Reconciling the Hologenome

There have been a couple of rounds of back and forth in print and online (here, here, here, here, and some shameless self promotion here and here...among multiple other places over the years). There is apparently an mBio special series starting today that teases a "heated discussion" akin to discussion about the neutral theory.

I don't have skin in this game (yet), and have tried to see and understand the points from both "sides". I lean towards the view in the Douglas and Werren paper, but I also see value in ascribing names to concepts. Yes, there are actually valid points on both sides. However, I'm starting to get frustrated by the whole discussion simply because I can't see a reasonable goal to work towards, and to me it seems as though both sides are starting to talk past one another. I won't go too much into it in this post, but I'll try and describe how I see the crux of the disagreement. It makes sense in my own head, but apologies in advance for what I get wrong.

It seems to me that many on the "anti-hologenome" side (for lack of a better word) seem to argue that we have all the models we need right now to get to the heart of interactions between hosts and microbiomes. They point towards GxE, GxGxE, multi-level selection, etc...and cite papers showing that these topics can be dealt with using the tools available. Why invent another term? I feel the frustration that these researchers have because (disclaimer, again this is IMO right now and can change if I'm presented with a great argument or explanation) the holobiont/hologenome concept has some important internal inherent disagreements. To illustrate, I've seen multiple "pro-hologenome" folks say that the utility of the hologenome lies in being able to describe natural selection acting at the level of the host+microbiome. That there is some value added by considering these two entities together. That's all well and good, but if you define the hologenome in terms of selection than there isn't any good way to fit neutral microbes into this worldview (because selection won't affect them). It's an internal inconsistency that Seth Bordenstein has already tried to convince me doesn't exist. All I'm saying, you can't point towards being able to describe selection better as a holobiont (and have this be the main example of why the concept is useful) and then include subsets of the microbiome that are neutral.

To me, the "anti-hologenome" side wants to see the hologenome concept as something that can be a predictive tool for modeling species interactions. The concept is certainly not there yet and I'm not sure if that's really where it's meant to go (see below). The holobiont definition gets a bit fuzzy when you push the limits as many on the "anti" side seem to want to do. Where does it end? What microbes are included? What about non-microbes that are vertically transmitted? The answers may be available, but I haven't seen a clear articulation of this anywhere (sorry Seth). I *think* much of the "anti" side frustration stems from not having clear/crisp enough definitions of the terms involved or the situations where the hologenome concept may apply. Not clear enough for predictive modeling purposes anyway.

Like I said above though, there is value in the hologenome concept writ large! If you squint your eyes and take the 30,000ft view, it's great to have a term that describes natural selection acting at levels greater than single organisms. We can use these terms for public communication of why microbes and microbiomes are important and not to be feared. We can use these terms to capture the imagination of burgeoning scientists or those outside of the fields that we work in. The utility of the holobiont concept is about communication and you don't need to get deep in the details for this to be true. We do actually need another term and another way to explain things like GxGxE and multilevel selection because the older terms aren't cutting it. We don't need a holobiont concept to create new ways to model multi-level selection, but I don't think that's ultimately what it's for.

That's how I see it, and I'm firmly trying to straddle both sides.