I could keep going on what an individual is, but at least at this point I have put out the main points I have been thinking about. It may be a subject we will return to in the future. What I really should talk about a bit is our recent paper, “Site-specific group selection drives locally adapted group compositions” (Pruitt and Goodnight, Nature 514:359–362).
I am actually a bit surprised that it has gotten so much positive press with so little backlash. But with a very few exceptions we are not being dismissed. I guess times have changed. I am actually not so much going to describe the study so much as talk about what we demonstrated and why it is in actuality a fairly small step.
First a disclaimer: This is John Pruitt’s project. I was honored when he asked me to participate in the analysis of the data, and sometimes I am not sure I did a lot more than provide cover so that he could talk about multilevel selection.
As with all science, this study is but a small step in a long line of studies.
The reason for that long-winded preamble is that in reality we did a relatively small thing. First some history. It has long been demonstrated that there were serious flaws in the reasoning of theoreticians dismissing group selection (Wade 1978, Quart. Rev. Biol. 53:101-114 – this paper is remarkable in how prescient it is given that it was published nearly 40 years ago). At the same time Wade was also doing the first studies showing that group selection worked in the lab (Wade 1977 Evolution 31:134-153). Later studies would demonstrate that indeed Wade had been correct in his quarterly review article: group selection could act on interactions among individuals in a way that simply was not available to individual selection (see Goodnight and Stevens 1997 Amer. Natur. 150:S59-S79), and a series of selection experiments led to the wide-spread adoption of group selection as a means of live stock improvement (e.g., Muir 1996 75:447-458). Thus, by this time we really have answered the early questions: In the lab group selection works, and it works so well because it can act on interactions among individuals. The next question was whether group selection IS acting in nature. The methodology for this was brilliantly provided by Heisler and Damuth (1987 Amer. Natur. 130:582-602), and promptly ignored. Fortunately, in recent years this method has been rehabilitated, and shown to work both in theory and in action. The results of these efforts is that, although not enough cases have been examined, it is pretty clear that group selection is at least not uncommon. To give you some idea about how common it might be, (1) recognize that theoretically we can show that soft selection is a mixture of group and individual selection (Goodnight, Schwartz and Stevens 1992, Amer. Natur. 140:743-761), (2) the constant yield law (Weiner and Freckleton 2010 Ann. Rev. Ecol. Evol., & Syst. 41:173-192) is almost universal in plants and (3) the constant yield law is a form of soft selection. Thus, group selection may indeed be extremely common in nature.
So, in some sense the main questions are answered: The models were wrong, group selection works, and it may be very common in nature. What was missing is that up to this point we did not actually have an example of an adaptation that was unequivocally a result of group selection. That is what Pruitt and Goodnight provided. This is no small feat. Consider how many solid examples we have of adaptation due to individual selection. There are a lot of traits that almost certainly are, but have never been demonstrated to be individual level adaptations. Examples of these are things like our hearts. Clearly an adaptation, but has it ever REALLY been demonstrated to be so? The examples we do have are few and far between, and all represent a huge amount of work on somebodies part. I am thinking of examples like the evolution of lead tolerance in grasses (Antonovics and Bradshaw 1970 Heredity 25:349-362) peppered moths (Kettlewell and later Majerus), and beak size in Galapagos finches (Peter and Rosemary Grant).
Social spiders have a group level adaptation that is the proportion of the colony that is aggressive vs. the proportion that is more docile. Populations have evolved to display a mix of these two proportions that is apparently optimal for their local environment. When the distribution is experimentally adjusted it always returns to the evolved ratio regardless of the environment in which they are raised. By the way, this strikes me as grasshopper hell. (From http://www.readcube.com/articles/10.1038/nature13755 — this is a nice writeup by Tim Linksvayer. I recommend it if you have not already seen it.)
Notice that in the cases where we have good evidence of evolution by natural selection there is environmental variation. In the case of lead tolerance there are mine tailings such that soils with high lead content are adjacent to pristine land lacking the metal. In the case of the moths and birds there is sufficient data over a long enough period of time that we can see adaptation occurring as the environment changes. Pruitt’s spiders were closer to the mine tailings scenario. That is there were different local environments that had different optimal mixtures of spider behaviors, and we were able to show that the spiders are locally adapted, and regardless of the environment we placed them in, they always adjusted their colony to reflect the adaptive mixture of behaviors in the environment they evolved in. Thus, Antonovics and Bradshaw were able to show that “normal” plants were unable to grow well in lead poisoned soil, we showed that spiders are unable to adjust their mix of behaviors when placed in the “wrong” local environment.
In reality, then, that is all we really did. We showed that these spiders have a group level adaptation to local conditions. Since it is a property of the group that cannot be meaningfully measured on individuals, it really is a group level adaptation, and since it is non-plastic it is a heritable change. This is the last of the qualitative issues to be addressed about group selection. Group selection works in theory, group selection works in the lab and in agriculture, we see group selection in nature, and now we know that group selection leads to adaptive change in nature. What is left is to work out the quantitative questions, such as how common is group selection relative to lower levels of selection, under what circumstances is it sufficiently powerful (and traits sufficiently heritable) that it leads to adaptations that can be attributed to evolution by group selection.