Coevolution and the Microbiome

Coevolution is defined as cases where two (or more) species RECIPROCALLY affect each other's evolutionary dynamics. Reciprocally is highlighted in every way that I possibly could in the preceding sentence because this aspect really is key. It's a difficult concept to get a grasp on and an even more difficult concept to actually test in nature. I don't want to spend too much space going over the ins and outs of coevolution because numerous people that are smarter than I am have done that in accessible ways...My favorite being Dan Janzen's "When is Coevolution". (For other good lists that are slightly longer and more intense, see Scott Nuismer's or John Thompson's Google Scholar page). I'm missing a bunch of other stuff out there, but it's late so please forgive me and add any other great links in the comments.

I mention this because there is a lot of work being published on microbiomes right now, and I'm sensing a pretty strong tendency across manuscripts and presentations to state that microbiomes and their hosts have "coevolved". In some cases this is certainly true (best examples I can think of off the top of my head are nutritional symbionts in insects, some nodulating Rhizobia in legumes, Plasmodium in humans, and Vibrio-Bobtail Squid). Here's where it gets fuzzy, and I'm largely focusing on human microbiome studies here because they often get all the press...in many cases where researchers claim that microbiomes and hosts have "coevolved" there is absolutely no evidence that this has happened. Sure, there are trends and correlations that make it seem likely that coevolution has taken place. However, read the Janzen piece above again and find me a study where researchers have reciprocally tracked genetic changes in the microbiome and have seen direct evolutionary (read:heritable) changes in human host populations. It's nearly impossible (let alone ethically challenging) to track fitness in human populations over time and cleanly and directly relate those to changes in the microbiome. Codiversification != coevolution, so any story that mentions Helicobacter pylori and humans is pretty much right out (h/t to Jonathan Klassen for that one). Moreover, health != fitness. By definition, obese people are unhealthy yet they can still have kids at a decent clip (note, I'm unaware of studies actually measuring the fitness affects of obesity in humans but would love to hear about them if you know of any). Likewise, much has been made about H. pylori affecting human health negatively through gastritis/gastric cancers and positively through asthma/GERD prevention. I'd love to hear how these things directly affect fitness in human populations, but there's absolutely no data to these points. Proto-humans might well have had gastric problems from H. pylori, but I'm betting that there were many other things that directly impacted their lifespans and fitness with greater magnitude. Please don't get me wrong, I'm not saying that it's impossible that humans and their microbiomes have coevolved, I'm saying that there is no direct evidence that directly addresses the hypothesis of coevolution outside of a handful of pathogens.

All of this is a roundabout way of saying that studying (and demonstrating) coevolution is really really really difficult. You need to actually measure how species 1 directly influences evolution in species 2 AND how species 2 then directly affects evolution of species 1. Reciprocality is key. There are many examples where species 1 influences some trait on species 2, but that doesn't mean that evolutionary dynamics in species 2 will be affected. Likewise, it doesn't mean that species 1 will then be reciprocally affected by this trait change.  Moreover, we don't have good models of host-microbiome coevolution because the math is difficult/complex so we therefore don't have very clear ideas about what parameters matter most to drive coevolutionary dynamics. One of my near to mid term goals in science is to try and change this, so as a first step I'm trying (fingers crossed) to organize a workshop at NimBios (probably in Fall 2016) to bring 35ish smart people from across the globe together to talk about how we begin to frame questions about host-microbiome coevolution. If you're interested please fill out the form at the following link: http://goo.gl/forms/G79CwnhYc8

I'll be submitting a workshop proposal by March 1st, and will keep you up to date on what's happening. If you're curious about NimBios and workshops, overview can be found here: http://www.nimbios.org/workshops/