In a paper published in The Quarterly Review of Biology in 1975, Mary Jane West-Eberhard reviewed the literature on kin selection and outlined “social, ecological and developmental factors” that might influence the evolution of beneficial social interactions. West-Eberhard was motivated to write this paper because she felt that there was too much emphasis on the degree of relatedness in discussions of kin selection. This emphasis, she felt, led to the mistaken impression that a high degree of relatedness is required for kin selection to operate. Through this review, West-Eberhard demonstrated that kin selection could also be important in social interactions between individuals that were not closely related. Forty-one years after the paper was published, I asked West-Eberhard about the making of this paper, its impact on kin selection research, and what we have learnt since about this topic.
Citation: Eberhard, M. J. W. (1975). The evolution of social behavior by kin selection. The Quarterly Review of Biology, 50(1), 1-33.
Date of interview: Questions sent by email on 16th November 2016; responses received by email on 7th May 2018.
Hari Sridhar: At the time when you published this paper in 1975, you had already worked on wasps for a long time. Which came first – an interest in wasps or in the theoretical aspects of sociality?
Mary Jane West-Eberhard: Well, not really a very long time, but this is difficult to disentangle. Because of their lively and alert behavior, I liked wasps better than any other insect when I did an entomology project as a member of a 4-H Club (a club mainly for rural kids, though I lived just outside of a small town, not on a farm), in secondary school. But I did not study them until needing to choose a thesis topic as an undergraduate zoology major (1962), and I decided to do observations on Polistes. But I was already very interested in evolutionary biology and social behavior, and my main first-hand experience the behavior of insects (e.g., a social cricket given to me by Richard Alexander one summer; my first paper was (with Alexander) on the sub-social behavior of that cricket – first draft written by Alexander, based on my observations. So I can’t really say whether a SCIENTIFIC interest in theory or wasps came first.
HS: More specifically, what was the motivation to write this particular paper in 1975? Would you remember when you read Hamilton’s papers for the first time?
MJW: I first read Hamilton’s papers while in the field in Colombia S. America (1964-65), working on my doctoral research (a comparison of Michigan temperate-zone Polistes and the two species I was observing in Colombia. Copies of Hamilton’s papers (on smooth pre-Xerox paper with purplish print) were mailed to me by Alexander while I was in the field in Colombia, and their importance was obvious especially since he referred explicitly to tropical Polistes. My thesis, written in 1966, described the first field test of kin selection theory and discussed how kin selection might explain various aspects of Polistes behavior, some of them mentioned by Hamilton in general terms (e.g. philopatry) and some not (e.g. dominance and subordinance behavior). So, thanks to Alexander I was thinking about kin selection as soon as Hamilton’s paper appeared, and began corresponding with Hamilton a couple of years later.
HS: In the Acknowledgements, you say that this paper began as a joint effort between you and Richard D. Alexander. Could you give us a sense of how this collaboration worked – how did it start, did Professor Alexander and you meet often to discuss ideas, where was most of this work done etc.? Also, if you don’t mind my asking, how come Professor Alexander wasn’t an author on this paper?
MJW: I think it was Dick Alexander’s idea to do a paper together on kin selection but I don’t remember the exact year –maybe about 1970. I had already written about kin selection and the evolution of social behavior, and this was to be his first on the general topic and he thought it would be rewarding to do it together. He was very interested in parental manipulation of offspring and convinced that the parents would always win. I was not convinced of that, and was unwilling to accept Alexander’s arguments on that question. I thought we had to figure out how to specify the conditions when parents would win, and when offspring would prevail. Also, I had some other ideas that did not interest him very much. I was the one who decided to do my own paper rather than a joint one, and it was a difficult decision for me (after all he was my doctoral advisor and had far more publishing experience, and I respected him a lot). But he himself had always encouraged independent thinking and debate. We continued writing on our own and I submitted my ms to the American Naturalist. George Williams was the editor and said that it was too long for Am.Nat. so he was “sending it upstairs to the Quarterly Review of Biology” (both were published at SUNY-Stony Brook, where Williams was a professor). Unfortunately Dick Alexander learned that mine was in press in an awkward way: he finished his and submitted it to QRB, whereupon he was told that mine was in press there and as a result they did not want to immediately consider another one on such a similar subject! This ended well for Dick: he contacted Annual Review Ecol & Syst and they were delighted because they had an immediate slot due to a cancellation. So his paper came out before mine and in time to be cited by Ed Wilson in his 1975 book on SOCIOBIOLOGY (the QRB process was slower and mine appeared later, dated 1975 rather than 1974).
HS: You also thank a number of other people – William Eberhard, Mary Corn, William Hamilton, Egbert Leigh, Charles Michener, Martin Moynihan, Katherine Noonan, Michael Orlove, Robert Trivers and Jose Ignacio Borrero. Could you tell us a little more about how you knew these people and the nature of their help?
MJW: William Eberhard is my husband and is a smart and well-informed critic of everything I write. As I explain in the Acknowledgements the other people critiqued certain parts or the whole ms for me; Mary Corn was Ed Wilson’s grad student and stayed with us in Cali while she did some work on Polistes; Bill Hamilton was my friend and correspondent; Bert Leigh is a theoretical evolutionary geneticist and colleague at the Smithsonian Tropical Research Institute (STRI) in Panama – suggested that I make the title as general as it was; Charles Michener of course was the world’s leading authority on bees including on their social evolution due to his vast knowledge of both solitary and social bees all levels of sociality; Martin Moynihan was the Director of STRI in Panama and an expert on vertebrate ethology; Kate Noonan was a grad student of Dick Alexander doing observations and experiments on kin selection in Polistes fuscatus in Michigan; Michael Orlove was a student interested in the mathematics of kin selection and also social insects who later studied with Hamilton and John Maynard Smith; Bob Trivers was a student we had known at Harvard and was sent the ms to review and I don’t remember whether his suggestions came before or after he reviewed it; Jose Ignacio Borrero was the chair of Biology at the Universidad del Valle in Cali where I was when I wrote the paper – he was a good field ornithologist and let me use his personal library, which was better than the university library for literature on bird behavior..
HS: Would you remember how long it took you to write this paper, and when and where you did most of the writing?
MJW: The writing was after we moved to Cali in 1969. Two of my three children were born during the period of work on that paper, and the oldest was a year old when it started. We were far from good libraries, which was a handicap, but I got lots of reprints including from colleagues who knew of my interests.
HS: Would you say this paper had a relatively smooth ride through peer-review? Was The Quarterly Review of Biology the first place it was submitted to?
MJW: The history of this is given above. I greatly appreciated all critical comments and have never viewed them as obstacles in a “smooth ride” toward publication. I did lots of revision and it took time.
HS: What kind of attention did this paper receive when it was published? Was it considered controversial at that time?
MJW: I was in Colombia and not hearing much academic gossip. All of my correspondents were quite interested in it and I do not think it was “controversial” within organismic evolutionary biology. I was not involved in the sociobiology wars and did not even know about them until I was invited to speak at a AAAS symposium held in Washington DC – there it was clear that there was controversy surrounding anything that might suggest the genetic determination of human behavior, and some of that was politically or sociologically motivated; but I did not feel affected because I was not, except very indirectly, writing about humans and did not pretend to be doing so.
HS: Did this paper have any kind of direct impact on your career? Could you reflect on how it shaped the future course of your research?
MJW: The article got lots of positive attention from the audience it was intended for, and I think it helped my reputation among those colleagues. So it helped my career. I did not think of it as shaping my research. I was interested in learning all I could about the natural history of social and group-living tropical wasps and my research was driven by the fabulous opportunities I had to observe them. I continued to try to see the general importance of my observations, in terms of evolutionary concepts including kin selection, factors like mutualism influencing the evolution of group life, and competitive displays and social communication.
HS: Today, 41 years after it was published, where would you stand on the ideas expressed in this paper? Do you think the theory needs to be updated in anyway?
MJW: I think the key idea, about non-relatedness aspects of kin selection as represented by Hamilton’s formulation (K, the benefit/cost ratio in relation to r), is still completely valid. Many people continued to care more about r, but I have continued to be interested in Hamilton’s Rule as a decision rule affecting behavior – not (for my focus) a population genetics side that was Bill Hamilton’s main interest. This has led to my interest in adaptive behavioral flexibility and the evolution of flexible development in relation to the genetic theory of evolution.
HS: Could you reflect on the impact this paper has had on animal sociality research? Also, what does the paper mostly get cited for?
MJW: I can’t give a good answer to that. The paper was intended for people interested in behavior and has been mainly used by a variety of such people. I see that it is now often forgotten and probably seldom read, but I think the ideas are still good and now much better documented than when I wrote it. I hope you will forgive me if I do not take the time to go through the paper and figure out more precise answers to your question(s).
HS: You say that, in the specific case of eusociality in insects, mutualism, parental manipulation and kin selection could have all played a role, Today, do we have a better understanding of the relative importance of these processes in the evolution of eusociality?
MJW: Yes of course, definitely. Including in my own understanding. I don’t think it is possible to say what proportion of eusociality can be explained by each factor because they would often apply simultaneously or sequentially and to different extents in different lineages, at different points (e.g., mutualism under selection for life in groups; kin selection in relation to divisions of labor). But those factors have received a lot of attention and are now more precisely documented. In my own thinking a little progress has been made: when I wrote the paper I did not understand Michener’s ideas about how mutualism can lead to the origin of nonreproductive females. Later I finally was taught what they mean and how they apply – taught by a wasp called Metapolybia aztecoides (in Cali). Trivers figured out a precise solution to parent-offspring conflict which I did not see (nor did Dick Alexander).
HS: You say “It [is] necessary to revise hypotheses about the function of dominance hierarchies by taking into account the possibility of individually advantageous subordinance”. To what extent do you think that has happened?
MJW: I think that ethologists have long understood that, in their realization that ritualized battle allowed conflict resolution without physical damage. I can’t give a good answer to how subordinance is now viewed. Certainly, the group-selection idea that subordinants would refrain from fighting to avoid hurting the group has been overcome, perhaps at least in part due to reasoning that within groups of kin this could be individually advantageous in terms of kin selection.
HS: You say “Reciprocal altruism  requires meticulous contemporaneous controls on cheating and is therefore probably restricted to intelligent animals, the only documented example being man.” Does that continue to be the case?
MJW: I think that some non-human primates are now known to show reciprocal altruism and to satisfy the requirements I mentioned.
HS: You say that Kin-selection theory and inclusive fitness “provides an approach which could serve as the basis for a general and comprehensive theory of social behaviour”. Could you reflect on the extent to which this has been achieved?
MJW: I thought then (1975) that the 1975 treatment of social evolution by Ed Wilson would have been more synthetic if it had been based on kin selection theory as I understood it (including costs and benefits etc) because that explained many aspects of how social interactions lead to divisions of labor and individual reproductive decisions, functions of social display, etc. A very extensive review of all social behavior had been compiled prior to Wilson’s book by Wynne-Edwards, but explained in terms of good of the group/species. I could see that you could take the same huge collection of examples and explain them in terms of social competition and kin selection – and took up the aspects of social display and social competition in a 1979 paper (Proc. American Philosophical Society), with the flexible-response-using-Hamilton’s-Rule aspect developed in publications on Developmental Plasticity and Evolution (2003 etc)..
HS: Have you ever read this paper after it was published? If yes, in what context?
MJW: I cited the paper in subsequent papers of my own and corresponded with others about it and gave lectures on the subject as well, but since I knew what it contained I did not keep re-reading it.
HS: Would you count this paper as a favorite, among all the papers you have written?
MJW: I am still proud of the paper, not embarrassed by it as outdated (it isn’t) or sloppy.
HS: What would you say to a student who is about to read this paper today? What should he or she take away from this paper written 41 years ago? Would you add any caveats?
MJW: I would tell them to skip the algebra and focus on the discussion of the different terms and the examples.