Randomness in Evolution (Bonner)

John Tyler Bonner’s Randomness in Evolution (2013; Princeton University Press) is a small and lightweight book— 123 pages, plus a bibliography with a mere 43 references.  So, I won’t feel too bad for giving it a rather small and lightweight review, based on a superficial reading.   Last year, I was tasked with reviewing Nei’s book and I went way overboard reading and re-reading it, trying to decipher the missing theory that Nei claims to be proving.  I even wrote to Nei with questions.  He literally instructed me to read the book without pre-conceptions.  (Pro tip: when a reader asks you to explain your work, do it— don’t pass the buck).

Bonner’s book is somewhat similar to Nei’s in that it is full of broad generalizations and narrow examples, without enough of the conceptual infrastructure in between; both books offer provocative ideas that are something less than a new theory.  The difference is that Bonner is aware of this.  His modest claim is simply that certain forms of randomness (which he describes) play an under-appreciated role in evolution.j9958

My first reaction, skimming parts of the book, was annoyance with Bonner’s repeated claims that randomness is essential to Darwin’s theory.  This is not correct historically or logically.  Darwin’s theory does not depend on variation having any of the various meanings that we normally assign to the term “random” in other contexts (uniformity, independence, spontaneity, indeterminacy, unpredictability), only on it being small and multifarious.  Imagine a deterministic mechanism of variation that creates a quasi-continuous range of trait values above and below the initial values, and you can get evolution exactly as Darwin conceived it.  Darwin believed that the variation used in evolution was stimulated by exposure to “altered conditions of life”.  In this theory of variation-on-demand, adaptation happened automatically.  The “random mutation” doctrine came along later, and it meant something (rejection of Lamarckian variation) that Darwin himself clearly rejected.

As I read more of the book, I realized that Bonner’s “randomness” covers several different ideas, one of which arguably justifies his references to Darwin.

In some cases, Bonner’s “randomness” means that different instances of a dynamic system inevitably disperse over a non-zero area of state-space, due to heterogeneity in factors we don’t care about (the technical language is mine: Bonner doesn’t describe it this way).  Imagine a local population of genetically identical slime mold cells: expose them to microheterogeneity in the availability of bacterial food sources, and you’ll get heterogeneity in the sizes of cells.  Even if you give those cells identical food, after some period of time they will be out of synchrony, and we’ll get a distribution that goes from skinny cells that just divided to fat ones that are about to divide.

I’ll call this flavor of randomness “predictable dispersion” or “reliable dispersion”, noting the relationship to arguments of McShea and Brandon.  Bonner argues that reliable stochastic dispersion in morphology and other gross features plays an important role in life cycles, e.g., when certain slime molds form a fruiting body, the skinny cells go on to become stalk cells, and the fat ones become spore cells.   This is an interesting argument, but is not developed in full detail.  This particular kind of “randomness” is suggestive of Darwin’s theory, though it isn’t what Darwin meant by “chance”.

Elsewhere, Bonner is simply invoking neutral evolution, e.g., neutral evolution of morphology.  In considering a group of marine planktonic organisms such as the foraminifera or radiolaria or diatoms, with literally thousands of morphologically distinct species (note the radiolarians on the cover, from Haeckel’s drawings), he finds it unfathomable that all of this morphological diversity is adaptive.  He argues quite reasonably that there is much more habitat heterogeneity in terrestrial than planktonic environments, yet these are largely planktonic marine organisms, often cosmopolitan, which argues against local niches.  This is about as far as the argument goes.

Actual diatoms arranged on a microscope slide, from the California Academy of Sciences collection

Diatoms artfully arranged on a microscope slide (scale bar, 100 microns; Cal Acad Sci collection,  https://www.flickr.com/photos/casgeology/sets/72157633997313366)

It seems to me that a cosmopolitan distribution argues against this thesis.  If these organisms are not segregating a niche, competitive exclusion would come into play and reduce diversity. At the risk of sounding like an adaptationist Pollyanna, I would wager that there is a constant differential sorting of planktonic organisms (due to subtle differences in temperature, current, viscosity)  in such a way as to preserve a diversity of morphologies, even when the system seems well-mixed on a larger scale.  Every time a squid swims by, I reckon, the patterns of turbulence sort planktonic critters in reliable ways that bring different resources to differently shaped species.  Even if such an adaptive hypothesis is true, Bonner’s argument remains relevant in the sense that (in my scenario) selection is blind to every aspect of morphology that looks interesting to us visually (and only cares about the effect on mechanical sorting).

Tip vortex of a small aircraft (wikipedia: turbulence)

Tip vortex of a small aircraft (wikipedia: turbulence)

Bonner also makes an argument about size and randomness that was not very convincing.  However, he makes it clear that he is not expecting us to be convinced by such arguments.  He wants only to inspire further thought.  I suppose he has succeeded, in my case, but I wish he had gone further to propose more specific hypotheses, and to outline a research program.

What thoughts has Randomness in Evolution inspired?  My main thought is that we need to stop using “chance” and “randomness” so casually, and start making meaningful distinctions.  Like Bonner— who frequently juxtaposes different ideas under the theme of “randomness”, and jumps jarringly from Darwin to Wright to Kimura to Lynch— we often use these terms to cover a wide array of concepts, and it isn’t helpful.

And please do not refer to drift as “Wright’s idea”.   The idea of neutral changes is generic and had been kicking around much earlier.  Early geneticists such as Morgan proposed the more specific idea of random changes in gene frequencies, and also the (slightly different) idea of random fixation of neutral mutations.   If we are looking for early advocates of the importance of drift, then according to what I’ve read (e.g., Dobzhansky’s account), we should honor a couple of Dutch geneticists, Arendt and Anna Hagedoorn, based on their 1921 book. Wright merely introduced the distinction “steady drift” = selection and “random drift” = drift, which degraded into simply “drift” to mean random drift.

The role that drift plays in Wright’s signature “shifting balance” theory, which came along later, is distinctive.  Wright did not introduce “randomness” in order to explain dispersion or unpredictability in the outcome of evolution.   To the contrary, his idea was to leverage drift in a scheme for improving search efficiency.  The role of drift in Wright’s theory is analogous to the role of heat in simulated annealing.  This and similar meta-heuristics used in optimization methods allow the system to explore solutions worse than the current solution, a property that reduces the chance of getting stuck at a local optimum, and (when properly tuned) ultimately increases optimization.  Wright assumed that evolution was a very good problem-solving engine, and that it must have some special features that prevent it from getting stuck at local optima.  He proposed that the special optimization power of evolution comes from dividing a large population into partially isolated demes, each subject to stochastic changes in allele frequencies.  The intention of this scheme was to make evolution more predictable, more adaptive and more reproducible.

Kimura was doing something entirely different, trying to solve a technical problem in the application of population genetics theory, which is that the rate of molecular evolution is high and constant, and seems incompatible with the projected population-genetic cost of selective allele replacements.  The solution was to propose that most changes take place at low cost because they are due to the random fixation of neutral alleles.  Kimura was deeply committed to his theory and defended it to his death, but I don’t think the random character of fixation by drift had any particular importance for him.

These ideas are different, again, from Lynch’s thesis.  The explanatory target of Lynch’s thesis is not the unpredictability of evolution, or an excess of unpatterned diversity.  Instead, Lynch purports to have discovered a pattern, and a drift-based explanation for that pattern, that takes much of the mystery out of genome size evolution.   Where previously we saw anomalous differences in genome size, we now (according to Lynch) see a widespread inverse correlation between genome size and population size, and we have a hypothesis to explain that correlation based on drift (in combination with a tendency to gain mobile elements).   In context, drift is responsible for a directional or asymmetric effect, because it is stronger in smaller populations.

My last comment, not stimulated by Bonner’s book, is that we really should reconsider what we mean by “randomness”, which I think is dispensable.  I do not say this because I have a secret belief that everything happens for a reason.  The problem with randomness is that everyone invokes it as if, by calling a process “random”, we are diagnosing some observable property of that process.

I think it is hardly ever the case that “randomness” properly belongs to the thing alleged to be random.  Where “randomness” connotes chance or independence, it is always a matter of one thing relative to another.  Calling something random is like calling something “independent”— it immediately prompts the question “independent of what?”.

In other cases, I think “random” is used as a heuristic, a kind of epistemological (methodological) perspective on factors.  A random process or factor is one that we do not care about— something we have placed in the category “unimportant”.  The process may rely on causes that are perfectly deterministic, and its behavior may be predictable and highly non-uniform, but if we don’t care about it, we assign it a stochastic variable and call it “random.”   Is movement random?  That depends.  If we are tracking wolves with radio collars, we care about the day-to-day movements of individual organisms.  The movements aren’t “random”.  If we are modeling the formation of a slime-mold fruiting body, we no longer care about the day-to-day movements of individual organisms.  They are random.  In reality, they are no less deterministic or predictable than the movements of wolves, but we don’t care about them.

Once you start caring about a factor, it is no longer random.  Once a factor is in the “important to me” category, we see that there are source laws that determine its behavior, and consequence laws that determine the effects of this behavior. Once I got interested in the role of mutation in evolution, I wanted to understand the cause of biases in mutation, and the consequences of these biases on the course of evolution and the doctrine that “mutation is random” meant only that some people still put mutation in the “unimportant to me” category, and these people typically are confused about the source laws and consequence laws of mutation.

Mendelian-Mutationism: the Forgotten Evolutionary Synthesis

What is Mendelian-mutationism?  And why do we argue in a recent paper in that it represents a forgotten evolutionary synthesis (Stoltzfus and Cable, 2014, Mendelian-Mutationism: The Forgotten Evolutionary Synthesis. J Hist Biol. doi:10.1007/s10739-014-9383-2)?


Effect of mutation bias in the 1-step adaptation model of Yampolsky & Stoltzfus, 2001. The greater the bias in mutation, the greater the tendency to evolve in the mutationally favored direction.

For me, the story started a long time ago with our theoretical demonstration (graph at right) that bias in the introduction of variation (by mutation-and-altered-development) is a fundamental cause of non-randomness in evolution (Yampolsky & Stoltzfus, 2001).

The novelty of this claim bothered me deeply.  Why?  Here was a basic principle— a causal link between non-randomness in biological inputs (mutational and developmental biases) and non-randomness in evolutionary outputs— as fundamental as the concept of selection or drift.  Yet, this principle was not mentioned in any textbook of evolution or population genetics (indeed, there is even a classical population-genetic argument against a determinative role for mutational biases).  I could not even find this principle in the research literature!  When it comes to contemplating the impact of biases in variation, evolutionary biologists habitually assume that such an impact is impossible, except in the special case of (1) rigid constraints (i.e., the impossibility of generating form B means we’ll get A or C instead), or (2) neutral evolution.   We knew that all of this was incorrect.

This prompted 2 questions.  Why wasn’t a general connection between biases in variation and biases in evolution recognized long ago, e.g., by Wright, Haldane or Fisher?   And, why— after it was discovered and published in 2001— didn’t this inspire a revolution?


The top of my evolution bookshelf, with historic works in roughly chronological order: from Darwin and Mivart to the Mendelians (top shelf), then the core of the Modern Synthesis, up to the early molecular era (next shelf) [1]

I’m still puzzling over the second, admittedly naive, question.  To address the first question, I’ve spent an inordinate amount of time studying the development of evolutionary thought (bookshelf at right).

The short answer is this: the notion that mutation has a dispositional role in evolution, influencing its rate and direction, represents a kind of “internal” causation, an internal source of direction in evolution, that Darwin’s followers rejected as illegitimate.  Ever since, it has been a blind spot in evolutionary thinking.

The nature of this rejection is hard to comprehend today, due to a process of amnesia and theory-drift.  Nearly all evolutionary biologists today believe that evolutionary biology has a prevailing theory, and that this theory— called the Modern Synthesis or modern neo-Darwinism— came together in the mid-20th century.   What few realize is how far the common conception of this theory has drifted from its original intentions.  The original Modern Synthesis was held together with Darwinian doctrines that most scientists today do not accept, such as the doctrine of gradualism, the idea that selection is creative, or the rejection of any internal causes of direction.  We can think of these as the “soft parts” of the Modern Synthesis, the muscles and connective tissue that gave it shape and motion.


The soft bits of this whale carcass rotted away, leaving only the bones.

Over time, the Darwinian character of the Modern Synthesis has rotted away, leaving only the more resilient parts.  This is why scientists today think of the Modern Synthesis as a kind of open-ended framework for understanding evolution. They are looking at an open-ended skeleton.

Our study of early geneticists revealed that this skeleton predates the Modern Synthesis.  There was an earlier Mendelian-Mutationist Synthesis that combined mutation, heredity and selection, without Darwinian doctrinal commitments to gradualism, the creativity of selection, and the “randomness” (non-importance) of mutation.  What most scientists today think of as the Modern Synthesis is actually the forgotten Mendelian-Mutationist synthesis. Like scientists today, the early geneticists or “mutationists” welcomed both selection and neutrality, allowed both gradual change and saltations, and welcomed the idea that biases in mutation could be the cause of parallelisms or trends.

The new paper by Stoltzfus and Cable describes what the early geneticists believed about how evolution works, and what they contributed to the foundations of evolutionary thought.  It also explains why they rejected Darwin’s theory (another case in which the popular conception of a theory today does not match what its historical meaning).

But that’s only half of the story.  The other big theme is historiography, the telling of history.  The disconnect between what actually happened and what scientists believe is not just a matter of theory-drift.

“History is written by the victors,” Churchill said.  In this case, the victorious architects of the Modern Synthesis promulgated a view of early geneticists as bumbling fools who saw mutation and selection as opposing principles, and who couldn’t think synthetically.  The period of 1900 to 1920, actually a rich period in which early geneticists laid the foundations of modern evolutionary thought, is described perversely as part of an “eclipse of Darwinism”— a period of darkness when the world was deprived of His light— lasting until Darwinism is re-born in the Modern Synthesis.  This story-telling has been so influential that, when contemporary scientists list historically important figures, all key figures of the Mendelian-Mutationist synthesis are removed, Soviet-style (see figure below).[2]


On this timeline of “notable people who have contributed to evolutionary thought” (source), I have super-imposed a salmon-colored box. This box includes the birth year of anyone 25 to 60 years old— the prime of a scientist’s life—  when genetics was discovered in 1900.  No timelines begin in the box. That is, the figure tells us there were no notable contributions by scientists born in this period, which includes the birth of de Vries (1848-1935), Johannsen (1857-1927), Bateson (1861-1926), Cuénot (1866-1951), Davenport (1866-1944), Morgan (1866-1945), and Punnett (1875-1967). Richard Goldschmidt (1878-1958), born just a few years later and listed as a non-Darwinian (top), was a second-generation mutationist whose 1940 book introduced “hopeful monsters” and provoked Ernst Mayr into writing a book of his own.

That is, the distorted view of history that evolutionary biologists hold today is not just a matter of passive amnesia, but of a highly successful public relations campaign, what evo-devoist Stuart Newman recently called “an unremitting 90-year campaign to identify ‘evolutionary theory’ with ‘Darwinism'”.

The recent paper on Mendelian-Mutationism is actually an off-shoot of a series of “Mutationism myth” blogs written for SandWalk in 2010.  To turn the blogs into a scholarly work worthy of publication in a peer-reviewed historical journal was a major project accomplished over the course of 2 years, by teaming up with a history-of-science graduate student named Kele Cable. Kele recently blogged about our paper on his web site.


[1] Some of my favorites: Haldane, 1932 (the tattered volume, top, second from right); the 1911 (3rd) edition of Punnett’s Mendelism, the first textbook of genetics (the slimmer of two burgundy volumes, top center); George Williams (1966) Adaptation and Natural Selection (row 2, 9th from right, with the shiny jacket cover); Lewontin, 1974 (row 2, right end, red with gold lettering next to Crow & Kimura 1970).

[2] Other examples could be given.  The Oxford Encyclopedia of Evolution (click for searchable online index) has an entry for Mendel, who made no direct contributions to evolutionary thinking, but lacks an entry for all of the mutationists except for Morgan.  Importantly, the entry for Morgan says nothing of his evolutionary views, only of his contributions to genetics.  Textbooks (e.g., Ridley, 1993, or Freeman & Herron, 1998) and online teaching materials (try a web search on “development” or “history”  of evolutionary thought) frequently jump from Darwin to the Modern Synthesis, with the explanation that Darwin’s theory was right but needed a mechanism, and this was supplied when the architects of the Modern Synthesis combined genetics and selection.  Early geneticists, if they are mentioned at all, are depicted only for their alleged failure to understand selection, accept small changes, or achieve synthesis.

The surprising case of origin-fixation models

In a recent QRB paper with David McCandlish, we review the form, origins, uses, and implications of models (e.g., the familiar K = 4Nus) that represent evolutionary change as a 2-step process of (1) the introduction of a new allele by mutation, followed by (2) its fixation or loss.

What could be surprising about these “origin-fixation” models, which are invoked in theoretical models of adaptation (e.g., the mutational landscape model) and in widely used methods applied to phylogenetic inference, comparative genomics, detecting selection, modeling codon usage, and so on?

Quite a lot, it turns out. (more…)

Going global with phylogeny: the tree-for-all hackathon

Earlier this year, the Open Tree of Life project made the first public release of its synthetic tree of 2.5 million species (from ~4000 source trees), and announced a web services API (Application Programming Interface) providing programmatic access to a continually updated set of resources:

  • synthetic tree covering millions of species
  • a database of thousands of source trees
  • reference taxonomy used to align names from different sources

Tree-for-All participants convene to hear a report from a hackathon team

The API release was timed to coincide with our open call for participation in a “Tree-for-all” hackathon, which took place September 15 to 19 (2014) at University of Michigan, Ann Arbor.  The hackathon— organized and funded by OT, the Arbor workflows project and NESCent’s HIP (Hackathons, Interoperability, Phylogenies) working group (Stoltzfus and Pontelli, PIs)— aimed to build capacity to leverage OT’s resources, making expert phylogenetic knowledge more accessible to scientists, educators, and the public.

To find out more about the hackathon, go to Open Tree’s blog (click on the “tree-for-all” tag), where I am guest-blogging about it.  Using web services to make phylogenetic knowledge more accessible is the theme of the Phylotastic project described by Stoltzfus, et al. 2013.

The Curious Disconnect: Introduction

This is a far-too-long introduction to a blog series that I started in 2010.  Now I’m ready to start it up again.  The themes will still be the same— but hopefully I have learned a bit about stating things more succinctly.

Striking a chord

The title of this blog — The Curious Disconnect — comes from a 2002 article by eminent evolutionary geneticist Allen Orr, who had broken new ground by developing predictive models of adaptation, and was reflecting on why such models weren’t developed long ago, referring to “a curious disconnect between the verbal theory that sits at the heart of neo-Darwinism and the mathematical content of most evolutionary genetics”.

That struck a chord with me. Since the 1990s, I had struggled with a disconnect that emerged while I was digesting a think-piece by paleontologists Elisabeth Vrba and Niles Eldredge. Among other things, Vrba & Eldredge made the startling suggestion that a key theme of “evo-devo” was that “bias in the introduction of phenotypic variation may be more important to directional phenotypic evolution than sorting by selection”. By 1999 when Constructive Neutral Evolution appeared, my thinking had shifted noticeably toward emphasizing (1) the mechanistic distinction between the process of introducing variants and the (separate, subsequent) process of reproductive sorting (selection and drift), and (2) a research program of accounting for non-randomness (in evolution) by invoking both bias in the introduction process, and bias in the sorting process.

This way of thinking suggested that mutational-developmental bias in the introduction of variation was a general cause of evolutionary bias or direction. That contradicted two things I knew about evolutionary thinking. (more…)

When “Darwinian adaptation” is neither

Getting stuff right

Early in the evolution of the Sequence Ontology, it was noted (by gadflies like myself) that SO asserts the relationship of mRNA to gene to be the “part of” relationship.  This is obviously wrong.  An RNA molecule is not part of a DNA molecule.   Saying that mRNA is part of a gene is like saying that a CD with some audio chapters from a book is part of that book.

Ontologies are supposed to support formal reasoning: errors in representation will lead inevitably to erroneous results.  For instance, if we are reasoning about the chemical composition of a cell using mRNA part_of gene as a constraint, we would conclude falsely that the mass of DNA must always be at least as much as the mass of mRNA, because the mass of a thing is always at least as great as the mass of some specified parts.


The Great Non-Debate on Evolutionary Theory (Nature, Oct 2014)

Some of you may have noticed a recent exchange in Nature on the question of whether evolutionary biology needs a re-think. The online article does not make clear the alignments of the listed authors, but those arguing in favor of a re-think are:

  • Kevin Laland, Tobias Uller, Marc Feldman, Kim Sterelny, Gerd B. Müller, Armin Moczek, Eva Jablonka, and John Odling-Smee

and those arguing against are:

  • Gregory A. Wray, Hopi E. Hoekstra, Douglas J. Futuyma, Richard E. Lenski, Trudy F. C. Mackay, Dolph Schluter and Joan E. Strassmann

I was a bit surprised that they didn’t get people who actually disagree about science, like Mike Lynch and Sean Carroll.  Instead, the debate takes place between participants who disagree on the meta-scientific question of whether the field needs a re-think.  What is each side saying?

Evolution: A View from the 21st Century (book review)

Last year I read James Shapiro’s Evolution: A View from the 21st Century (2013, FT Press) along with 2 other recent books, Nei’s Mutation-Driven Evolution and Koonin’s The Logic of Chance.  All 3 fall into the category of recent books by seasoned researchers whose primary focus is molecular, and who argue that we ought to rethink evolution based on findings of molecular biology or molecular evolution.   The 5-word summaries of these books are:

  • Engineering, not accident, provides innovation (Shapiro)
  • Mutation, not selection, drives evolution (Nei)
  • After Darwinism, things get complicated (Koonin)

In the case of Koonin, you have to read the whole book to understand what he means. If you are not familiar with the past 10 to 20 years of findings from comparative genomics, then it will be educational, and regardless of your familiarity with genomics, it will be entertaining and thought-provoking.  In the case of Nei, you can read the whole book and still not understand his thesis because he never defines terms and never actually compares mutation and selection to determine which one drives evolution (the wikipedia “mutationism” page has links to a handful of reviews of Nei’s book, including my review in Ev & Dev).

In Shapiro’s case, the book explains precisely what is meant by the idea that innovation is the result of engineering, not accident, though he leaves open the question of what are the general implications of this for evolutionary theory. (more…)

Theory vs. Theory

What does it mean to invoke “evolutionary theory”? Is “neo-Darwinism” (or “Darwinism”) a theory, a school of thought, or something else? What gives a theory structure and meaning?  Can a theory change and, if so, how much?  What is the relationship between mathematical formalisms and other statements of “theory”? Who decides how a theory is defined, or redefined (e.g., is Ohta’s “nearly neutral” theory an alternative to, or a variant of, Kimura’s Neutral Theory of Molecular Evolution)?

For various purposes, it is useful to have a framework for discussing “theory” and “theories”.  Here I begin by identifying two distinct ways that scientists use the word “theory”. 1