The (ongoing) evolution of evolutionary theory

by Massimo Pigliucci

Nature magazine recently ran a “point-counterpoint” entitled “Does evolutionary theory need a rethink?” [1] Arguing for the “Yes, urgently” side were Kevin Laland, Tobias Uller, Marc Feldman, Kim Sterelny, Gerd B. Müller, Armin Moczek, Eva Jablonka, and John Odling-Smee. Arguing for the “No, all is well” thesis were Gregory A. Wray, Hopi E. Hoekstra, Douglas J. Futuyma, Richard E. Lenski, Trudy F. C. Mackay, Dolph Schluter, and Joan E. Strassmann.

That’s a good number of top notch evolutionary biologists, colleagues that I very much respect, on both sides of the aisle. My own allegiances have been made clear in a number of papers [2] and a co-edited book [3]. I have been arguing for some time now for what I consider the moderate-yes side of the debate: yes, evolutionary theory does need (and is, in fact, getting) an update, but that update is yet another expansion along the same trajectory that has moved us from the original Darwinism to the so-called neo-Darwinism to the Modern Synthesis to the (ongoing) Extended Synthesis (more on all of these in a moment). This expansion has nothing to do with hyped claims of rejection of the Darwinian tenet of natural selection, resurgence of Lamarckism, and so forth. (Cue immediate snarky commentary by the Discovery Institute.) Indeed, I have chastised more than once some of my more, shall we say, enthusiastic, colleagues (including, among the above listed authors, Eva Jablonka) for unwittingly creating a backlash among “conservatives” by talking about Lamarck and the death of Darwinism.

That said, I wasn’t going to chime in about the Nature commentaries because I had made my case plenty of times before, and also because I think I see the tide (among the all-important young practitioners of the field) moving our way, so why bother. It is interesting, and both amusing and flattering, for instance, to see that in recent years I have almost without exceptions been invited to talk about these issues by groups of graduate students around the country, but rarely by older colleagues. (I guess Planck was right, if a bit harsh, when he famously said: “A new scientific truth does not triumph by convincing its opponents and making them see the light, but rather because its opponents eventually die, and a new generation grows up that is familiar with it.”)

Why, then, am I writing this essay? Because my friend Sean Carroll (the cosmologist, not the evolutionary developmental biologist) commented on the Nature articles, and took the wrong side! [4] I was surprised, because Sean is usually fair and open minded, and rarely comments on fields that are so far from his own. I must admit I was also slightly piqued by the fact that it didn’t occur to him to check with me before publishing his essay (it’s not hubris, it’s just that I often check with him whenever I write something about quantum mechanics or cosmology, because you know, they ain’t my field).

Be that as it may, let me start with what Sean gets wrong, then zoom out to explore the broader picture so that the controversy can be seen in its proper context.

Sean states, near the beginning of his commentary: “I’m a complete novice here, so my opinion should count for almost nothing. But from reading the two arguments, I tend to side with the gradualists on this one.” At least some of the basis of his position seems to be his impression that the “yes” side has engaged in ad hominem attacks on their opponents, an example of which (from the Nature exchange) is the following:

“Too often, vital discussions descend into acrimony, with accusations of muddle or misrepresentation. Perhaps haunted by the spectre of intelligent design, evolutionary biologists wish to show a united front to those hostile to science. Some might fear that they will receive less funding and recognition if outsiders — such as physiologists or developmental biologists — flood into their field.”

I must admit (and I’m certainly biased) that this hardly sounds like ad hominem. It is a reasonable, if unwelcome, analysis of the sociology and psychology underlying the debate. It is definitely the case that evolutionary biologists are worried by the specter of ID. I’m not so sure about the bit concerning funding, though with current levels of NSF approval of research grants as low as 6% that’s not entirely out of the question either.

Moreover, though Sean couldn’t possibly know this, the other side has also engaged in quite a bit of harsh commentary. Here, for instance, is what my colleague Jerry Coyne said to Nature back in 2008, commenting on a conference that I organized in Vienna about the Extended Evolutionary Synthesis [5]:

“The whole thing about natural selection being an insufficient paradigm seems grossly overblown. There are a lot of interesting new things coming out that will change our view of evolution. But to say the modern synthesis is incomplete or fatally flawed is fatuous. … People shouldn’t suppress their differences to placate creationists, but to suggest that neo-Darwinism has reached some kind of crisis point plays into creationists’ hands.”

To think that scientific controversies are just about the science, and that personalities, social allegiances, and of course money, don’t play any significant role in them, is a bit naive, and I take it that Sean was joking when he concluded his post with: “Fortunately physicists are never like this! It can be tough to live in a world of pure reason and unadulterated rationality, but someone’s got to do it.”

Let us now move back to what the actual scientific controversy is about. To do this, I will have to provide a very brief overview of the history of evolutionary theory. Bear with me, I think it’s worth it. [6]

It all began [7], as it is well known, in 1858, when Charles Darwin and Alfred Russel Wallace presented a joint paper on evolution and natural selection at a meeting of the Linnean Society [8]. The paper was swiftly followed by Darwin’s publication, the following year, of On The Origin of Species, a bestseller that quickly eclipsed Wallace’s own contribution.

The twin foundational concepts underlying the Darwinian theory are common descent and natural selection. The idea is that all living organisms are related to each other, and that the major (though, crucially, even then, not the only) mechanism that explains their diversification through time is natural selection. Moreover, natural selection is the mechanism responsible for adaptation, i.e., the functional match between organismal characteristics and the environments in which the relevant organisms live.

The first major improvement on the original Darwinism, which came to be known as neo-Darwinism (and which to this day even practitioners of the field confuse with the later Modern Synthesis!) came at the hands of Wallace himself, together with developmental biologist August Weismann. You see, the problem is that Darwin didn’t have a mechanism of heredity handy (despite the fact that, unbeknownst to him, Mendel had published his work on pea plants in 1866, while Darwin was alive and well). So Darwin flirted with a bit of Lamarckism (inheritance of acquired characteristics), and even proposed his own half baked theory of blended inheritance. Wallace and Weismann sought to get rid of the Lamarckian stigma once and for all, which they accomplished via Weismann’s famous doctrine of the separation between somatic (i.e., non reproductive) and germ (i.e., reproductive) cell lines: even if the environment influences the makeup of somatic cells, these have no way to pass that information down to new generations, so Lamarckism is ruled out. (In reality things are much more complex, for instance because plants and a number of other organisms do not obey the Weismannian doctrine.)

We then come to the Modern Synthesis (MS), the next improvement over the original version of evolutionary theory. The MS is actually divided into two major phases, one roughly extending from 1918 to the early 1930s, the other taking place from the late ‘30s through the early ‘50s.

To simplify quite a bit, by the turn of the 20th century the neo-Darwinian theory was in trouble, so much so that historians of science refer to that period as “Darwin’s eclipse” [9]. The problem — ironically — was partly created by the rediscovery of Mendel’s work, which initially was interpreted not as the much sought after theory of heredity necessary to complement Darwin’s insights, but rather as a threat to the edifice of evolutionary theory. That’s because Darwin had insisted that evolutionary change is always gradual (despite warnings to the contrary by his friend and champion, Thomas H. Huxley), while “Mendelism” seemed to show that the genetic material is inherited as a number of discrete units (the genes, whose chemical basis was, of course, still unknown). Moreover, the early geneticists had begun working on mutations, especially in the fruit fly, which seemed to bring more trouble for Darwin, since all known mutations appeared to produce radical changes in the phenotype (the appearance or behavior of organisms), again contradicting the idea of gradualism. The combination of Mendelism and mutationism, together with the resistance to Darwinian ideas by paleontologists (who saw long term trends in the fossil record, which were thought to be independent of the vagaries of environmental change), produced the widespread feeling that scientists were on the verge of dealing a death blow to neo-Darwinism.

A small group of brilliant mathematical biologists came to the rescue, chiefly Ronald Fisher, followed by J.B.S. Haldane and Sewall Wright. Fisher was almost single-handedly responsible for the reconciliation (i.e., the “synthesis”) between Mendelism, Mutationism and (neo)Darwinism: he showed how, assuming (as it turned out to be the case) that phenotypic characteristics are influenced by a relatively large number of genes, the statistical effects of those genes (and their interactions with the environment) creates precisely the sort of continuous distribution of characteristics that Darwin thought would allow natural selection to work. Indeed, Fisher formalized the Darwinian insight in mathematical form, arriving at what still today is a cardinal idea in population genetics, his Fundamental Theorem of Natural Selection [10].

The second, and equally crucial, phase of the MS was brought about by a more diverse group of biologists, most prominent among whom were Theodosius Dobzhansky, Julian Huxley, Ernst Mayr, George G. Simpson, and G. Leydard Stebbins. Indeed, it was Huxley (grandson of Thomas Henry) who coined the term “Modern Synthesis.”

What did the MS-phase 2 consist of? Of the application of the new principles of statistical genetics, cast in a neo-Darwinian fashion, to population genetics (Dobzhansky), natural history (Mayr), paleontology (Simpson), and botany (Stebbins). It was a synthesis in the sense (different from MS-1) that it broadened the scope of what could by then fairly be called the Darwin-Fisher theory of evolution to a good number of (but, crucially, not all!) other domains in biology.

The Modern Synthesis is, by and large, what is taught today in undergraduate and graduate textbooks, it represents the Standard Model of the biological sciences. But, just as the Standard Model in physics is known to be incomplete and there has been (pace Sean’s joke) quite a bit of controversy among physicists about how and when it is going to be replaced, so to has the Modern Synthesis been under increasingly severe stress, dating back from the 1960s and ‘70s, but much more intensely so in the ‘90s to the present.

Whence the stress, despite assurances by the “no” side that “all is well”? Here is a quick run down of the major points:

• Developmental biology was famously left out of the MS, and needed to be brought in. Systematic attempts at doing so have resulted in the development of an entirely new field of research, colloquially known as “evo-devo” [11], which has been developing its own agenda and principles.
• Ecology was also only marginal to the MS, and some recently developed ecological principles, such as niche construction theory, need to find an organic place in our way of thinking about evolution [12].
• The possibility that selection acts at multiple levels, rather than just on organisms (Darwin) or genes (modern population genetics) has been raised several times. After a couple of false starts under the label of “group selection,” there is now a well developed multi-level theory of selection and its action [13].
• Eldredge and Gould’s idea of punctuated equilibria [14], which maintains that some lineages evolve (geologically) very quickly and then remain unchanged through long periods of stasis.
• Evolutionary genomics has yielded not only terabytes of new data on the genetic makeup of biological species, but new insights into the evolution of regulatory vs structural (“house keeping”) genes, and has especially highlighted the necessity of thinking in terms of gene networks and their interactions with the environment, rather than single genes with the environment treated as background information [15].
• Much research has been devoted to a widespread phenomenon known as phenotypic plasticity, which allows us to model the interaction between genomes and environments in novel ways. Plasticity had been discovered in the early part of the 20th century, but the field has come into its own only in the last couple of decades [16]. A number of authors, chiefly Mary Jane West-Eberhard [17], have argued that plasticity represents a novel type of evolutionary mechanism, much under appreciated until recently.
• A trio of interrelated new concepts has been proposed, and has begun to be investigated empirically, to further expand the known set of evolutionary mechanisms: evolvability, robustness, and modularity [18].
• There has been increasing evidence that there exist a panoply of epigenetic (i.e., non-genetic) inheritance systems that are responsive to environmental stresses (though definitely not in a Lamarckian fashion!), that interact with the known genetic inheritance system, and that may play a role at the least in short-term evolutionary responses [19].
• A degree of biological complexity can be obtained independently of natural selection. This has been known since D’Arcy Thompson’s classic study on “growth and form” [20], but has been elaborated theoretically and investigated empirically under the name of “facilitated variation” [21]. This is related to, but further builds on, Gould’s old idea [21] that so-called developmental constraints can actually play a positive role in evolutionary change.
• There is increasing evidence — if you ask paleontologists — that macro-evolutionary phenomena (i.e., changes above the species level) are partially causally decoupled from micro-evolutionary ones (i.e., within species) [23]. This has nothing whatsoever to do with the specious arguments proposed by creationists, and everything to do with species selection and group-level properties.

I may be missing something, but you get the idea. Now, you could say, as the “no” camp maintains, that all of the above is just cherries on the cake of the Modern Synthesis. I, and a number of others, beg to differ. The above represents a huge set of empirical discoveries and theoretical advances that go well beyond, and are certainly not implied by (and yet do not contradict) the Modern Synthesis. This is stuff that needs to be further explored, better articulated, and explicitly integrated into the general framework of evolutionary theory — work, I might add, that has been well under way for years.

The eminently sensible idea behind a push for the recognition of an Extended Synthesis in evolutionary biology, then, is that the above constitutes at the very least the same amount of conceptual novelty in the biological sciences that was represented by the universally acknowledged break between neo-Darwinism and the Modern Synthesis, and certainly much more than the one separating the original Darwinism from the Wallace-Weismann version of the theory.

In the end, of course, it doesn’t matter what we call it. Phenotypic plasticity, evolvability, epigenetics, niche construction, facilitated variation and all the rest are here to stay. But, we do usually label different versions of scientific theories with different names, and for good reasons. They mark significant advances in our understanding of the world, and of course recognize the work that went into making those advances, as well as the people who did that work. There certainly is no need for antagonism, on either side of the divide, we can and should all work together to further biological research. But it is hard to see what could possibly justify — given all of the above and much, much more — this recalcitrance to recognize that biology is entering a new phase of its history. It’s a very exciting phase, and one that will, thankfully, soon be in the hands of todays’ graduate students and young researchers.

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Massimo Pigliucci is a biologist and philosopher at the City University of New York. His main interests are in the philosophy of science and pseudoscience. He is the editor-in-chief of Scientia Salon, and his latest book (co-edited with Maarten Boudry) is Philosophy of Pseudoscience: Reconsidering the Demarcation Problem (Chicago Press).

[1] Does evolutionary theory need a rethink?, Nature, 8 October 2014.

[2] An Extended Synthesis for Evolutionary Biology, by M. Pigliucci, Annals of the New York Academy of Science 1168:218-228 (2009). / The extended (evolutionary) synthesis debate: where science meets philosophy, by M. Pigliucci and L. Finkelman, BioScience (2014).

[3] Evolution – the Extended Synthesis, by M. Pigliucci and G.B. Müller, eds. (2010), MIT Press.

[4] The Evolution of Evolution: Gradualism, or Punctuated Equilibrium?, by S. Carroll, Preposterous Universe, 10 October 2014.

[5] Biological theory: Postmodern evolution?, by John Whitfield, Nature, 3 October 2008.

[6] A more in depth treatment of the history of evolutionary theory from a philosophical perspective can be found in: Biology’s last paradigm shift. The transition from natural theology to Darwinism, by M. Pigliucci, Paradigmi 2012 (3):45-58 (2012).

[7] It actually began much earlier: for a fascinating discussion of pre-Darwinian concepts of evolution, and how the whole field was actually considered pseudoscientific (!), see Michael Ruse’s “From pseudoscience to popular science, from popular science to professional science,” in Philosophy of Pseudoscience: Reconsidering the Demarcation Problem, by M. Pigliucci and M. Boudry, eds. (2013), Chicago Press.

[8] The 1858 Darwin-Wallace paper.

[9] The Eclipse of Darwinism: Anti-Darwinian Evolution Theories in the Decades around 1900, by P.J. Bowler (1992), Johns Hopkins University Press.

[10] Fisher’s fundamental theorem of natural selection, Wiki entry.

[11] Evo-devo, by the Understanding Evolution team.

[12] Niche construction, an overview.

[13] Evolution and the Levels of Selection, by S. Okasha (2009), Oxford University Press.

[14] Punctuated equilibrium, Wiki entry.

[15] Here is an example of what evolutionary genomics labs do.

[16] Rather immodestly, I can say that I wrote the book on phenotypic plasticity a few years ago: Phenotypic Plasticity: Beyond Nature and Nurture, by M. Pigliucci (2001), Johns Hopkins University Press.

[17] Developmental Plasticity and Evolution, by M.J. West-Eberhard (2003), Oxford University Press.

[18] Is evolvability evolvable?, by M. Pigliucci, Nature Reviews Genetics 9:75-82 (2008). / Robustness and Evolvability in Living Systems, by A. Wagner (2007), Princeton University Press.

[19] What Role Does Heritable Epigenetic Variation Play in Phenotypic Evolution?, by C. Richards, O. Bossdorf, and M. Pigliucci, BioScience 60 (3):232-237 (2010). / Transgenerational epigenetics, Wiki entry.

[20] On Growth and Form, by D.W. Thompson (1945), Cambridge University Press.

[21] The theory of facilitated variation, by J. Gerhart and M. Kirschner, Proceedings of the National Academy of Sciences, 104:8582-8589 (2007).

[22] Ontogeny and Phylogeny, by S.J. Gould (1985), Belknap Press.

[23] See, for instance: Mass extinctions and macroevolution, by D. Jablonski, Paleobiology 3:192-210 (2005).