Do the peptides secreted by your gut bacteria help decide what to eat, who to mate with, when to fight and when to run?

Enter Toxoplasma gondii, a protozoa that has just such subtle effects on human behavior. In an article published in the European Journal of Personality researchers report that human beings inoculated with these tiny creatures are more outgoing socially, have a higher rate of car crashes, and become less and less conscientious the longer they carry the parasite (especially men).  The shocking part of this study was the number of people who host this little bug - 22.4% of the US population over the age of 12! T. gondii is generally thought to be benign unless present in pregnant women or infants where it can cause damage to developing tissue.  The protozoa is so small during the stage of its life cycle when it lives inside humans it actually penetrates the cells, living in heart and brain tissues. As it replicates it can form benign cysts in the heart and brain... yuck!  The prevalence of T. gondii is underscored by it's signature behavioral modification - extroversion.  By rendering its host more outgoing it increases the likelihood it will spread to additional hosts. Diabolical! Are there any benefits to knowing this? could someone with chronic shyness inoculate themselves with this bug and make themselves more sociable? Might we extract the biochemical mechanism this bug uses and just make an extroversion drug instead? Who knows! Time will tell.  

To me, it is interesting to ponder how deep this connection between medical ecology and human behavior will play out. Are we, like the ant at the beginning of this story, bouncing like a pin-ball between the needs and desires of tiny creatures that call our bodies home?

By writing out these thoughts I want to get my readers thinking about behavior and the unseen factors that influence it. You know that person at work who really gets on your nerves with the constant close-talking? Maybe it's not their fault. May they're acting on a whim of one of their microbial free-riders. Maybe this is true for a lot of human traits. Will we identify more human behaviors that operate under direct feedback by bacteria? fungus? protozoa? cats? dogs? Can we "fix" people by modifying their microbial clouds? Should we? How will super-cheap gene sequencing affect social dynamics?

I do not have the answers to these questions. Maybe you do. Is this a worthy line of scientific inquiry? Share your thoughts below or find me on twitter @thorsonofodin.

Written by Kristopher Hite

1.) Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL, Billen J, Boomsma JJ, & Hughes DP (2009). The life of a dead ant: the expression of an adaptive extended phenotype. The American naturalist, 174 (3), 424-33 PMID: 19627240  

2.) Khoruts A, Dicksved J, Jansson JK, & Sadowsky MJ (2010). Changes in the composition of the human fecal microbiome after bacteriotherapy for recurrent Clostridium difficile-associated diarrhea. Journal of clinical gastroenterology, 44 (5), 354-60 PMID: 20048681  

3.) Jitka Lindová1,, Lenka Příplatová,, & Jaroslav Flegr (2012). Higher Extraversion and Lower Conscientiousness in Humans Infected with Toxoplasma European Journal of Personality, 26 (3), 285-291 DOI: 10.1002/per.838