The microbiome: competition or cooperation, adaptation or adaptability?

We're just now getting around to blogging about a Perspectives piece in the Oct 12 Science called "Animal Behavior and the Microbiome" by Vanessa Ezenwa et al. It's an overview of current thinking about the role microorganisms play in animal behavior.  The Human Microbiome Project documenting the extent of such organisms in humans, and the essential role these guys play in human health and disease, has found that the genes in the trillions of microorganisms with which we share our bodies outnumber ours by 100 to 1.

Since at least some of these are necessary for life, one offshoot of learning about this is to ask what 'the' human genome really is.  Most bacteria we know of, like the ones in our gut, have to do with rather prosaic, if vital, physiology such as digestion.  These are interesting and important, but they don't involve more sensitive issues such as our personal identity -- our behavior.  The role of microbes in animal behavior is just beginning to be understood, and it may be more profound than had been thought. 

Kudzu bug; Wikipedia

For example, as described in the paper, "the Kudzu bug (Megacopta cribraria), an agricultural pest, is born without any symbionts (species with which both have a mutually necessary affiliation for survival). After birth it acquires a specific symbiont from bacterial capsules left by its mother. If these capsules are removed, the bugs show dramatic wandering behaviors, presumably to search for symbiont capsules left with nearby eggs."

Or, bumble bees acquire gut microbiota either through contact with nest mates or by feeding on feces containing the microbiota required by the gut. Bees without these microbiota were more susceptible to a bumble bee parasite, Crithidia bombi. Fruit flies that share the same diet-acquired microbiota are much more likely to mate with each other than with those that don't.  And then there's the zombie ant, infected by killer fungi, and the rats -- and cat ladies -- infected by Toxoplasma gondii, both of which we described here.  The examples go on and on.

But what does the recognition that we don't go through life alone mean for the usual understanding of social context, ecosystems and the evolution of behavior?  It's tempting to suggest that these are examples of exquisitely fine-tuned co-evolution, and the usual darwinian interpretation would be that every organism is out for itself, selfishly hijacking another's gut, brain, feces, nasal passages, skin, eyes, now manipulating their behavior -- any and everything -- to make a living.  And needing to out-compete all the other microbes fighting for the same territory.  But don't get too greedy or you'll kill your host and then you're in trouble too.  (Reminiscent of how humans feel about climate change -- we have to save the planet so we can continue to exploit it ourselves.) 

But this is rather a stretch, really, and depends on fitting the facts to a preconceived view of the purpose of organismal interactions (apply our take on why people believe microbes will be found on Mars here).  And that preconceived view is that life is all about selfishness, exploitation and competition.

But there's an alternative view, and that is that what this represents is cooperation, one of the fundamental principles of life that we've often written about here and in our book MT.  It's a principle that requires abandoning the long-held belief in the primacy of "survival of the fittest" because that very rarely happens.  A better description would be "failure of the frail" -- it's only the weakest organisms that can't reproduce; most everyone else does just fine.  Plus, much of survival depends to a large degree on luck and has nothing to do with genes or competition or your ability to outwit your neighbor.

So, this Russian doll kind of life-within-life-within-life that's being catalogued is an ongoing documentation of the centrality of cooperation in life.  There's surely some adaptation going on -- the bumble bee is better off without Crithidia bombi than with, but 10-20% of worker bees in hives in the field have been shown to be infected and bees have carried on; it's only now that they're bombarded with infection with multiple parasites and more that it's a problem.  But the bee did not evolve to be infected with gut microbiota to fight off C. bombi, the bee evolved with the ability to host gut microbiota and to fight off the parasite, however that happens. 

Further, some infection was survivable, and the parasite didn't need the bumble bee because it's an equal opportunity infector, infecting other insects.  This brings up another fundamental principle of life, and that's adaptability.  Because it's ubiquitous, we believe adaptability is a characteristic of life that was present very early in evolution. So, humans can't live without a gut full of microbiota, but the species that we host are widely variable, they change when we're ill or pregnant, we can kill them off in great numbers with antibiotics, can add more with probiotics or natural exposures, and we're fine.  The same has to be true for other organisms.

One can say that what's here has to work, or at least to have worked successfully enough in the past to be here today.  But that's only a part of the biology, and there has been a tendency to focus more on how that evolved via competition, than on the interactions themselves.  How cooperation works is turning out to be an elegant but complex business.  Even if Darwinian explanations are 100% correct -- and there are reasons to temper such a view -- understanding how such things work today is in itself a challenge, and a very interesting one at that.  Though, perhaps our very interest in it is because of some microbe in our brains, that makes us sympathetic to the lives of microbes...