More on fitness assignments and individuality

In my last post I briefly mentioned that the level at which fitness is assigned is an interesting problem, but not a conundrum, or a serious conceptual issue. I think it would actually be quite useful to expand on this. The basic ideas came out of discussions I had 20 some odd years ago separately with Lorraine Heisler and John Damuth over a series of years. Heisler and Damuth took this one direction (Group Selection 1 and Group Selection 2), and I went in another direction, which involved not publishing anything until my Chapter on “defining the individual” (Goodnight 2013, Chap. 2 in “Defining the individual” Bouchard & Hueneman eds).


working hard in the forest

In case you were wondering where I was, I was working hard in the Amazonian flooded forest. (I was at the Uakari lodge. I recommend it if you are ever in the Manaus area. )

So here is the basic issue: Biological things tend to be organized hierarchically. This need not be the case, but it often is. Thus, we have cells, which group together, possibly with other species, to become organisms – yes, it is probably incorrect to think of “humans” as a single species – which group together to become populations or groups, which finally group together to become communities.

Using the most basic definition of evolution: the change in the distribution of a set due to the gain or loss of members of that set, it should be clear that it is possible for evolution can take place at any of these levels. By the way, I use this very clutzy definition of evolution here to avoid using terms like “individual” and “population”. Normally this is not a problem, but in this particular circumstance we need to be very careful. The point is that change occurs, and it can be potentially defined as evolution. However, at least for selection, it can only be defined as evolution by natural selection if there is variation in fitness. Here is the problem. Contextual analysis, and I would argue human understanding, really only allows fitness to be defined at a single level.

Herein lies the issue. We can choose to define fitness at any level. Different levels may be better choices than others, but ultimately, the level at which we assign fitness is an arbitrary construct of the investigator. I would argue that once we have assigned fitness at any particular level, that becomes the “member” of the set in our definition of evolution.   In other words, when we define fitness as occurring at a particular level, we are in fact defining the individual in the less clutzy definition of evolution: Change in the distribution of a population due to the gain or loss of individuals.   Even though we really only need to define fitness with regard to selection, and adaptation, it makes no sense to have concepts of individuality for mutation, migration and drift that are different than our concept for selection. Thus, the I would argue that logically the level at which we define fitness defines individuality for all evolutionary forces acting on that trait.

Of course, the level at which we define fitness does not alter the changes that occur in the organism. The changes that occur are independent of human observation. What DOES change, however, is our interpretation of those changes. Only changes at or above the level of individuality—the level at which we assign fitness – can be interpreted in an evolutionary framework. Certainly for adaptation, we can only interpret changes as being due to natural selection if there is variation in fitness, and there is no variation in fitness below the level at which we assign fitness. So, what we do is we call those changes that occur below the level of individuality as something else. For example, we typically we assign fitness at the level of the organism, and changes within the organism are called “development”. However, were we to choose to assign fitness at the level of the cell we could reasonably call these changes evolution, and view differential cell division and mortality as selection.

This idea of the relativity of individuality, and the role of the observer in interpreting the nature of changes is at the heart of the problem that people have with Group Selection 1 and Group Selection 2.   This is also why I am not a big fan of the GS1/GS2 terminology. Basically, I think we would be better served by stating the level at which we define fitness. Thus, we might say “In this study we define the organism to be the individual”, or “we assigned fitness at the level of the colony in this study”. I think this is clearer and removes a lot of ambiguity. For example, consider a hypothetical study of Tasmanian Devil Face Cancer. This potentially has three or more levels at which we could assign fitness, including the cell, the organism, the population, and potentially the species. Defining the level of the individual has the flexibility to handle this GS1 and GS2, just gets difficult (if we assign fitness at the level of the species is that GS4?)

The problem, of course, is the idea that there is this desire to have the “individual” be a natural unit, and to have “development” qualitatively different than “evolution”. The idea that the individual is a construct of the observer is really not compatible with these thoughts. That said, I am quite comfortable with the arbitrariness of the level at which we assign fitness. I see no other way that we can have transitions of levels: There really is no qualitative difference between the most organized colonies and the least organized organisms (compare Volvox to Trichoplax). It is also the only way we can study cancer as evolution, and not have to assign fitness at the level of the cell when we are studying, say, foraging behavior. Nevertheless, I understand that many will find this deeply disturbing, and many will reject this relativity of individuality as a viable world view. That said, I think if you can get your head around it, it will help you in understanding multilevel selection.

Volvox-aureus-DF trichoplax

Volvox (left) is considered to be a colonial protist, whereas Trichoplax is considered to be a single organism and an animal. There are differences in their structure, but the differences are not great considering that one is a colony of cells and the other is multicellular organism. (Volvox:, Tricoplax: )

I am out of space, but as I mentioned above, although the level at which we assign fitness is, in my view, arbitrary, there are nevertheless better and worse levels that we can choose. For example, often there is a reasonable a-priori choice. Higher organisms are made up of trillions of cells. It would be a ridiculous, and probably impossible, task to assign fitness at the level of the cell if we are studying morphology or behavior at the whole organismic level. Other times, contextual analysis can be used to identify the lowest level at which selection on a particular trait is acting, and that level becomes a reasonable one for assigning fitness. Still other times there may be adaptations (policing, mitosis) that minimizes adaptation by natural selection at lower levels. In this case it makes sense to assign fitness at the level at the lowest level that a response to selection is likely to occur. Finally, at the beginning, I mentioned that MLS works fine if groups are not nested. However, any study with non-nesting groups will only work if fitness is assigned at a level that is fully encompassed within all higher groups. For example in a continuous population of plants every organism (ramet?) can be considered to be at the center of its own neighborhood. Obviously these neighborhoods overlap. Nevertheless MLS analysis will work as long as fitness is assigned at the level of the organism instead of the neighborhood.

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