In 1976, Stephen Stearns published a paper in the Quarterly Review of Biology that reviewed and organized the theoretical ideas, available at the time, about the evolution of life-histories, and provided a vision for future research in this area. This paper, which went on to become a ‘classic’ in the ecology and evolution literature, was a revised version of the Introduction section of Stearns’s PhD proposal. Forty years after the paper was published, I asked Stearns about his motivation for writing this paper, the people who influenced his thinking at the time, and what we have learnt since about the evolution of life-history tactics.
Citation: Stearns, S. C. (1976). Life-history tactics: a review of the ideas. The Quarterly review of biology, 51(1), 3-47.
Date of interview: Questions sent by email on 24th November 2016; answers received by email on 2nd December 2016.
Hari Sridhar: It is rare for a PhD paper to become a classic and have such a big impact on a field. I would like to start by asking you what motivated you to write this paper, and whether you had any inkling of how important it would turn out to be, as you were working on it?
Stephen Stearns: (This answer is taken from Designs for Learning, an essay that you can read in its entirety here
When I arrived at UBC (The University of British Columbia) in January of 1972 to start my PhD, I was advised to have a chat with Peter Larkin, a professor of fisheries biology and a former Rhodes scholar, who would later become the dean of the UBC graduate school. He had read what I had written in my independent projects at Wisconsin, and he had some advice for me. Do not, he said, listen to those who will advise you to start a research project immediately. Instead, spend a year or so reading widely and thinking about what is important that has not yet been done. Only then, when you understand what you want to do and why it is important, should you begin your research. He was advising me to use about a quarter to a third of my time in my PhD program to identify and take ownership of the issues that would shape my research. He was also advising me not to let the direction of my research and my career be shaped by professors who gave me projects to work on, but to shape it myself. This stance resonated with what I had learned in the three years that I had worked in a corporation: take charge of your own life, take responsibility for your own ideas, and act upon them.
I took his remarks to heart and, with the approval of my faculty mentor, acted on them. UBC has a streamlined PhD curriculum with few required courses. One writes a proposal, gets it approved by an examination committee, does the research, writes the thesis, gets the degree, and gets on with life. The proposal is to be presented within 18 months of arrival. I dived into reading and thinking about what I might do and, after some over-ambitious first attempts, managed to come up with a package that I thought was both promising and practical. It consisted of a long introductory review of life history evolution that justified the design of three research projects, which I proposed to start in parallel to see which were feasible and then to drop two of them to concentrate on the one that worked best. The ideas that I was proposing to test were not very familiar to anyone on the faculty at UBC, but I thought I had done a good job in my proposal of describing why they were interesting and plausible.
I defended my proposal late in the spring of 1973 before a departmental committee composed of the faculty mentor, four other members of the department, and an external member, in this case from cancer research in the medical school. The format was a 15-20-minute oral presentation followed by questions from the committee. When I finished my presentation, the fellow from cancer research went first, and he did not ask a question. He attacked, opening with, “This proposal is bad science and bad philosophy. The optimality arguments suggest that evolution is moving towards some goal. That’s teleological, and that’s wrong. Defend yourself – if you can.”
I got angry. I had spent 18 months reading, thinking, and writing, and I thought I had done it well. This professor misconstrued what I had written and presented, did not understand evolution, and was not challenging me constructively. He was attacking me in a way that could terminate my career in science before it could get started. We got into an intense argument that lasted about an hour. The other members of the committee looked on bemused as we went at it and finally asked a few friendly questions. Then they asked me to leave the room while they discussed my fate. I paced back and forth in the hall outside for 45 of the longer minutes of my life. At last the chair of the committee, Peter Hochachka, emerged to inform me that I had passed, barely, and that the decisive comment had come from Alf Acton, which I paraphrase as, “We cannot tell from this document and this examination whether he is a fool or a genius. I suggest we take the risk and pass him.”
Evidently, I had pushed the envelope about to its limits without realizing it.
Well, I am no genius, but the part of the proposal that had caused the problem, the long introduction to life history evolution, was revised and published in The Quarterly Review of Biology in 1976, its essential message intact. That paper is a revised version of the long introduction to my PhD proposal.
Did I have any inkling that it would be an important contribution? Frankly, I was so tied up in the process of self-definition as a scientist, and in my struggles to gain recognition for the kind of science that I wanted to do, against some significant opposition, that I did not think much about the long-term impact of my intellectual development in 1972-1974. Only when I was nominated for, and received, a Miller Fellowship at Berkeley, and then the reprint requests for the QRB paper started to arrive in my mailbox, did I start to think that I might have done something significant.
HS: Stepping back a bit, could you tell us how you got interested in evolutionary biology?
SS: I grew up on a sugar plantation on the north end of the Island of Hawaii, where I was surrounded by nature. My parents were both amateur naturalists, my mother more interested in birds and fish, my father in plants and trees. Shortly after I learned to swim and could manage a mask and snorkel (I was then four years old), my mother put me in the water at a little bay just north of Mahukona. I saw a magnificent adult male parrotfish, which seemed to be nearly as big as I was (it could not have been, but it was impressive), and chased it into deep water. That started an engagement with nature that has never stopped.
It was soon reinforced by experiences like the following, which I wrote about in the preface to the book on extinctions (Watching, from the Edge of Extinction) that I wrote with my wife:
“One morning, when I was in first grade in Kohala Elementary School on the north end of the Island of Hawaii, my father came into school and asked permission of the teacher to take me out for a few hours. It was an unusual request, but she granted it, for he was her husband’s boss. Most men on the sugar plantation would never have dared to make the request in the first place. We got into the jeep, drove down to Upolu Point, got out, and walked over to the edge of the sea cliff. He pointed out into Alenuihaha Channel and said, “I wanted you to see this. You’ll probably never see it again.” It was the winter of 1952-53, the end of the Korean War. He had been in a meeting that morning with Harry Taylor, who smoked, and I could smell cigars on his khaki clothes. I was barefoot, wearing blue jeans and a white t-shirt. He put his arm around me as we looked out into the channel, the trade wind blowing strong into our faces, whipping up white caps.
“There were hundreds, perhaps thousands, of whales in front of us, big ones, little ones, mothers, babies. They were moving slowly from left to right around the point and down the coast towards Honokaa, spouting, breaching, some jumping clear of the water. The trade wind was steady; Dad’s arm was around me; the sun was hot but the breeze was cool.
“During World War II there was no organized whaling, stocks recovered a bit, and the populations from both the Arctic and Antarctic had made their annual migration to Hawaii to give birth in a region where the water was warmer and where there were no killer whales and fewer sharks than in the feeding grounds nearer the poles.
“Dad and I watched in silence for about half an hour, then went home to lunch at the plantation house in Hawi. Many years later, a few years before he died, hardly believing my memory, I asked him whether it had really happened. He confirmed that it had, and that I was not exaggerating the numbers. I shall not be able to show that many whales to my boys in my lifetime. Perhaps their grandchildren will see them again.”
My parents gave me Darwin’s Voyage of the Beagle for Christmas when I was about 12 years old. Although I did read it, it did not make an immediate impression. However, through my parents I was becoming aware of the unique Hawaiian radiations of honeycreepers and lobelias, and I managed to see some of them as a teenager. Those early experiences of nature are what motivated my study of biology and, as I got into it, of evolution.
There was another important influence. I really enjoyed learning about math and physics and was enchanted by the great romance of knowledge represented by Galileo, Newton, Einstein, et al. It formed my model of good science: a body of knowledge informed by theory that is rigorously tested against observations and experiments. That early enchantment influenced the type of evolutionary biology that I went into: I wanted to help build a science based on sound theory.
At the time almost the only evolutionary theory available was population genetics. I took James Crow’s course in theoretical population genetics at Wisconsin in the summer of 1971. Jim Crow was a legendary population geneticist, one of the greatest of his generation, a gentleman, a very kind man, and a gifted cellist. Crow was impressive; I respected him; he was worth rebelling against.
That summer was the first time Crow taught his graduate course after his landmark book with Motoo Kimura was published; he took us on a tour through the chapters that he had written. They involved algebra and a little calculus, whereas Kimura used stochastic differential equations in the later chapters – I was relieved that we did not get into them. I experienced the course as applied mathematics with a strong element of probability theory, not as empirical science, for there was at that time very little data available to which one could apply the theory (that changed with ever cheaper DNA sequencing). I liked the theoretical elegance, and I enjoyed doing the homework, but I deplored the absence of whole organism biology. All the interactions of organisms with environments were reduced to a single parameter, w or r, that was used to predict changes in gene frequencies, which were clearly important but far from the whole story.
I made a deal with Crow. I would write a paper on the role of phenotypes in evolutionary theory, and I would also take the final exam. My grade would be based on the paper, not on the exam, and he would grade both. My choice of topic was strongly influenced by one of three books that Stan Dodson (my mentor for my master’s thesis) recommended. I had read them over Christmas break 1970-1971. They were Ramon Margalef’s book on community ecology, which I found unconvincing, Richard Levins’ book on theoretical evolutionary ecology, which I found inspiring but hard to apply, and George Williams’ 1966 book Adaptation and Natural Selection, which impressed me deeply. In that book, which contained a devastating critique of group selection and a summary of his thinking on the evolution of aging, Williams laid out the major ideas that would become life history theory, in particular, the idea that reproduction trades off with survival. Madhav Gadgil and William Bossert picked up that idea in a paper published in The American Naturalist in 1970, where they used it to develop predictions that remain largely successful.
I took their paper as the core reference in my paper for Crow. I got a B+ on my paper, which counted, and an A on the final exam, which did not. While irritated with myself and dissatisfied with the paper, I did not regret my decision to be graded on the paper and not on the exam, for my A on the exam told me that I had understood the material, and my attempt at a paper started a line of thought that paid off later. When I published The Evolution of Life Histories in 1992, I sent Jim a copy thanking him for his teaching and noted that the book represented the paper that I wished I had been able to write for him twenty-one years earlier in the summer of 1971. When he visited Switzerland shortly thereafter, he graciously acknowledged the gift, but I am not sure that he ever read the book. He was a geneticist first, last, and always; how evolution designs phenotypes for reproductive success was not a problem on which he focused. That was George Williams’ problem.
HS: In the Introduction of this paper you say “Another review of life history is waiting to be written. It would take the hypotheses reviewed in this paper, or their surviving descendants, and test them against the massive body of evidence…I have not attempted to summarize that body of data in this paper…but I hope someone will.” Later, did you decide to do this yourself, and is that what forms the 1977 AROES paper?
SS: The 1977 paper does some of that, and my later books and Derek Roff’s books do more of it. That goal became less relevant when experimental evolution began to allow direct tests of hypotheses.
HS: Do you remember how you drew the figures in this paper?
SS: Most were drawn by hand, and they show it. In 1976 the software options were limited.
HS: Would you remember how long it took you to write this paper, and where and when you did most of the writing? I notice that it is published in 1976, four years after you defended your proposal. Did you put this away for a while, and come back to it after you did other work in your PhD?
SS: I started the paper in the fall of 1972 and completed the first draft by spring 1973. I then gave it to supportive faculty at UBC. Two of them, in particular, did great jobs in suggesting revisions: Bill Neill and Dennis Chitty. Dennis line-edited sentence-by-sentence; his careful attention then improved my writing ever after. I submitted the paper to QRB in September 1974. A few days later, I got a 3 page long, single spaced, letter from George Williams, who was editor-in-chief of QRB at the time. It was full of constructive points and made clear that, although he would check with referees, the paper was essentially accepted subject to revision. It was formally accepted by late 1974; the delay in publication occurred because QRB only publishes 2-3 papers per issue and only have 4 issues per year, and they had a backlog of accepted papers.
The paper was much longer in print than is normal for QRB, which imposed page charges. I was a poor graduate student who could not pay them. My PhD committee and some other faculty generously agreed to support me, and it cost them several thousands of dollars of their research budgets to do so. Those contributing included Con Wehrhahn, Bill Neill, Don McPhail, and Buzz Holling. Tom Northcote, Peter Larkin, and Charlie Krebs may have chipped in as well.
HS: If you don’t mind, I would like to go over the names of people you acknowledge to find out a little more about how you knew them and how they helped:
SS: For these three, see above:
William Neill
Dennis Chitty
George Williams
David Mertz – I met David at an ESA meeting in 1975 and discussed bet-hedging with him. He was one of the first people outside UBC with whom I had a conversation about life history evolution.
Eric Charnov – Ric came to UBC as a postdoc in 1972. He and I organized a graduate seminar on life history evolution that was attended by John Krebs, then a junior faculty member at UBC, and five or six fellow grad students. Ric and I discussed life history evolution frequently while we were both at UBC. I recall looking over his shoulder and suggesting that he try to optimize the logs rather than the untransformed variables in an equation he was working on. I do not now recall whether it pertained to optimal foraging or to life history evolution.
James MacLean – Jim was a fellow graduate student working with Don McPhail. He and I spent a lot of time together in the coffee room and at the gym. He provided emotional support.
Conrad Wehrhahn – Con was officially my major professor, the head of my PhD committee. Con was a theoretical population geneticist who did Kimura-style diffusion equations, mostly at 2 am. During the day he hung out in the coffee room and was often available there for a chat. Con was very open minded about my research, which was rather different from his, and quite supportive, but he did not provide me with much helpful technical advice. I could have used more help in learning how to write an empirical research paper.
Judith Myers – Judy arrived, I believe, in 1973 as a starting assistant professor. She had the office directly across the hall from mine, her door was always open, and she was a cheerful and supportive presence. She is a field ecologist who has worked mostly on insects, and she has a fine mind especially good at critiquing the empirical support that theoretical ideas do, or do not, enjoy.
JD McPhail – Don was by training an ichthyologist, an expert on the fishes of Canada, but he was just as interested in evolution, ecology, and genetics as he was in phylogenetics. His work on sticklebacks in British Columbia forms the foundation on which Dolph Schluter has built much of his work on ecological speciation. Don was that member of the UBC faculty most interested in the questions I was asking about life histories and the most supportive in teaching me how to do experiments on fish in the laboratory.
CS Holling – Buzz was a member of my PhD committee and a friendly and supportive cheer leader whose letters opened doors. He was the director of the Institute of Animal Resource Ecology, its intellectual leader, and its most famous scientist. Having the support of someone with that profile meant a lot.
Beverly – Bev is my wife of 45 years, my best friend, and someone from whose courage and grace I have learned and enormous amount. More than anyone in my life, with the possible exception of my parents, she has made me a better human being.
Peter Larkin – At the time that I got to know him, Peter was an administrative leader, a respected founder of the institute, and a beloved teacher. His advice launched this paper (see above) and changed my life.
Michael Ghiselin – Michael was my postdoc mentor at Berkeley who hosted me for the Miller Fellowship. It was his reading of the manuscript of the not-yet-published QRB paper that probably got me that opportunity. However, he had a mental breakdown shortly before I arrived, and I never interacted with him much at Berkeley.
OTS courses 72-3 and 73-4 – I took the first course and taught in the second. The faculty in the first included John Vandermeer and Doug Gill; the students in the second included Russ Lande, Les Real, and Peter Abrams. Doug Futuyma gave a visiting talk. Conversations and presentations in both courses significantly advanced my thinking about life histories.
HS: Did this paper have a relatively smooth ride through peer review? How did you decide to submit this to The Quarterly Review of Biology?
SS: Yes. See above. I submitted it to QRB because the journal had been founded by someone who worked on comparative demography (Raymond Pearl), had published important work on life histories (e.g. Cole 1954), and was edited by a person who had contributed some of the most important ideas that shape the field (George Williams).
HS: At the time it was published, did this paper attract a lot of attention and discussion?
SS: Yes, I immediately began to receive reprint requests. At that time, they arrived by mail. Within the first year I had gotten about 1000 of them.
HS: This paper has been cited over 3000 times. Do you have a sense of what it mostly gets cited for?
SS: I think it gets cited for several reasons. One is simply as a convenient way to cite one review paper rather than many original research papers. Another is because it synthesized an emerging field, placed it in context, and, in a sense, made it important. I do not think it often gets cited for any original ideas that it may contain. There are some, present mostly in larval form, and most of those were better developed later by others.
HS: Did this paper have any kind of direct impact on your career? In what way did it influence the future course of your research?
SS: This paper established me in my field, helped to create that field, and led directly to my later positions. It made my career possible. Subsequent work solidified that. This paper was, in retrospect, a necessary but not a sufficient condition. Continued performance was also needed.
HS: This paper gives the reader the impression that you were quite frustrated with the state of the discipline at that time. Today, 40 years later, could you reflect, again, on the main message of this paper and the current health of life-history research?
SS: The main message of the paper was that there was a mismatch between theory, of which there was a lot, and empirical tests, of which there was not enough. Today that is not the case. Many experiments have been performed, and many observations have been made, that confirm some of the major theoretical claims reviewed in the paper. It is now well-established that if extrinsic mortality on adults increases, age at maturity will decrease, early fecundity will increase, and lifespan will decrease.
At the same time, theory has become more sophisticated. We now have many models dealing with stochastic environments and plastic responses, and for those predictions, we are rather close to the situation in 1976, where there was an imbalance between theory and evidence. I am no longer as personally frustrated by that situation, for in the interim I have seen how the scientific community does make progress where progress can be made, and I have come to better understand why there will always be an imbalance between theory and experiments, for in this field one can come up with a new model much more quickly than one can test it experimentally.
HS: If you were to write such a paper again today, in what ways would your emphasis change?
SS: Please see my 1992 book. I used it again to teach in 2016, supplementing it with papers, and I find that it still provides a good conceptual framework, although it is now out of date concerning specific results.
HS: In the next few questions I would like to focus on specific sentences in the paper, where you highlight lacunae and directions for future research, and ask you to reflect on the extent to which they have been addressed today.
You say, “As a weak link in the chain of evolutionary logic, our failure to deal realistically with sex [in life history theory models] deserves wider discussion”
To what extent have we improved in our treatment of sex in life history theory?
SS: This had been well addressed by Brian Charlesworth in the two editions of his book on evolution in age-structured populations, and the issue has been extended by the concept of intra-locus conflict, which points out that most genes in diploid organisms spend half their time in males and half their time in females. Differences in selection between the sexes, and genetic correlations between the sexes, then result in constraints on the evolution of one sex caused by things happening in the other sex. This is interesting, important, and by no means completely understood.
HS: You say, “Our knowledge [of life-history tactics] will advance most rapidly through the interaction of theory and experiment at the intraspecific level”
To what extent has this happened?
SS: The experimental evolution of life histories in fruit flies and bacteria has been used to test the theory. We now have quite an impressive tradition of that, coming from many distinguished labs. We also have wonderful long-term field studies in which individuals have been followed from birth to death for generations. Both approaches have yielded key insights that bring us much closer to understanding causation than do the currently popular macro-ecological approaches that rely on correlations detected in patterns.
HS: You say, “A direct test of the Charnov-Schaffer prediction would involve selection experiments on short-lived organisms, preferably in the field. [] such experiments have yet to be done”.
Have these experiments happened?
SS: No, not for those specific predictions. However, field work on lobelias on Mt. Kenya by Truman Young confirmed the main ideas in the Charnov-Schaffer model.
HS: You say, “theories accumulate, few of them formulated in common terms, much faster than evidence can be assembled to test them. The result is a confusion of untested ideas…If the field is progress we must…get back to rigorous empiricism”.
Would you say the balance of theory and experiment has improved today?
SS: Yes, it has, and I am no longer as frustrated by that tension as I was in the early 1970s.
HS: You say, “No fitness definition simultaneously accounts for sexual recombination, applies to whole organisms and their progeny rather than to populations of single genes, and allows for the different contributions of male and female offspring. Furthermore, fitness only applies to organisms in the context of a given environment.”
Today, do we have a better mathematical definition of fitness?
SS: No, not really. There has been a lot of work on geometric mean fitness and its extension, the Lyapunov exponent, but fitness remains a mathematical convenience, absolutely necessary for modeling but nevertheless a human artifact, a tool we invent to help us understand nature. In nature, we see what has survived from the origin of life up to now. That’s nature’s fitness definition.
HS: You say, “In order to make progress at this point [in understanding how environments influence life history] we need carefully controlled field experiments on a short-lived plant or animal…Drosophila would take the least effort, but a poecilid fish would provide the best analogy to larger fish and other vertebrates”.
Could you reflect, to what extent, this has happened, especially with regard to the taxa you suggest?
SS: It has happened, and abundantly. There is now a large literature reporting experiments on life history in Drosophila (Linda Partridge, Mike Rose, Kuke Bijlsma, my lab, many others) and in poecilid fish (Dave Reznick’s work in Trinidad, but also my work in Hawaii).
HS: You discuss models that tackle a tradeoff between reproduction and subsequent survival and reproduction and say that a suitable system to test this would be ”clutch sizes of a bird species that has a long period of paternal care, and which does not put a large proportion of its reproductive effort into the production of an egg.” And that “A nesting colony of cliff swallows might present a good opportunity to do this if adults return to the same colony each year”.
Would you know if anyone has take up your suggestion and done such a study?
SS: The ornithologists working on clutch size have been very productive. The study done by Serge Daan, Cor Dijkstra, and Joost Tinbergen on kestrels is a classic. It was published in 1990, but on this issue, I do not think it has yet been surpassed. (I would be happy to be informed that my scholarship is deficient on this point.)
HS: In the 40 years since this paper was published, have you ever read it again? If yes, in what context? What strikes you most about it when you read it now?
SS: I have not read it very often in recent years. I did refer to it in the 70s and 80s, particularly when I was starting to write the 1992 book, which in my thinking has effectively replaced it.
HS: Would you count this as one of your favourites, among all the papers you have published?
SS: I now find it a bit too large in scope and, in the light of later work, not nearly as precise as it could be about some important ideas, including bet-hedging. However, it was a good thing to write at the time, and many people have found it helpful. It was certainly my favorite for at least 5 years after it was published.
HS: What would you say to a student who is about to read this 40-year old paper today? What should he or she take away from it? Would you add any caveats?
SS: I do encourage students to think about turning their PhD proposals into review papers, and some of them have done so. In that sense, it continues to serve as a useful model, although it is not the only one. And I continue to recommend the process that produced it – an extensive period of reading and reflection during which one tries to identify the leading ideas, and the major deficiencies, of the field in which one is interested and then summarize them in a clearly written document that can be critiqued by others. But if one wants to get an introduction to life history evolution today, it is better to read the books by Charlesworth, Roff, Charnov, and myself, than to read this paper, which I think is now mostly of historical interest.
Reflections on Papers Past 