In a paper published in PNAS in 1975, David Sloan Wilson showed that group selection can evolve in a population if it is made up of clusters of individuals that regularly interact (e.g. predation, mating, competition), and the clusters are connected through dispersal. The strength of group selection, he showed, depended on the variation in genotypes across the clusters. Based on his model, Wilson proposed that group selection and individual selection are best-viewed as two ends of a continuum along which selection operates. Forty-two years after the paper was published, I interviewed David Sloan Wilson about development of the ideas presented in this paper and his current thinking on group selection.
Citation: Wilson, D. S. (1975). A theory of group selection. Proceedings of the National Academy of sciences, 72(1), 143-146.
Date of interview: Interview conducted over email between 11th December 2016 and 12th June 2017.
Hari Sridhar: I would like to start by asking you about motivation. I read somewhere else that this work formed the entirety of your PhD thesis at Michigan State University! At the time when you joined graduate school did you already know you were going to work on group selection? What got you interested in the topic?
David Sloan Wilson: I probably have the shortest PhD thesis in the history of evolutionary biology (11 pages), but there is a back story. I dabbled in group selection when I was an undergraduate student, but went on to study optimal foraging theory and community ecology in graduate school. I was working on a normal size thesis and had several articles published or in press when I took up group selection again. Almost the entire field had rejected group selection but my simple algebraic model showed otherwise and the import was not lost on me. I boldly approached Edward O. Wilson to sponsor my article for the Proceedings of the National Academy of Sciences, which he did, after sending it out for review. When it came to redefining my thesis topic, my PhD advisor reasoned that what was good enough for E.O. Wilson and PNAS should be good enough for a thesis. My other articles on optimal foraging theory and community ecology were published (and one on the adequacy of body size as a niche difference became a citation classic) but were not part of my thesis.
HS: Stepping back a bit, could you tell us how you got interested in ecology and evolution? You say you dabbled a bit in group selection during your undergraduate years. Could you tell us when and how did you first become aware of the idea of group selection? Also, would you remember how you came back to it during your PhD, i.e. what was the trigger for the renewed interest?
DW: My father – Sloan Wilson – was a famous novelist, which might explain my interest in writing and exploring the human condition. As a boy, however, it was too daunting to follow in his footsteps, so I decided to become a scientist. I loved nature, so as soon as I figured out that I could be an ecologist and spend my time outdoors rather than inside a laboratory, I was hooked. I made this decision by my 2nd year in college at the University of Rochester in New York. I was a poor student in lecture courses but was lucky to be mentored by Dr. Conrad Istock, and I thrived assisting his research on mosquitoes that live in pitcher plants and doing independent study projects on feeding and vertical migration in zooplankton. The historically separate disciplines of Ecology, Evolution, and Behavior were becoming integrated during this period, so I learned all of them at once. In Conrad’s lab I started to read the primary literature and enter into discussions with faculty and grad students. I read Animal Dispersion in Relation to Social Behavior by V.C. Wynne-Edwards, who had become a lightning rod as a proponent of group selection. One of his ideas was that vertical migration was a group-level adaptation in zooplankton. The details need not concern us, but I knew that zooplankton spatial distributions were highly patchy, both horizontally and vertically, so that group-level selection should not be dismissed out of hand. Nevertheless, it was only one interest out of many so I turned my attention to other topics. In graduate school at Michigan State University (MSU) I started to build mathematical models that could be applied across taxa. An article on vertical migration in zooplankton prompted me to dust off my old ideas, so I built a simple algebraic model of selection within and among groups in a multi-group population. My key innovation was to define a group as the set of individuals that influence each other’s fitness with respect to the expression of a given social behaviour, which I called a trait-group. This was implicitly how groups are defined in most models of social evolution, but I made the assumption explicit.
HS: Who were the people you were discussing these ideas with? Among the people you acknowledge, you have already discussed the roles of Conrad Istock and E.O Wilson. Could you also tell us more about the contributions of the others – E.E. Werner, D.J. Hall, G.C. Williams, H. Caswell, FM Stewart, B. Levin and the Ecology group at MSU?
DW: I went to MSU intending to be an aquatic ecologist. My thesis advisor was a Donald J. Hall. He was a free spirit and gave me free rein to explore ideas. Although MSU is large, I interacted primarily with a small group of young faculty members and their students, including Earl E. Werner, a postdoc, and Hal Caswell, a fellow grad student. Both would go on to distinguished careers. The small group dynamic led to a lot of independence, which I thrived upon. We were fearless about breaking new ground. George C. Williams was the main person associated with the rejection of group selection, based on his book Adaptation and Natural Selection (1966). On my way to visit E.O. Wilson (as I described earlier), I made a detour to visit Williams at the State University of New York at Stony Brook. As I remember the encounter, I strode into his office and said “I’m going to convince you about group selection!” and he offered me a post-doctoral position on the spot. That was the beginning of a lifelong friendship among intellectual opponents. He was a wonderful man. Frank M. Stewart and Bruce Levin were the two people that E.O. Wilson called upon to review my manuscript for the Proceedings of the National Academy of Science. Both signed their reviews so I acknowledged them in the article.
HS: Would you remember how the paper was received when it was published? Did it attract a lot of attention and discussion in academia?
DW: The main reaction that I remember is “Yes, but…” – Yes, but it shouldn’t be called group selection. Yes, but it’s only a model. Anything to avoid concluding that group selection might be plausible after all!
HS: This paper has been cited nearly 1000 times. At the time when you were doing this work, did you anticipate at all the kind of impact it would have on the field? Do you have a sense of what it, mostly, gets cited for?
DW: I kept a detailed journal back then so I don’t need to rely on my memory. I thought that it would be earthshaking, so much that I questioned my own judgement, since I’m prone to feeling euphoric over new ideas. I kept asking myself: “Is this just me being euphoric, or is it as important as I think it is???” However, I did not anticipate the amount of time it would take to become accepted.
HS: How did this paper influence the future trajectory of your research, both in the short-term and the long-term? What kind of impact did it have on your career?
DW: With the publication of this article, multilevel selection became the “main event” of my career. I followed it with a much longer article in The American Naturalist in 1977 and my first book, The Natural Selection of Populations and Communities, in 1980. I started to do empirical research in addition to theoretical models, resulting in publications all the way up to my most recent book, Does Altruism Exist? in 2015. At the same time, I did not lose interest in other topics. Even as a graduate student I was thinking about human mentality as an evolutionary process and regarding these thoughts as equally or more important than my thoughts on group selection. With my wife, Anne B. Clark, I pioneered the study of personality in non-human species, which has grown into a very hot topic. Evolutionary theory is a passport to all subjects, and I have used my passport to travel widely!
HS: Today, 42 years after the paper was published, could you reflect on where you stand with regard to its main conclusion?
DW: Although the word “paradigm” is overused and also used too often for self-serving purposes, there is something about Multilevel Selection Theory (and therefore the article) that counts as paradigmatic, compared to other theories of social evolution. Its logic of making a nested series of relative fitness comparisons (between genes within individuals, between individuals within groups, between groups within a metapopulation, etc.) is simple and intuitive once you get the hang of it, but can appear mystifying from other theoretical perspectives that account for evolutionary change in other ways, such as averaging the fitness of lower-level units across higher-level units. Please consult the chapter of Does Altruism Exist? titled “Equivalence” for more on this topic.
HS: What according to you has been this paper’s most important impact on the field of evolutionary biology?
DW: Along with a few other publications, notably by George Price and W.D. Hamilton, it marked the beginning of the revival of Multilevel Selection Theory in evolutionary biology. In plain language, it shows how adaptations can evolve at any level of a multi-tier hierarchy, from genes to ecosystems. This is in stark contrast to the view that adaptations only exist at lower levels such as individuals or genes. By the way, the cloud of ambiguity over whether individuals or genes count as the “fundamental” unit of selection is one of many confusions easily resolved by MLS theory.
HS: Have you ever read the paper after it was published? If yes, in what context?
DW: I seldom had cause to read the paper but recently did so, along with my old journals, in the context of a documentary that is being filmed of my work. In retrospect, I am struck by the innovation of the trait-group concept— the idea that a single randomly mating population (a deme) can consist of multiple groups as far as the expression of traits is concerned. Before then, the groups of group selection theory were assumed to be separate demes.
HS: Would you count this as one of your favourites, among the papers you have published?
DW: Papers are like children! They are all special in their own way!
HS: What would you say to a student who is about to read this paper today? Would you guide his or her writing in anyway and point him or her to subsequent papers they should read along with this? Would you add any caveats?
DW: So much has happened with the development of Multilevel Selection Theory that my 1975 paper is NOT the way to start! A student should begin with my most recent book, Does Altruism Exist?, and proceed from there, reading my 1975 paper for a sense of history. Thanks to you for providing a sense of history with this interview.