David Sloan Wilson's Statement: The Neo-Darwinian Revolution Is Far from Complete

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I thank TheBestSchools.org for sponsoring this dialogue and pairing me with Denis Noble. In some ways I am an odd choice to argue for the position that neo-Darwinism is enough, since I am a well-known critic of selfish gene orthodoxy and a participant in the first workshop to use the title “extended evolutionary synthesis.”[1] Nevertheless, I am happy to argue for this position as long as it is appropriately framed.

My programmatic activities during the last 13 years also qualify me for the job: First, as director of EvoS (standing for “Evolutionary Studies,” and pronounced as one word), which teaches evolution across the curriculum at Binghamton University, and then as co-founder and President of the Evolution Institute (EI), which applies evolutionary theory to public policy issues of all sorts. Through a number of communication outlets managed or supported by the EI (This View of Life, Social Evolution Forum, Evonomics.com, and PROSOCIAL Magazine), I have taken on the role of a newspaper reporter, covering the beat of evolutionary science. I will draw upon this experience, in addition to my own research, in what follows.

Defining Neo-Darwinism

One of the most elegant distillations of conventional evolutionary theory was by the pioneering Dutch ethologist Niko Tinbergen (below right), in an article titled “On aims and methods of ethology” (1963).[2] At the time, it was not widely accepted that a behavioral trait (such as aggression) can evolve in the same way as a physiological or anatomical trait (such as a deer's antlers). In the process of making this case, Tinbergen observed that four questions need to be addressed for all products of evolution, concerning their function, mechanism, development, and phylogeny.

Niko Tinbergen portrait, black and white
Biologist and ornithologist Nikolaas Tinbergen, 1907–1988

The function question concerns why the trait exists, compared to many other traits that could exist, often because of the winnowing action of natural selection. The mechanism question concerns how the trait exists in a physical sense. The development question concerns how the trait comes into being during the lifetime of the organism. The phylogeny question concerns how the trait came into being over multiple generations, since evolution is a historical process.

Tinbergen's case that behaviors evolve much like other traits has become so thoroughly accepted that no one questions it anymore. He shared the 1973 Nobel Prize in Physiology or Medicine with Konrad Lorenz and Carl von Frisch for their pioneering work in ethology [the scientific study of animal behavior—eds.]. Tinbergen's four questions, however, are still widely cited as a compact description of a fully rounded evolutionary perspective. I will take them as my definition of neo-Darwinism.

Ernst Mayr, evolutionary biologist
Evolutionary biologist Ernst Mayr, 1904–2005

Some might disagree. For example, it is often said that the so-called Modern Synthesis left out development. In this regard, it is notable that Harvard ornithologist Ernst Mayr (left), one of the main names associated with the Modern Synthesis, made a two-fold distinction between ultimate and proximate causation,[3] rather than Tinbergen's four-fold distinction.

Roughly, Tinbergen's function and history questions map onto Mayr's concept of ultimate causation, while the mechanism and development questions map onto the concept of proximate causation. So Mayr's terminology did push development into the shadows by failing to distinguish between the adult trait and how it comes to exist during the lifetime of the organism. Nevertheless, there is no reason to privilege Mayr over Tinbergen in their characterization of evolutionary science during the 1960s.

Having clearly stated my definition, here is the position that I will defend in this essay: Tinbergen's four questions are enough for the future progress of evolutionary theory. In fact, to claim otherwise is a distraction.

The Neo-Darwinian Revolution is Not Yet Complete!

It is shocking, when one pauses to think about it, how many fields of inquiry do NOT employ a fully rounded four-question approach. In this sense, the neo-Darwinian revolution is very far from complete. An example will illustrate the enormity of the problem.

James Coan is a highly regarded clinical psychologist and neuroscientist at the University of Virginia's Department of Psychology. In many respects, he is at the cutting edge of his field, employing brain imaging techniques to investigate the nature of problems such as post-traumatic stress disorder (PTSD) in war veterans. Yet, difficulties interpreting a line of experiments and a suggestion by a colleague to read a book titled An Introduction to Behavioural Ecology[4] led Coan to have what can only be called a born-again experience.

Coan read the fourth edition of this book. The first edition was published in 1981 and reflected a maturation of what Tinbergen, Lorenz, and von Frisch had started. Especially powerful was the maturation of the “function” question. More and more, animal behaviorists were asking the question: “How would the organism that I study behave, if it were a product of natural selection?”

Asking this question allowed mathematics to be employed in a way that was new for the study of animal behavior, although customary in the field of economics (more on this below). For example, in a foraging organism that is adapted to maximize its rate of energy gain (E) per unit time (T), just a few additional assumptions about its foraging behavior (e.g., it can only handle one item at a time) and its foraging environment (e.g., each prey type, i, is randomly encountered and is characterized by a density, an amount of energy, ei, and handling time, hi) are sufficient to generate detailed predictions about its foraging behavior (e.g., it should rank each prey type according to its e/h ratio and always accept the highest-ranked prey types down to a cut-off point, below which it should ignore all prey types) that were highly novel and testable in the laboratory or field.

If the assumptions of this particular model don't fit a particular foraging organism, then models with different assumptions can be built (e.g, non-random food distributions, foraging under the risk of predation). In this fashion, a whole family of models called “optimal foraging theory” sprang up in the 1960s and 70s, which organized the study of foraging behavior as never before. As for foraging behavior, so also for every other behavior (e.g., mating, fighting, cooperation) and traits that are typically not considered behaviors (e.g., sex ratio, life history strategies, developmental strategies, strategies of the immune system).

Optimal Foraging TheoryThe function question helped to inform the other questions, and vice versa. White-tail deer and kangaroos are both mammalian herbivores, but the fact that they evolved on different continents makes them very different from each other, which influences their development and specific adaptations to their environments. To focus on brain mechanisms, suppose that I assigned you the task of studying the brains of two bird species without telling you anything about their ecologies. Unbeknownst to you, one species migrates south during the winter and is adapted to memorize the night sky as a nestling. The other remains north during the winter and is adapted to memorize the location of thousands of food items stored during the fall. How many decades would be required for you to discover the mechanistic basis of these adaptations, studying only the brains of the two species?

All of this was part of my training as a graduate student in the 1970s, but it was new to Coan in the 2010s and reading the fourth edition of An Introduction to Behavioural Ecology was like the scales falling from his eyes. Here is how he described the experience during an interview that I conducted with him in 2016 [soon to be published]:

James Coan: I think “meteoric” is the right way to describe its impact on me. By the time I had finished the first chapter I was already thinking about my own work, and indeed, thinking about psychology as a broad discipline completely differently. The book starts out introducing principles that organize behavior—that when you give them even a little bit of thought make complete sense. Principles like the management of bio-energetic resources; that if you're going to engage in a behavior as an organism, to accrue resources, you have to invest resources that you have in store. That is a very risky business, so you need a certain amount of information about the demand of the environment and your own resource cache. That entails certain principles that get built into the genome over time about keeping an excess, having a surplus, and maintaining a surplus. So you must balance your investment against …

David Sloan Wilson: Tradeoffs, tradeoffs, tradeoffs.

JC: Tradeoffs everywhere. I had a kind of personal and intellectual crisis, where I thought “Holy shit! What have I been doing all this time? I've been thinking about constructs that aren't tethered to any ultimate goals or any ultimate constraining principles. In psychology, anything goes, because the thinking isn't constrained by these imperatives of biological organisms across evolution and ontogeny. Then I started going through chapter after chapter, example after example, of these principles existing not just as logical arguments but as empirical data. It was enough to almost make me cry.

Coan's academic disciplines of psychology and neuroscience were highly sophisticated in their own ways, but they had not converged upon Tinbergen's fully rounded four-question approach. In a sense, Coan was like someone who had been given the brain of a species to study without being told nearly enough about the ecology and evolutionary history of the species—Homo sapiens, in his case.

Once one becomes attuned to the four-question perspective, the extent of its absence becomes shocking. Consider this segment of an interview that I conducted with the Harvard population geneticist Richard C. Lewontin in 2015. Lewontin (left) was a student of the geneticist Theodosius Dobzhansky, who famously pronounced that “Nothing in biology makes sense except in the light of evolution” in an article written in 1973.[5]

Richard Lewontin: I was raised not as an evolutionist but as a population geneticist.

David Sloan Wilson: Right.

RL: That's a big difference.

DSW: Why is that a big difference? Let's clarify that for me. I tend to see it as a small difference. What's the difference between being a population geneticist and an evolutionist?

RL: A population geneticist by theoretical training has certain parameters of population change. That's become broadened by the realization that there are between-population changes, and so on, but within a population we're talking about changes in gene frequency and we have a catalog of the causes: selection, inbreeding, chance, mutation, and so on. Our job as population geneticists is to do the necessary observations of the various things that give us estimates of the strength of those different forces. Now, historically one of the most interesting—now I want to talk a little about the sociology of our science—Theodosius Dobzhansky, my professor and then-greatest living evolutionary biologist…

DSW: Mr. “Nothing in biology makes sense except in the light of evolution.”

RL: Yeah, right. He was a very bad field observer. Theodosius Dobzhansky never, in his entire life, nor any of his students, me included—I would go out in the field with him, actually—ever saw a Drosophila pseudoobscura in its natural habitat.

DSW (laughs): Yeah, OK!

RL: We didn't know where they laid their eggs. We couldn't have counted the number of eggs of different genotypes. How did we study Drosophila in the wild? We went out into the desert, into Death Valley, we moved into a little oasis, we went first to the grocery store, and bought rotten bananas. We mushed up the bananas with yeast till they fermented a bit, we dumped that into the paper containers, put it out in the field and the flies came to us.

DSW: Right! No naturalistic context whatsoever.

RL: None … at … all. And to this day we do not know anything about the actual habitat of Drosophila pseudoobscura, although by the way, interestingly enough, in more recent years, Tim Prout actually succeeded in trapping pseudoobscura in orange groves, so we don't even know how much they hang out with cultivated fruit.

DSW: Right.

RL: Now let me go one step further because we cannot understand the development of evolutionary biology if we don't understand questions of the sociology of academic life. If I wanted to study evolutionary forces acting on some genetic polymorphism in Drosophila, I would go and look for some species of Drosophila where I could actually look at, perturb, and work with the actual breeding sites and egg-laying sites, and pick up larvae in nature, and so on. And in fact there is such a group of Drosophila. They are the cactophilic ones. There is a group [of scientists] from Texas and other places that studies the cactophilic Drosophila in an ecologically sensible way of going to the rot pockets and perturbing them, getting larvae out of them, and so on. That group never acquired the prestige associated with the Dobzhansky school because—I don't know why. They were doing what one has to do. That's why, for example, I try to convince students who are entering evolutionary biology not to study animals at all but to study plants. Plants stay in one place. You can manipulate them. You can move them. Plants are much better than animals for studying things in nature. Yet, plant evolutionary biology is not, for sociological reasons that I don't understand—I could make up stories—has never had the prestige that animal work has had when it comes to population genetics.

DSW: Right. I think that [there was an] all-consuming interest in physical mechanisms as opposed to a more fully rounded approach. I place a lot of emphasis on the classic paper by Niko Tinbergen, “On aims and methods of ethology”, in which he says that you have to ask four questions: Function, History, Mechanism, Development. Are you familiar with that paper?

RL: No, I'm not. Send me a reference to it.

DSW: It's such a succinct summary of what a fully rounded approach needs to be …

Lewontin's comments reveal that Tinbergen's four-question approach is still a work in progress within the biological sciences, before we even get to more human-oriented academic disciplines.

Every major discipline such as ethology, ecology, paleontology, systematics, development, genetics, population genetics, biochemistry, and molecular biology has a separate history that is contemporaneous with the theory of evolution. Model species such as Drosophila were chosen during the early twentieth century because they were easy to culture in the laboratory or because their chromosomes were easy to stain and observe under the microscope. The most pressing questions were often mechanistic in nature, pushing Tinbergen's other three questions into the background. Who needs to know the nuances of the ecology of Drosophila when you're trying to work out the basic mechanisms of recombination, the transcription of genes into proteins, and the like?

As mechanistic knowledge increases, then the need to bring in the other questions becomes increasingly important, but integration can require decades and is impeded by a variety of intellectual and sociological factors. If I were to nominate the single most important priority for the biological sciences, it would be to get everyone on the same page with respect to Tinbergen's four questions.

George C. Williams
Evolutionary biologist George C. Williams, 1926–2010.

A similar story can be told for medicine and the health sciences, which are obviously advanced and sophisticated in their own ways, but shockingly clueless, for the most part, about Tinbergen's four questions. That's why George C. Williams (right), an evolutionary biologist by training, and Randolph Nesse, a psychiatrist by training, could write a groundbreaking academic article in 1991 titled “The Dawn of Darwinian Medicine,” followed by their trade book Why We Get Sick in 1995.[6] Both of these works are elementary tutorials, much like the article that Tinbergen wrote in 1963, except oriented toward the topic of medicine rather than ethology. Fast-forwarding to the present, Nesse is founding director of Center for Evolution and Medicine at Arizona State University, which was established in 2015. In my 2016 interview with him, he reports that a fully rounded four-question approach is only beginning to gain a toehold in the health sciences.

Let's zoom in on cancer as one topic within the health sciences. Cancer is natural selection taking place among the cells of a multicellular organism. Evolution has no foresight, so the fact that proliferating cancer cells eventually bring about their own demise with the death of the organism is immaterial. That might also be our epitaph if we succeed in causing our own extinction as a species. Since multicellular organisms that are relatively cancer-proof survive and reproduce better than those that are relatively cancer-prone, billions of years of natural selection at that level have resulted in elaborate genetic and physiological mechanisms that protect against cancer cells. Nevertheless, lower-level selection (among cells within the organism) is only suppressed by higher-level selection (among organisms), never entirely eliminated, and can erupt when evolved protective mechanisms are disrupted by modern environmental factors that were not present in our ancestral environments.

The preceding paragraph describes a fully rounded, four-question approach to the study of cancer. Once learned, employing the four-question approach is as easy as riding a bicycle. But the first scientific articles describing cancer as natural selection among cells within our bodies weren't published until the 1970s and the community of cancer researchers employing the four-question approach is a minuscule fraction of the larger cancer research community. The dynamic is similar to what Lewontin described for genetics in the first half of the twentieth century—an obsessive focus on physical mechanisms and inattention to the other three questions.

Athena Aktipis, psychologist
Athena Aktipis, co-Director of The Human Generosity Project

One cancer researcher who does champion the four-question approach is Athena Aktipis (left), who was trained as a theoretical evolutionary biologist and studies a variety of topics centered on the evolution of cooperation in addition to cancer. In my 2016 interview with her and her report on the first Evolutionary Biology and Ecology of Cancer (EBEC) Summer School at the Wellcome Genome Campus in the UK, she describes the same emerging paradigm that I described for the study of behavioral ecology in the 1960s and 70s, which was so new for James Coan in the areas of clinical psychology and neuroscience.

Here is an example of how elementary four-question reasoning provides new insights for the study of cancer. Since natural selection within the body requires cell divisions, the more cell divisions that take place, the higher the likelihood of cancer. This pattern is typically observed within a species. Old people get cancer more than young people (which you already knew) and tall people get cancer more than short people (which you probably didn't know—at least I didn't!). Yet, the pattern does not hold across species. The incidence of cancer in long-lived species such as elephants is not greater than in short-lived species such as mice. This is called Peto's paradox and the most likely explanation is that long-lived species have evolved better cancer-prevention mechanisms than short-lived species. Knowing this, you'd think that cancer researchers would be interested in studying long-lived species to discover new drugs, gene therapies, and the like for the treatment of cancer in humans. More generally, you'd think that cross-species comparisons would be an important part of cancer research, but this is not the case. The vast majority of cancer research is conducted on a very few model organisms chosen for ease of laboratory research—like the early days of Drosophila research described by Lewontin. Granted, it's not easy to study elephants, but the comparative study of cancer in different dog breeds provides rich opportunities for employing a fully rounded, four-question approach and this too is a new idea in cancer research.

Let's pause to take stock of the argument that I have developed so far for why neo-Darwinism is enough. If by “neo-Darwinism” we mean Tinbergen's four questions, then we can see that he was premature to suggest in 1963 that they are already being employed by biologists for the study of non-behavioral traits and merely needed to be extended to behavioral traits. A fully rounded, four-question approach also needed to be applied to many non-behavioral traits, especially in areas of the biological sciences where an excessive focus on physical mechanisms—one of the four questions—crowded out the other three questions. Moreover, this problem still exists for topic areas such as neuroscience and cancer research in the twenty-first century. No amount of sophistication in the study of proximate mechanisms can substitute for a fully rounded, four-question approach. Until this point is well understood, to say that we need to go beyond the four-question approach is a distraction.

My argument so far also highlights the need for a fine-grained understanding of the many disciplines that comprise the biological sciences. They are connected to a degree, but they also have their own histories and integration is still a work in progress. History matters—for the study of academic disciplines no less than for the study of biological species.

The Human-Related Academic Disciplines

When we move from the biological and “hard” psychological sciences (e.g., neuroscience) to the human behavioral sciences and humanities, the situation gets even worse. It is not an exaggeration to say that the study of evolution in relation to human affairs lags behind the study of evolution in the biological sciences by about a century.

As an example, Sociobiology: The New Synthesis, published by the evolutionary biologist Edward O. Wilson in 1975,[7] was cut from the same cloth as An Introduction to Behavioural Ecology and reflected the maturation of what Tinbergen, Lorenz, and von Frisch had started. Wilson's thesis was that a single theoretical framework could explain the evolution of social behaviors in all species, from microbes to humans. It was celebrated as a synthetic triumph, except for the final chapter on humans, which created an uproar, complete with charges of fascism and an infamous pitcher of water that was dumped on Wilson's head during an annual conference of the American Association for the Advancement of Science.

Over a century after the publication of Darwin's Descent of Man in 1871,[8] it was not permissible to study human social behavior from an evolutionary perspective. It wasn't until the 1980s that terms such as “Evolutionary Psychology,” “Evolutionary Anthropology,” “Evolutionary Economics,” and “Literary Darwinism” began to be coined, signifying a renewed attempt to rethink the human-related academic disciplines from an evolutionary perspective–and even these had an air of scandal about them.

That's the bad news. The good news is that enormous progress has been made since then, which is reported in dozens of books and hundreds of peer-reviewed articles without anyone raising an eyebrow. The future is already here for a sizable community of scientists and scholars who use a fully rounded, four-question approach to explore the length and breadth of humanity. However, this community is still a tiny fraction of the worldwide academic community in the human-related academic disciplines. Also, these recent developments are scarcely reflected in college-level education, a point that is central to the mission of TheBestSchools.org, as I will discuss in more detail below.

C.P. Snow, black and white
English physical chemist C.P. Snow, 1905–1980

The two communication outlets that are produced by the Evolution Institute—This View of Life (TVOL) and Social Evolution Forum (SEF)—exist to catalyze the completion of the neo-Darwinian revolution. TVOL articles are written for a broad audience without being watered down and SEF blogs, target essays, and commentaries are written at a more professional level. If you visit these sites, you will see nothing more or less than the application of Tinbergen's four questions to “anything and everything” in biology, the human-related sciences, and the humanities. For example, my target essay in SEF titled “The One Culture” reviews four books that are helping to unify the sciences and humanities, in contrast to the disconnect between them that the British scientist/novelist C.P. Snow (above right) called attention to in his famous 1959 Rede Lecture entitled “The Two Cultures.”[9]

“The Two Cultures” can't become “The One Culture” unless human culture itself can be understood from an evolutionary perspective. Progress toward this goal was impeded for most of the twentieth century, not only because of avoidance on the part of humanists, but also because evolutionary biologists became excessively gene-centric. Darwin knew nothing about genes and conceptualized evolution in terms of variation, selection, and heredity—a resemblance between parents and offspring—which can be measured at the phenotypic level without any knowledge of the underlying mechanisms. Once the science of genetics was born in the early twentieth century, however, it was treated as the only mechanism of inheritance, as if the only way for offspring to resemble to their parents was by sharing genes. This is patently false, but it has taken until now for evolutionists to return to their roots by thinking in terms of heredity, with genes as one mechanism of inheritance.

Eva Jablonka
Genetecist Eva Jablonka

This opens the door for studying the human capacity to transmit learned information across generations as both
a product of genetic evolution and an evolutionary process with its own inheritance mechanisms (see my “One Culture” essay and interview with Eva Jablonka (above left) for more).

To summarize, if large swaths of the biological and health sciences still need to absorb the meaning of Tinbergen's four questions, then the human related academic disciplines need to even more so. But wait! There's more!

Beyond the Ivory Tower

Beyond the Ivory Tower, there are legions of politicians, economists, and policy experts of all stripes charged with managing our affairs and making our world a better place. Most are college educated in topic areas that developed without reference to evolutionary theory since before they were born, however sophisticated these topic areas became in other respects. Some (especially politicians) are beholden to constituents who know even less, such as the roughly 50 percent of Americans who claim not to accept evolution and the other 50 percent who nominally accept it but who know scarcely anything about what this might mean for understanding and improving the human condition. If Tinbergen's four questions are needed inside the Ivory Tower, then they are needed outside the Ivory Tower even more so!

Improving literacy might seem like a hopeless quest, but I am actually optimistic, based on extensive experience since co-founding the Evolution Institute in 2008. Here I will report progress on three fronts: Social Darwinism, Evonomics, and Prosociality.

Social Darwinism: One reason that is often cited for the rejection of evolutionary theory in relation to human affairs is “Social Darwinism,” or the use of the theory to justify social inequality. Here is where a fine-grained analysis of scientific and social history, written in a way that is accessible to a broad audience, becomes essential, which TVOL has provided in a series of articles titled “Truth and Reconciliation for Social Darwinism.

It turns out that the term “Social Darwinism” has always been used as a pejorative for “laissez-faire,” or the justification of the status quo, much as it is used today. For example, when the U.S. Democratic President Barack Obama called Republican social policies “Social Darwinist,” he was saying that the policies benefit the rich at the expense of the poor, not that Republicans were relying upon evolutionary theory to support their claims. That would be ludicrous, since many Republicans profess to be creationists.

Adolf Hitler
Was Adolf Hitler a Darwinian?

Based on scholarship that already exists and merely needs to be made accessible to a broad audience, we can say with authority that Darwin's theory did not unleash a plague of toxic social policies justifying inequality. At most, it was added to a quiver that was already full of other arrows, including religious and economic justifications. The claim that Darwin's theory was used to justify Hitler's war policies, either directly or indirectly, is demonstrably false, as recounted in an article featuring the work of the historian of science Robert J. Richards entitled Was Hitler a Darwinian? No! No! No![10]

At the same time, Darwin clearly did influence progressive social reformers such as John Dewey, as I discuss with the philosopher Trevor Pearce in an interview titled “Was Dewey a Darwinian? Yes! Yes! Yes!”. But Dewey and other figures who used evolutionary theory to argue for social equality and mutual aid, including Peter Kropotkin, Thomas Huxley, and Darwin himself, are never called Social Darwinists. Go figure. The very enterprise of making an historical figure such as Darwin and his theory morally culpable for later applications is deeply problematic. Are chemists morally accountable for the use of their compounds in Hitler's gas chambers? As with other truth and reconciliation processes, this series of articles clears the air and enables a more positive and constructive exploration of social policy from an evolutionary perspective to take place.

Evonomics: The economics profession exists both inside and outside the Ivory Tower. Inside, it is supported by a mathematical edifice that looks impressive but is based on absurd assumptions about human abilities and preferences (“Homo economicus”) and the social environment in which economic transactions take place (e.g., that it is at equilibrium). The economist Paul Romer calls this “mathiness” and observes that it is used as a front to disguise ideology as science. The main competing school of thought, behavioral economics, challenges the orthodoxy on empirical grounds but has no theoretical framework of its own, resulting in a long list of results that appear anomalous and paradoxical against the background of orthodox theory. Some academic economists have concluded that there will be no replacement for orthodox theory. The Age of Big Theories is over and all we can do is play with data using whatever perspective we like.

Adam Smith, black and white, pen and ink
Moral philosopher Adam Smith, 1723–1790

Outside the Ivory Tower, policies are justified by appealing to iconic figures such as Adam Smith (left), John Maynard Keynes, Friedrich A. Hayek, and Milton Friedman in ways that bear little if any relationship to their actual work. Adam Smith's invisible hand metaphor is invoked in ways that would make him cringe. The fact that the novelist Ayn Rand is cited as much as the economic icons adds proof, if more is needed, that the entire show is driven by purpose-driven narratives, not science.

Again, I am optimistic that something can be done, despite the enormity of the problem, based on progress that has already been made. One key is to realize that progress needs to be made both inside (the science) and outside (the narrative) the Ivory Tower, with the science and narrative connected to each other more responsively and responsibly than in the past. On the science end, the Age of Big Theories is not over. When we step away from the encapsulated world of academic economics, we can see that two Big Theories are alive and well. The first is complex systems theory, which explains the dynamics of complex systems of all sorts. The second is evolutionary theory, which explains the dynamics of living systems of all sorts. Together, they provide a new scientific foundation for economics. My colleagues and I are communicating this message to academic economists through workshops, conferences, and their published outputs. For example, the lead article for a special issue of the Journal for Economic and Behavior Organization entitled “Evolution as a General Theoretical Framework for Economics and Public Policy” is explicitly framed in terms of Tinbergen's four questions,[11] and an edited volume entitled Complexity and Evolution: Toward a New Synthesis for Economics, based on a five-day conference organized with the help of Germany's Ernst Strüngmann Forum, has just been published by MIT Press.[12]

Ivory TowerExplaining all of this to a large and diverse audience outside the Ivory Tower, including the lay public, in addition to politicians, applied economists, and policy experts of all stripes, is easier than you might think. After all, Tinbergen's four questions are far, far easier to understand than orthodox economic theory! In addition to content on TVOL and SEF, the EI has assisted in the creation of Evonomics.com, which has achieved a circulation of a quarter million page views per month during its first year, including many thought leaders among its authors and readers. Check it out and judge for yourself how we are doing on the narrative front. My own assessment is that Tinbergen's four questions can be intuitive, appealing, and eminently useful on both sides of the Ivory Tower.

Prosociality: It is ironic that Social Darwinism is associated with the justification of ruthless competition, because the truth is just the reverse. A proper understanding of evolution in relation to human affairs reveals the importance of prosociality and identifies practical strategies for achieving it at scales ranging from small groups to the global village. Prosociality can be defined as any attitude, behavior, or institution oriented toward the welfare of others or one's group as a whole. It therefore includes behaviors that are labeled “cooperative” and “altruistic.”

Here are some examples of Tinbergen's four questions in action on the topic of prosociality. Starting with the function question, as a basic matter of tradeoffs, behaving for the good of one's group requires time, energy, and risk on the part of group members, which makes prosocial individuals vulnerable to passive free-riding and active exploitation by less prosocial individuals. This should be true for all social species, although the details will depend upon the ecological context of cooperation and the properties of the species (the history question, highlighting the importance of cross-species comparisons). A large family of models has been built and tested by behavioral ecologists, along the lines that I described for optimal foraging theory. E.O. Wilson (1975) called altruism “the central problem of Sociobiology”[6] and six chapters of the Introduction to Behavioural Ecology (fourth edition)[4] are devoted to various forms of prosociality.

Even though prosocial behaviors can evolve in theory and many cases have been documented, the same can be said about antisocial behaviors. This is a hard lesson to learn about nature. Many animal societies are highly despotic and unjust in human terms. Individuals stay in groups because to strike out on one's own would be even worse. Sexual conflict can be severe, with males pursuing their reproductive success in ways that are highly detrimental to females and vice versa, all depending upon the circumstances. In some species, the highest source of mortality on infants is members of the same species, killing the babies of others so that they can have their own.

The selection pressures favoring prosocial and antisocial behaviors are not static but can themselves evolve. When mechanisms evolve that suppress the advantages of disruptive self-serving competition within groups (the mechanism question), prosociality evolves to such an extent that the group becomes a higher-level organism. All of the entities that we currently recognize as individuals, such as single-celled and multicellular organisms, evolved not by small mutational steps from other individuals, but as highly regulated social groups of lower-level units—a process called a “major evolutionary transition.” This is something that was beyond Darwin's imagination.

Even more amazing, human genetic evolution can be understood as a major evolutionary transition. In chimpanzee and most other primate societies, members of a group cooperate to a degree, but are also each other's chief rivals. Even cooperation usually takes the form of small alliances that compete with other alliances within the same group. To the best of our current knowledge, our distant ancestors became adept at suppressing disruptive, self-serving behaviors within their groups, so that succeeding as a group became the primary evolutionary force. We are the primate equivalent of the eusocial insects (ants, wasps, bees, and termites), although most of the proximate mechanisms are of course very different (the history and mechanism questions).

The capacity to communicate with symbols and transmit large amounts of learned information (the mechanism question) is a form of prosociality and also an evolutionary process in its own right. This means that Tinbergen's four questions need to be asked for products of cultural evolution, no less than for products of genetic evolution. When human groups became bigger with the advent of agriculture, they outstripped our genetically evolved ability to enforce prosociality and became despotic, ironically more like chimpanzee societies than small-scale human societies (the history question). Despotic groups tend to fare poorly in intergroup competition with more internally prosocial groups, however, so cultural group selection, driven largely but not entirely by warfare, led to the mega-societies of today. Modern nations vary considerably in their degree of prosociality, expressed both internally and toward other nations. The same genetic and cultural evolutionary forces that brought us to our current condition are still operating.

Neolithic Revolution
Great Hall of Bulls, Lascaux, France / Paleolithic Europe, 15,000–13,000 BCE

Tinbergen's four questions have been especially insightful for the study of religion. Religions puzzle the scientific imagination because they seem both irrational and counterproductive. It's easy to understand why people would make blankets, but why would they burn them in sacrifice to imaginary agents for which there is no empirical evidence?

Two broad solutions have been proposed from the beginning of scholarship on the subject. First, religious beliefs and practices might be just as irrational and counterproductive as they seem and persist as byproducts of other beliefs and practices that are useful in non-religious contexts. Second, religious beliefs and practices might have a hidden logic and utility after all. Émile Durkheim was a proponent of the latter view, which is reflected in his famous definition of religions as:[13]

… a unified system of beliefs and practices relative to sacred things … which unite into one single moral community called a Church, all those who adhere to them.

However, more than 150 years of scholarship and analysis of religion have not resolved the issue. The study of religion from a modern evolutionary perspective started at the turn of the twenty-first century and has made impressive progress reaching a consensus. Religions are a fuzzy set comprising many beliefs and practices. As with all products of evolution, adaptations come with byproducts, but the idea that religions writ large are byproducts can be authoritatively rejected. Instead, most enduring religions are impressively designed to foster prosociality among members of the religious community, which is what Durkheim proposed, although the evolutionary perspective avoids many of the problems that became associated with the tradition of functionalism that he initiated.

A common distinction between the “vertical” and “horizontal” dimensions of religion maps intriguingly onto Tinbergen's “function” and “mechanism” questions. While religions are consistently designed to foster prosociality within religious groups, interactions among groups can range from highly prosocial to highly antisocial, depending upon the ecological conditions.

Holding HandsJames Coan's research described earlier takes the study of prosociality in a mechanistic direction. The line of research that led him to read An Introduction to Behavioural Ecology involved placing people in a brain scanner, stressing them with the possibility of an electrical shock, and measuring the effect of holding the hand of a loved one on the brain's response to the stress. Holding hands had a huge calming effect. In a second experiment, the loved one outside the scanner was the one being stressed with the possibility of an electric shock and the person inside the scanner was the one being supportive by holding hands. According to Coan, a skilled reader of brain scans would be required to tell the difference between someone being shocked and someone holding the hand of a loved one being shocked. Thanks to his newly acquired, four-question perspective, Coan now thinks of the brain as an organ that seamlessly integrates personal resources and social resources in making its trade-off decisions.

Research on prosociality can also be taken in a developmental direction. It is common for developmental psychologists to regard nurturing environments as optimal and harsh environments as debilitating, resulting in various pathologies comparable to a car breaking down. From an evolutionary perspective, nearly all species occupy a range of environments, from benign to harsh, during their evolutionary histories and are adapted to respond appropriately to the full range. Facultative responses to harsh environments include discounting the future and withholding prosociality toward others, since prosociality is not being extended to oneself. To say that these responses are facultative does not mean that they are voluntary. Many responses take place beneath conscious awareness and some aren't even cognitive in nature, such as an acceleration of sexual maturation. Developmental responses to harsh environments can begin before birth, can be difficult to reverse during the lifetime of the organism, and can be transmitted to offspring through epigenetic in addition to social inheritance mechanisms.

Public health efforts tend to be highly fragmented, with every problem considered in isolation. An evolutionary perspective helps us to see that prosociality is a master variable: Having it results in multiple assets and not having it results in multiple liabilities. If there could be only one policy prescription, it would be to foster prosocialilty.[14] The way to do this is to construct social environments that allow prosociality to succeed as a behavioral strategy in competition with less prosocial strategies. This can be done in a very practical way by implementing a number of core design principles that provide a strong group identity, prevent disruptive self-serving behaviors within the group, and cultivate appropriate relations with other groups. The Evolution Institute has developed a framework for coaching groups in the core design principles called PROSOCIAL. Please visit PROSOCIAL Magazine to learn more, including case studies of groups that have improved their efficacy by implementing the core design principles.

Advice for a College Applicant

Earlier I stated that the future is already here for a growing number of scientists and scholars who employ the four-question approach in all topic areas. In the spirit TheBestSchool.org's primary mission, here is some advice for students who wish to receive a fully rounded, four-question college education.

Now is a good time to start. Neo-Darwinism is not an advanced topic. Any inquiring person can learn the basics, especially when the relevance of neo-Darwinism to matters of importance is made clear. As you have probably gathered from reading this essay, once learned, Tinbergen's four questions can help you understand nearly everything that interests you in your personal and future professional life.

Don't expect it to come automatically. Academic culture can be surprisingly conservative. A decade or more can be required for new developments in science and scholarship to find their way into textbooks. At the vast majority of colleges and universities worldwide, evolution is still taught as a biological topic. Even if you become a biology major, many of your courses will focus on mechanisms in a way that crowds out the other three questions. If you major in a human-related topic, most of your professors will have had little or no training in evolution during their own higher education, although some will have picked it up on their own.

The best education is self-education. Given this somewhat bleak assessment, it's up to you to seek out a four-question education. The more you can learn on your own, the better you will be able to direct your search. I wrote my book Evolution for Everyone: How Darwin's Theory Can Change the Way We Think About Our Lives (Delacorte Press, 2007) with this in mind. Chapter 10, which begins on page 63, is titled “Your Apprentice License,” which means that I was able to provide the basics in the previous nine short chapters. The remaining 26 chapters apply the basics to a smorgasbord of biological and human-related topics. From there (or even before), I suggest perusing the articles on This View of Life, which cover “anything and everything from an evolutionary perspective.” Then just follow your bliss. Whatever interests you, it is likely that others have started to approach it from an evolutionary perspective—although there will still be plenty of uncharted territory for you to explore!

Seek out the professors who are at the forefront of what interests you. Once you have refined your own interests, you can check out the colleges and universities that include the leaders in those areas. Are you aiming for medical school? Then check out Arizona State University, home of the Center for Evolution and Medicine, or a consortium of four universities in North Carolina that have created the Triangle Center for Evolutionary Medicine.

Are you fascinated by cultural anthropology? Try UCLA, UC Davis, or Harvard. The Arts? Check out the NeuroArts Lab at McMaster University in Ontario, Canada. Don't be shy about emailing professors directly. Most of them are dedicated teachers who will be impressed by your initiative and willing to take a few moments to advise you. Tell them that you have become interested in evolutionary theory and in their research area. Ask for their opinion about their institution as a place where an undergraduate student can get a good evolutionary education and what other institutions they might recommend. Ask about opportunities for working with them and/or their graduate students.

Evolution for EveryoneCheck out EvoS programs and their equivalents. Only a handful of colleges and universities feature a campus-wide evolutionary studies program for undergraduate students and most of them are based on the EvoS program that I started at Binghamton University in 2003. If you came to Binghamton, you could earn a certificate in Evolutionary Studies in parallel with any major. You could take our 100-level “Evolution for Everyone” course during your first semester to learn the basics. Then you could choose from a menu of other courses to deepen your knowledge in the topic areas that interest you.

You could join the EvoS undergraduate student club to socialize with like-minded individuals and with graduate students in the EvoS Graduate Student Association. You would find it comparatively easy to start working with EvoS faculty participants and their graduate students. You would be required to take the two-credit “Current Topics in Evolutionary Studies” seminar at least twice. This course is built around the campus-wide EvoS seminar series, which brings approximately 10 speakers to campus every semester to speak on “anything and everything” from an evolutionary perspective.

In preparation for each seminar, EvoS students are required to read one or more articles from the primary literature, write a commentary due before the seminar, attend the seminar, and attend an extended discussion with the speaker following the seminar. Students who earn the EvoS certificate will have repeated this experience 20 different times for different topics, along with the four-credit courses that they have taken and their research experiences—all in parallel with their conventional major.

Please visit the EvoS Consortium website for a list of colleges and universities that offer multicourse programs such as the one that I direct at Binghamton, along with programs under development. I think you can see how such programs create synergies that go beyond individual professors and their research programs. But don't take my word for it—here is how one EvoS student at Binghamton named Benjamin Seitz expressed the value of his education (go here for more).

Ultimately, what the EvoS program does here is provide undergraduates with the opportunity to function as graduate students. Every week, we are exposed to researchers from around the world, who share a similar passion for evolutionary studies. Not only do these speakers broaden our exposure to current research in the field, but they provide phenomenal networking opportunities for those of us wishing to pursue careers in academia. On top of this, the EvoS program encourages self-learning and the pursuit of knowledge for the sake of pursuing knowledge. The evolutionary toolkit, which is so feverishly promoted by the EvoS program, is a phenomenal catalyst for stimulating intellectual discussion. It is a tool and a perspective that once turned on, is seemingly impossible to turn off.

Lastly, the EvoS program provides a community on campus. When I was in high school and looking at colleges, I was torn between the intimacy of small liberal arts colleges and the vast possibilities offered at large research intuitions. I knew I wanted to get involved in research, but I figured the best way to do so would be to go to a tiny college where I could get to build strong relationships with my professors, and perhaps have a beer with them if I was lucky. Fortunately, I ended up at a large research institution, and the intimacy that I was seeking from a small college I found immediately from the EvoS program. It's a rather simple formula really: bright and welcoming people, who share a common interest and understanding of the world, who are highly encouraging and respectful to all those interested in getting involved. That's how I see the EvoS Program here at Binghamton, and this program will by far be what I cherish most about my four years here.

Is Neo-Darwinism Enough for the Experts?

So far, I have made the case that the Neo-Darwinian revolution is far from complete and that its completion will be transformative for both academic knowledge and our practical ability to make the world a better place. Against this background, it is a distraction to say that neo-Darwinism is not enough.

Some readers might be willing to grant me this claim but might still argue that neo-Darwinism is not enough for the experts at the cutting edge of evolutionary science. In this final section of my essay, I will argue that neo-Darwinism is enough for the experts. My argument will be consistent with enthusiastic support for the so-called “extended evolutionary synthesis” (EES).[15]

Massimo Pigliucci
Massimo Pigliucci, Professor of Philosophy at CUNY-City College

Terms such as “paradigm,” “research program,” and “synthesis” are used loosely by scientists and the lay public, often in ways that are self-promoting, but they are also used in more careful ways by historians and philosophers of science to understand continuities and discontinuities in the scientific process. Massimo Pigliucci (right), who has a Ph.D. in both philosophy of science and evolutionary biology, carefully coined the term “extended evolutionarysSynthesis” to signal continuity. He described it to me this way during a 2016 interview.

Now for the key concept of “synthesis.” This is not a philosophical term [in contrast to “paradigm” and “research program”, as it was introduced by [Julian] Huxley with the title of his famous book (Evolution: The Modern Synthesis) [1942]. What he meant to convey was the idea that the MS was not something radically different from Darwinism and neo-Darwinism (the late 19th century modification of the original theory that got rid of Lamarckian influences, largely thanks to the work of August Weissman and Alfred Wallace). Rather, it was a merging, a reconciliation, of Darwinism with the new discoveries coming out of genetics, and in particular the demonstration, achieved by Ronald Fisher, that Darwinism and Mendelism were not at all at odds with each other, as many thought at the time. The Synthesis then got expanded to a number of additional disciplines, from natural history to zoology and botany, and of course to paleontology (but, crucially, not to embryology and developmental biology).

It is in this same sense that most proponents of an Expanded Synthesis use the term: we don't think that we are witnessing a Kuhnian paradigm shift, or the replacement of a Lakatosian research program by another one. We are, however, in need of explicitly and organically incorporating into the framework of the MS a number of new discoveries and concepts (phenotypic plasticity, epigenetic inheritance, evolvability, and so forth) that were unknown to, or unappreciated by, the architects of the Modern Synthesis.

Richard B. Goldschmidt
Geneticist Richard B. Goldschmidt, 1878–1958

Like Richard Lewontin, Pigliucci appreciates the personal and sociological aspects of science in addition to the intellectual aspects.

We tend to forget that science is a human enterprise, and as such—at the least in the short run—affected by social dynamics and power struggles. One of the dominant personalities during the period in which the MS congealed was Ernst Mayr, who staunchly defended a number of notions that were important to him (such as allopatric speciation), and equally forcefully rejected others that didn't fit his view of evolution (such as G.G. Simpson's distinction between bradytelic and tachytelic evolution). It was Mayr who famously justified the exclusion of developmental biology from the Synthesis on the basis that, allegedly, developmental biologists were simply not interested in evolution. In fact, many were, but subscribed to views more similar to those of the famous geneticist Richard B. Goldschmidt (left), who proposed the idea of “hopeful monsters” to account for speciation and for major transitions in the fossil record. That idea didn't sit well with Mayr's emphasis on gradualism, and was accordingly purged from the canon, despite Goldschmidt's stellar reputation at the time. Today we think that the notion of hopeful monsters was indeed misguided, but also that Goldschmidt was more prescient than Mayr in understanding the fruitful interaction between genetics and developmental biology—something that nowadays goes under the name of “evo-devo.”

The evolutionary biologist Kevin Laland has taken a leadership role in developing the EES, including a major grant from the John Templeton Foundation that will fund over 20 research projects. He also emphasizes continuity in my 2016 interview with him, from which the following is taken.

I was drawn to thinking about these issues through my research on niche construction, with John Odling-Smee (Oxford) and Marc Feldman (Stanford). John was a participant at the Altenberg meeting (organized by Pigliucci), and he and I, together with evolutionary ecologist Tobias Uller (then Oxford, now Lund), began discussing whether there was a conception of the EES that could do useful work. We had no sympathy with the argument that evolutionary biology was undergoing a “paradigm shift”—to my mind paradigm shifts are an outdated notion (sciences change more through gradual evolution than dramatic revolution). Nonetheless, we were very conscious of how academic fields possess conceptual frameworks—ways of thinking—that influence what questions are asked, what data is collected, and how that data is interpreted. Here, alternative perspectives can be of real value to the extent that they encourage researchers to generate and test novel hypotheses, or open up new lines of inquiry. That is how we envisaged the EES could be of service—as an alternative way of thinking about evolution, which could be deployed alongside traditional perspectives to stimulate innovative research.

However, any such alternative needs to be formulated in a disciplined way. We noted that certain literatures—for instance, those concerning developmental bias, developmental plasticity, and expanded views of inheritance—stood out as being open to both traditional and progressive interpretations, leaving them lying squarely on the fault line. In all cases, the more progressive reading emphasized an organism-centered perspective, rejected the idea that development was controlled by a genetic program, and recognized that developmental processes played important (and not fully appreciated) evolutionary roles. It made sense to conceptualize the EES as an eco-developmental perspective, and to highlight these literatures as the intellectual territory on which an EES might focus.

None of these considerations require going beyond Tinbergen's four questions, although they do highlight the relative neglect of the “development” question during the middle of the twentieth century, which began to be remedied with the advent of the “evo-devo” movement (this term was coined in the 1990s).

Here are three examples of major developments in evolutionary science that still fall squarely within neo-Darwinism as I have defined it. I will focus on my own research projects, not because I think I made outsized contributions, but because of my familiarity with them. If my research can be called distinctive, it is by showing how someone equipped with Tinbergen's four questions can parachute into nearly any topic area and make a contribution as measured by the gold standard of expertise in science—peer-reviewed publications.

Multi-level selection. George C. Williams started to write Adaptation and Natural Selection (1966) in the late 1950s to correct what he regarded as sloppy thinking about evolution. His Ph.D. training at UC Berkeley included population genetics, which made it second nature for him to think about natural selection in terms of relative fitness. It doesn't matter how well an organism survives and reproduces in any absolute sense, only that it does so better than other organisms in its vicinity. Relative fitness creates the problem that group selection is needed to solve. As a basic matter of trade-offs, the traits that maximize relative fitness within a social group are unlikely to benefit the group as a whole. Traits that are “for the good of the group” require time, energy, and expense on the part of group members that can be exploited by passive free-riding and active exploitation by other group members. For these traits to evolve, there must be a process of selection among groups in a multi-group population, which is largely opposed by selection among individuals within groups.

Darwin understood this, but many scientists during the first half of the twentieth century, including ecologists who were newly learning about evolution, naively assumed that adaptations could evolve at the level of individuals, groups, species, and ecosystems without needing to distinguish among the levels. When the need for multiple levels of selection was acknowledged, it was often assumed that higher-level selection easily trumped lower-level selection. As one of the most widely used ecology textbooks of the 1950s put it, the prevailing law of nature was “all for one and one for all.”[16]

In his effort to combat this kind of naïve adaptationism, Williams asserted that it was most parsimonious to invoke individual-level selection and to require proof for putative examples of higher-level selection. Based on his own review, he concluded that higher-level selection was almost invariably trumped by lower-level selection, so that “group-level adaptations do not, in fact, exist.” If individuals appear to behave for the good of their groups, then their apparent altruism needs to be explained as a form of self-interest.

By the time Adaptation and Natural Selection was published in 1966, W.D. Hamilton had published his theory of inclusive fitness,[17] which showed how individuals could evolve to benefit “their” genes in the bodies of their genetic relatives. Then, Robert Trivers introduced the concept of “reciprocal altruism” in 1971,[18] which explained apparent altruism in terms of return benefits to the altruist. These two new theoretical frameworks, coupled with Williams's skeptical analysis of group selection and invocation of parsimony, made group selection appear as dead within evolutionary theory as Lamarckism. When I began graduate school that year, it was almost mandatory for authors to assure their readers that they were not invoking group selection.

George R. Price
Population geneticist George R. Price, 1922–1975

But that is also when the tide began to turn. An obscure theoretical biologist named George R. Price (left) created an equation that statistically partitioned natural selection in a multi-group population into within- and between-group components. When W.D. Hamilton compared his theory of inclusive fitness to the Price Equation, he was shocked to discover that they were equivalent.[19] His own formulation obscured the fact that when social interactions take place among genetic relatives, there are multiple groups. Sometimes, the groups are spatially defined, as when a butterfly lays a clutch of eggs on a leaf. Sometimes, the groups are behaviorally defined, as when an individual preferentially interacts with a relative and avoids interacting within non-relatives. Either way, the evolving population is composed of multiple local groups as far as the social interactions are concerned. This fact, which might seem obvious in retrospect, was made clear to Hamilton by the Price Equation, which also showed that altruism is selectively disadvantageous within kin groups and requires selection among kin groups to evolve. Hamilton wasn't wrong about genetic relatedness as an important factor for the evolution of altruism, but he was wrong to regard his theory as an alternative to group selection, as he announced to the world in a 1975 article.[20]

That was also the year that I published my first article on group selection,[21] which noted that social interactions almost invariably take place among sets of individuals that are small compared to the total evolving population. If these sets of individuals (I called them “trait-groups”) are regarded as the groups of a multilevel selection model, then traits conceptualized as only “apparently” altruistic in kin selection and reciprocal altruism models are “really” altruistic, in the sense that they are selectively disadvantageous within trait-groups and require selection among trait-groups to evolve. My algebraic model was different from Price's statistical model, but both made the same basic point.

A very important new concept for the history and philosophy of science was emerging that has become known as “equivalence.”[22] In the standard portrayal of science, alternative hypotheses invoke different causal explanations of a given phenomenon, such that one can be shown to be right and the other wrong on the basis of empirical evidence. Even paradigms are replaced by other paradigms, although the process is messier and more protracted. No one (other than historians) talks about pre-Copernican views of the solar system any more.

But some alternative explanations are not like that. Rather than invoking different causal processes, they invoke the same causal processes from different perspectives. As such, they deserve to coexist to the extent that the different perspectives offer novel insights. Familiar analogies from everyday life include different financial accounting systems, different languages, and viewing complex objects such as a mountain from different directions.

The history of the group selection controversy from 1975 to the present is the history of confusing theories that offer different perspectives on the same causal processes with theories that invoke different causal processes. Here is the sober assessment of two philosophers of science, Jonathan Birch and Samir Okasha in a 2014 article:[23]

In earlier debates, biologists tended to regard kin and multilevel selection as rival empirical hypotheses, but many contemporary biologists regard them as ultimately equivalent, on the grounds that gene frequency change can be correctly computed using either approach. Although dissenters from this equivalence claim can be found, the majority of social evolutionists appear to endorse it.

Why four decades were required to reach this consensus will be a juicy topic of conversation among historians of science for years to come. Personal and sociological factors were almost certainly involved, as Lewontin and Pigliucci have stressed for other aspects of evolutionary thought. It probably wasn't a coincidence that the “everything is selfish” perspective among evolutionists coincided with a similar perspective in economics and methodological individualism in the social sciences during the second half of the twentieth century. In any case, the entire controversy is primarily a clarification of Tinbergen's “function” question and does not require going beyond the four-question approach.

Chaos: Making a new ScienceComplex systems theory. In his book Chaos: Making a New Science (Viking, 1987), James Gleick described how the study of complex systems was retarded by theorists who regarded analytical mathematical models as superior to other modeling approaches, such as computer simulations—and therefore ignored interactions that were too complex to model with analytical equations. For this and other reasons, the formal study of complex systems is remarkably recent. The institute most closely associated with complex systems theory, the Santa Fe Institute, was founded in 1984.

Complex systems theory can be said to be more general than evolutionary theory because it covers complex systems of all sorts, living and non-living. Pioneers of complex systems theory include some biologists, such as Robert May, whose work on chaotic population dynamics is described in Gleick's book, but also many non-biologists specializing in the study of complex physical systems such as the weather or computer simulation models such as English mathematician John H. Conway's “Game of Life” (below left), in which “agents” following simple rules interact to produce an amazing variety of system-level behaviors.

Game of Life Screen Capture
John H. Conway’s “Game of Life”

Complex systems theory has profound consequences for all four of Tinbergen's questions. On the other hand, complex systems theorists who are not biologists are likely to be naïve about Tinbergen's four questions, however brilliant they may be in other respects. I mean no disrespect by making this statement. I am merely observing that the same process of integration that took place in topic areas such as animal behavior, ecology, and population genetics decades earlier is now needed for complex systems theory. Why should it be otherwise?

The key term “complex adaptive system” (CAS) provides an example.[24] It has at least two meanings: A complex system that is adaptive as a system (CAS1); and a complex system of agents that follow adaptive strategies (CAS2). Examples of CAS1 include social insect colonies, brains, and the immune system. Examples of CAS2 include multispecies ecosystems, crowds, and the stock market. If you visit the Wikipedia entry for “complex adaptive system” (or some other, more authoritative source, if you like), you will see both CAS1 and CAS2 systems lumped under a single label as if there is no need to distinguish between them. This signals confusion about units of functional organization—the very problem that is addressed by multilevel selection theory.

Complex interactions can produce lots of pattern at the system level, but they are no more likely than a point mutation to produce adaptive pattern without a process of selection. Once this foundational point is grasped, then we can proceed to study how multilevel selection operating on complex systems differs from multilevel selection operating on more simple systems. For example, in models that assume a simple relationship between genes and phenotypic traits (e.g., a single genetic polymorphism that codes for altruism vs. selfishness), phenotypic variation among groups is directly proportional to genetic variation among groups. If groups are formed by drawing N individuals at random from a large population, then the amount of genetic and phenotypic variation among groups will decline rapidly with the value of N as an inevitable consequence of sampling error. This is one reason why genetic relatedness (= groups initiated by a small number of individuals) is considered so important for the evolution of altruism.

Multiple Microbial Generations
Multiple Microbial Generations

Now, let's assume a more complex genotype-phenotype relationship. Instead of coding directly for a given phenotypic trait, genes code for component traits that interact with each other to produce the phenotypic trait. With this alteration of the model, something magical happens. Genetic variation among groups declines with N, as before, but phenotypic variation among groups can remain high, even with very large values of N. This is because even tiny initial differences among groups don't remain tiny, but can be magnified by complex interactions taking place within each group. This is called “sensitive dependence on initial conditions” and also explains why the weather is unpredictable and how a small genetic change in an organism (such as a single-nucleotide substitution) can be magnified by developmental processes to result in a large phenotypic change.

The bottom line is that selection at the level of higher-level units such as single-species groups and multi-species communities might be much more potent than expected on the basis of simple models. To test this hypothesis, William Swenson and I created microbial ecosystems in the laboratory that were initiated by many hundreds of species and millions of individuals from a single well-mixed source.[25] Initial variation among the ecosystems, based on sampling error, was vanishingly small. Nevertheless, these differences did not remain small, but grew larger during the course of a few days and weeks (= many microbial generations) based on complex interactions taking place within each ecosystem. The differences in species composition and the genetic composition of each species influenced measurable properties of the ecosystems, such as pH or the ability to degrade a toxic compound. When ecosystems were selected on the basis of these properties and used colonize a new set of ecosystems, there was a response to selection, which is proof of ecosystem-level heritability. In short, we demonstrated that ecosystems can be selected for their properties in much the same way as individuals, which appeared theoretically impossible based on simpler models.

This research was published in 2000 as two articles in journals that are hard to ignore (Proceedings of the National Academy of Sciences and Environmental Microbiology)—but nevertheless they were largely ignored. Many evolutionists were still in denial about multilevel selection and many microbiologists focused on mechanisms to the exclusion of Tinbergen's other three questions. The fact that our inquiry was led by Tinbergen's “function” question and could inform the study of mechanisms did not impress such microbiologists—including the reviewers of grants that we submitted to continue the research.

Two thousand was also the year that the term “microbiome” started to be used with increasing frequency. By now, it is widely appreciated that every multicellular organism is inhabited by an ecosystem of microbes and other small creatures in numbers that often exceed that of the organism's own cells. Selection at the level of the microbiome has become impossible to ignore and other laboratories are beginning to continue the line of research initiated by Swenson and myself, with a greater capacity to address all four of Tinbergen's questions than we had.[26] For the purpose of this essay, the main point to stress is that complex systems theory is profoundly relevant to Tinbergen's four questions without necessitating going beyond them.

Evolution as a directed process. One of the dogmas that became established early during the history of evolutionary thought, thanks largely to August Weismann, is that phenotypic variation, while not necessarily random in the strict sense of the word, is nevertheless arbitrary and undirected with respect to the traits that are being selected. Anything that smelled of directed evolution was branded with the label “Lamarckian” and declared impossible, much as group selection was declared impossible during the 1960s and 70s.

Backing away from this dogmatic position is an important part of the extended evolutionary synthesis. For me, the best way to think about directed evolution is to focus on animal behavior, which brings the arc of this essay back to Tinbergen. In the conventional view of natural selection, mutations are not directed, but they result in the evolution of behaviors that are indubitably directed. Optimal foraging behavior is anything but random or arbitrary with respect to searching for prey!

James Mark Baldwin
Philosopher and psychologist James Mark Baldwin, 1861–1934

Since the work of James Mark Baldwin (left),[27] we have known that directed behaviors that are a product of undirected evolution can double back to influence the evolutionary process. What the organism chooses to do by learning alters the selection pressures operating on the genes of the organism. This was celebrated as a major insight at the time—a form of directed evolution that was fully consistent with Weismann's doctrine—but very little was done with it over the ensuing decades.

In the meantime, the study of behavior became increasingly sophisticated, including the distinction between closed and open forms of phenotypic plasticity. In closed forms, the behavioral alternatives are genetically programmed and triggered by environmental cues, such as a tadpole that is prepared at birth to either forage or seek a refuge, depending upon the chemical scent of its predator.

In open forms, organisms vary their behavior in a relatively open-ended fashion and adopt the behaviors that are most rewarding, such as a rat that learns to press a lever to receive food in a Skinner box. The capacity to learn in an open-ended fashion evolved by genetic evolution—for example, reinforcers such as pleasure and pain are genetically programmed, but they result in behaviors that are not genetically programmed, such as the pigeons that Skinner reinforced to play ping pong.

Open forms of phenotypic plasticity are properly regarded as evolutionary processes built by other evolutionary processes, or “Darwin machines” to use the felicitous phrase coined by William Calvin and elaborated upon by Henry Plotkin.[28] Unlike genetic evolution, Darwin machines are expected to be directed forms of evolution, although they must also have an arbitrary component to remain open-ended. When Darwin machines become transgenerational through forms of social learning found in many species and forms of symbolic thought that are distinctively human, there should be no stigma whatsoever about the fact that they are partially directed.

A point I made about An Introduction to Behavioural Ecology as a maturation of what Tinbergen, Lorenz, and von Frisch started, is that the distinction between behavioral traits and non-behavioral traits became blurred. To most people, the length of the small intestine is not a behavioral trait. Yet, it can grow longer or shorter depending upon the foraging ecology of a species and is even a phenotypically plastic trait in some species, which means that it can become shorter or longer within an individual, depending upon what it eats. In many frog species, tadpoles don't just change their foraging behaviors depending upon the scent of a predator; they undergo a whole-body makeover.

In the same way, ideas about directed evolution that have been worked out for the study of behavior are applicable to traits that are not customarily regarded as behavioral, such as genetic and epigenetic inheritance mechanisms, the immune system, developmental programs, and neural processes in the brain. Rigid adherence to Weismann's doctrine should be declared thoroughly obsolete, along with rigid rejection of group selection. These are profound advances in evolutionary thought, but they do not require going beyond Tinbergen's four questions. If anything, they require a proliferation of Tinbergen's four questions for every evolutionary process that is built by another evolutionary process.


Charles Darwin
Naturalist and geologist Charles Darwin, 1809–1882

In this essay I have strived to show that the neo-Darwinian revolution is far from complete—in the biological sciences, in the human-related sciences and humanities, in economics, government, and public policy, and in higher education. Even the most advanced topics associated with the term “extended evolutionary synthesis” operate within the framework of four questions that must be addressed for all products of evolution, concerning their function, mechanism, development, and phylogeny.

Completing the neo-Darwinian revolution will be transformative and quite frankly essential for solving the problems of our age. Unless we can become wise managers of evolutionary processes, then evolution will take us where we don't want to go.[29]

Luckily, Tinbergen's four questions are sufficiently simple to learn and employ, once their relevance is understood, that widespread literacy is within reach.

Join the Dialogue!

Share your thoughts in the comments section below …while the comments are still open!



1.  M. Pigliucci and G.B. Müller, eds., Evolution—The Extended Synthesis. Cambridge, MA: MIT Press, 2010.

2.  N. Tinbergen, “On aims and methods of ethology,” Zeitschrift für Tierpsychologie, 1963, 20: 410–433.

3.  E. Mayr, “Cause and Effect in Biology,” Science, 1961, 134(3489): 1501–1506.

4.  N.B. Davies, J.R. Krebs, and S.A. West, An Introduction to Behavioural Ecology, 4th ed. Chichester, UK: Wiley-Blackwell, 2012.

5.  T. Dobzhansky, “Nothing in biology makes sense except in the light of evolution,” American Biology Teacher, 1973, 35: 125–129.

6.  G.C. Williams and R.M. Nesse, “The Dawn of Darwinian Medicine,” Quarterly Review of Biology, 1991, 66: 1–22; and R.M. Nesse and G.C. Williams, Why We Get Sick: The New Science of Darwinian Medicine. New York: Times Books, 1995.

7.  E.O. Wilson, Sociobiology: The New Synthesis. Cambridge, MA: Harvard University Press, 1975.

8.  C. Darwin, The Descent of Man, and Selection in Relation to Sex, two vols. London: John Murray, 1871.

9.  C.P. Snow, The Two Cultures. Cambridge: Cambridge University Press, 1959.

10.  See R.J. Richards, Was Hitler a Darwinian? Disputed Questions in the History of Evolutionary Theory. Chicago: University of Chicago Press, 2013.

11.  D.S. Wilson and J.M. Gowdy, “Evolution as a general theoretical framework for economics and public policy,” Journal of Economic Behavior and Organization, 2013, 90(Supplement): S3–S10. (http://doi.org/10.1016/j.jebo.2012.12.008)

12.  D.S. Wilson and A. Kirman, eds., Complexity and Evolution: Toward a new Synthesis for Economics. Cambridge, MA: MIT Press, 2016.

13.  É. Durkheim, The Elementary Forms of the Religious Life. London: George Allen & Unwin, 1915; numerous editions. (Originally published as Les formes ÉlÉmentaires de la vie religieuse in 1912.) [The passage cited occurs near the end of Book 1, “Preliminary Questions,” Chapter 1, “Definition of Religious Phenomena and of Religion,” on p. 62 of the 1965 Free Press paperback edition—eds.]

14.  A. Biglan, The Nurture Effect: How the Science of Human Behavior Can Improve Our Lives and Our World. Oakland, CA: New Harbinger Publications, 2015.

15.  K.N. Laland, T. Uller, M.W. Feldman, K. Sterelny, G.B. Müller, A. Moczek, E. Jablonka, and J. Odling-Smee, “The extended evolutionary synthesis: its structure, assumptions and predictions,” Proceedings of the Royal Society of London B, 2015, 282(1813): 20151019. (http://dx.doi.org/10.1098/rspb.2015.1019)

16.  W.C. Allee, A.E. Emerson, O. Park, T. Park, and K.P. Schmidt, Principles of Animal Ecology. Philadelphia: Saunders, 1949.

17.  W.D. Hamilton, “The genetical evolution of social behavior: I and II,” Journal of Theoretical Biology, 1964, 7: 1–52.

18.  R.L. Trivers, “The evolution of reciprocal altruism,” Quarterly Review of Biology, 1971, 46: 35–57.

19.  For a book-length account, see O.S. Harmon, The Price of Altruism. New York: Norton, 2010.

20.  W.D. Hamilton, “Innate social aptitudes in man: an approach from evolutionary genetics,” in R. Fox, ed., Biosocial Anthropology. London: Malaby Press, 1975; pp. 133–155.

21.  D.S. Wilson, “A general theory of group selection,” Proceedings of the National Academy of Sciences, USA, 1975, 72: 143–146.

22.  For an accessible review, see Chapter 3 of D.S. Wilson, Does Altruism Exist? Culture, Genes, and the Welfare of Others. New Haven, CT: Yale University Press, 2015.

23.  J. Birch and S. Okasha, “Kin Selection and Its Critics,” BioScience, 2014, 65(1): 22–32. (http://doi.org/10.1093/biosci/biu196)

24.  D.S. Wilson, “Two meanings of complex adaptive systems,” in D.S. Wilson and A. Kirman, eds., Complexity and Evolution: A New Synthesis for Economics. Cambridge, MA: MIT Press, 2016 (in press).

25.  W. Swenson, J. Arendt, and D.S. Wilson, “Artificial selection of microbial ecosystems for 3-chloroaniline biodegradation,” Environmental Microbiology, 2000, 2: 564–571; and W. Swenson, D.S. Wilson, and R. Elias, “Artificial Ecosystem Selection,” Proceedings of the National Academy of Sciences, USA, 2000, 97: 9110–9114.

26.  For example, K. Panke-Buisse, A.C. Poole, J.K. Goodrich, R.E. Ley, and J. Kao-Kniffin, “Selection on soil microbiomes reveals reproducible impacts on plant function,” The ISME Journal, 2015, 9: 980–989. (doi:10.1038/ismej.2014.196)

27.  J.M. Baldwin, “Development and Evolution,” Philosophical Review, 1903, 12(4): 442–451.

28.  W.H. Calvin, “The brain as a Darwin machine,” Nature, 1987, 330: 33–34; H. Plotkin, Darwin Machines and the Nature of Knowledge. Cambridge, MA: Harvard University Press, 1994.

29.  D.S. Wilson, S.C. Hayes, A. Biglan, and D. Embry, “Evolving the Future: Toward a Science of Intentional Change,” Behavioral and Brain Sciences, 2014, 37: 395–460.

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