Reactionary fringe meets mutation-biased adaptation. 5.2. The Modern Synthesis of 1959

This is the eighth in a series of guest posts by Arlin Stoltzfus on the role of mutation as a dispositional factor in evolution.

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Reactionary fringe meets mutation-biased adaptation. 5.2. The Modern Synthesis of 1959
by Arlin Stoltfus
As we learned in What makes it new?, the newness of the effect of biases in the introduction process results from a classical assumption that evolution can be understood as a process of shifting the frequencies of existing alleles. How did this position emerge? Was it a technical, mathematical issue?

The revolt of the clay

Reactionary fringe meets mutation-biased adaptation
Introduction
1. The empirical case
2. Some objections addressed
3. The causes and consequences of biases in the introduction process
4. What makes this new?
5. Beyond the "Synthesis" debate
    -Thinking about theories
    -Modern Synthesis of 1959
    -How history is distorted
    -Taking neo-Darwinism
      seriously
    -Synthesis apologetics
6. What "limits" adaptation?
7. Going forwardThe crucial issue, following Ch. 4 of Provine's (1971) seminal The Origins of Theoretical Population Genetics, was not a matter of mathematics at all, but whether selection is the kind of creative governing force required in a neo-Darwinian view.

Early in the 20th century, Johannsen experimentally refuted Darwin's non-Mendelian theory of evolution via environmental fluctuations and blending inheritance (see Roll-Hansen 1989; Gayon, 1998). Bateson and the early geneticists called for a new understanding of evolution based on genetics (see Stoltzfus and Cable, 2014). They refashioned the concept of selection as a sieve, or as a force that shifts the frequencies of true-breeding types, as in the allelic selection model of 1915, which Provine (1971) calls "the perfect complement to Morgan's theory of evolution by single gene replacement" (p. 141).

In a world of discrete genetics, they argued, selection is not creative.  Instead, "mutation proposes, selection disposes," referring to the popular aphorism "Man proposes, God disposes," which has versions in English, French and German, and traces back 600 years to Thomas à  Kempis's Latin aphorism using proponit (proposes) and disponit (manages). That is, the mutationist aphorism puts selection in the role of God, with the connotations of Edwin Landseer's 1864 painting "Man proposes, God disposes" (above), a dire reflection on the thwarted ambitions of Franklin's lost expedition.

The arguments of the geneticists brought the status of neo-Darwinism to its lowest point. Poulton (1908) describes this era as the "revolt of the clay against the power of the potter," referring to the biblical admonition against challenging one's creator:

"What sorrow awaits those who argue with their Creator. Does a clay pot argue with its maker? Does the clay dispute with the one who shapes it, saying, 'Stop, you're doing it wrong!' Does the pot exclaim, 'How clumsy can you be?'" (Isaiah 45:9, New Living translation)

The restoration of neo-Darwinism

In Provine's (1971) narrative, the neo-Darwinian revival, restoring selection as the potter and variation as the clay, is sparked by Castle's famous selection experiments. Beginning with mottled black-and-white rats, Castle and his coworkers selected lines that were nearly all white, and nearly all black: "wholly new grades," according to Castle. The scale of the experiment was only 20 generations, too short for new mutations to play an important role. Instead, color changed incrementally as new, more extreme genetic combinations of alleles at many loci came together by recombination and were selected.

As Provine concludes, "Castle had been able to produce new types by selection," without mutation, providing an experimental basis to rebut the mutationists and argue for selection as the creative force in evolution.

A general theory was constructed from this paradigm of selection, recombination, and shifting gene frequencies, representing a formally complete Mendelian justification for neo-Darwinism. By the time of the 1959 Darwin centennial, this theory was invoked by Mayr, Simpson, Dobzhansky, Huxley, Stebbins and others (Stoltzfus, 2017). Viewed from the outside, in terms of visible features, evolution is a smooth shift in phenotypes driven by selection (figure, below). At the genetic level (center), frequencies of small-effect alleles at many loci (A1 vs. A2, B1 vs. B2, etc) are shifting simultaneously from the previous optimum to a new optimum. All of evolution follows from shifting gene frequencies. 

In mathematical models based on this theory, the population moves in the topological interior of an allele-frequency space (right), without an introduction process.

Of course, every allele had to arise by mutation at some time in the past, but the theory holds that the dynamics of this process are not consequential, because selection does not wait for new mutations, but leverages variation available in an abundant gene pool.

Thus, the theory deliberately excludes the mutationist view that the course of evolution depends importantly on the timing and character of individual events of mutation. Mutations play no direct role, but simply replenish the gene pool, as Stebbins (1959) explains:

" ... mutation neither directs evolution, as the early mutationists believed, nor even serves as the immediate source of variability on which selection may act.  It is, rather, a reserve or potential source of variability which serves to replenish the gene pool as it becomes depleted through the action of selection" (p. 305) 

Likewise, Mayr (1960) says

"The real function of mutation is to replenish the gene pool and to provide material for recombination as a source of individual variability in populations."  (p. 355 of Mayr E. 1960. The Emergence of Evolutionary Novelties. In: Tax S, Callender C, editors. Evolution After Darwin: The University of Chicago Centennial. Chicago: University of Chicago Press).

or

"Evolution is not primarily a genetic event. Mutation merely supplies the gene pool with genetic variation; it is selection that induces evolutionary change." (p. 613 of Animal Species and Evolution, 1963).

Mayr did not study these population processes himself, but is merely drawing on a way of thinking learned from others. This is how we know that a theory exists: it causes different people to carry out similar forms of reasoning. For additional statements of this theory, contrasted with contemporary thinking, see Stoltzfus (2017) or The shift to mutationism is documented in our language.

And its demise

In passing, please note—for purposes of the subsequent post—that the quotations above are examples of good historical evidence.  They show the operation of a theory at work, revealing how scientists invoke the logic of a theory to reach high-level conclusions.  Above, Mayr and Stebbins invoke the gene-pool logic of the Modern Synthesis of 1959.  Previously (part 4), we saw that Huxley, Gould, Maynard Smith, et al. and Reeve and Sherman invoke the opposing-pressures argument. In the case of Huxley, Gould, Mayr and Stebbins, the conclusions  are offered as powerful truths, without qualification, i.e., they exemplify the relationship we defined previously [part 5.1] as "love" or "commitment."

That is, although the Modern Synthesis of 1959 was a speculative theory, proponents believed that it was well supported, e.g., Stebbins (1959) follows his description of principles (cited above) by declaring that:

"The factual evidence in support of these postulates, drawn from a wide variety of animals and plants, is now so extensive and firmly based upon observation and experiment that we who are familiar with it cannot imagine the appearance of new facts which will either overthrow any of them or seriously limit their validity."

Stebbins's confidence was misplaced: the theory was promptly contradicted in the 1960s by molecular sequence comparisons suggesting evolution as a Markov chain of mutation-fixation events. At the time, this contradiction was resolved superficially by arguing that the Modern Synthesis correctly depicts evolution for the kinds of visible features discussed by all previous generations of evolutionists, regardless of anything discovered at a previously invisible "molecular" level isolated from phenotypes and selection (this is my view; see also Dietrich, 1998).

And so, "molecular" evolution was left to "molecular" evolutionists, who held that "we need new rules in order to understand the pattern and dynamics of molecular evolution" (King and Jukes, 1969).

Among the new rules was a direct link between the rate of evolution and the rate of mutation that (as we have discussed) classical theory did not supply.  Yet, mutationist models remained in the domain of molecular evolution, being used mainly by neutralists (McCandlish and Stoltzfus, 2014). The introduction process was not the focus of contending theories, which addressed other issues (see Crow, 2008).  The dominant conflict was neutralism vs. selectionism, not neo-Darwinism vs. mutationism (but see King, 1971 for an incisive minority view).

Today, the role of the introduction process in evolution is due for re-examination, based on the evidence that the course of adaptation reflects biases in the introduction of variation.

The theory behind the Synthesis story

In the Synthesis story, a new and powerful understanding of evolution emerges in the mid-20^th century, (1) combining genetics with neo-Darwinism, (2) sweeping away all rivals, and (3) providing a unified basis for biologists to apply evolutionary principles to their work.

What theory satisfies this description? What theory plays the starring role in the Synthesis story?

The Modern Synthesis of 1959 described above (see also Stoltzfus, 2017) (1) offers a Mendelian justification for neo-Darwinism, (2) excludes mutationism (via the gene-pool theory) and internally biased evolution (via the opposing-pressures argument), and (3) supports high-level principles that can be applied across disciplines, e.g., they can be applied to interpreting the fossil record without knowing details of genetics and development, because the theory says that these details are not determinative.

By contrast, the lists of diluted, sterilized "Synthesis" principles from apologists for orthodoxy (e.g., Futuyma, 2017) fail to justify neo-Darwinism, fail to exclude mutationism, and fail to support the high-level principles that (for instance) allowed Simpson to infer that trends in the fossil record must be due to selection because there is no alternative. Such lists of principles are not theories designed to take bold risks or to inspire the imagination, but are merely the output of an algorithm: describe evolutionary thinking so as to maximize the apparent similarity with mainstream views of 1959.

As mainstream thinking has diverged from 1959, the output of this algorithm has dwindled. Today it says merely that evolution is a process that takes place in populations through the action of mutation, selection, drift and recombination, with selection playing a very important role. Relative to the Modern Synthesis of 1959, this "theory" is weak, but in Synthesis apologetics, it is claimed to be powerful on the grounds of lasting 60 years.  This is a truism, of course: the description generated by running the Futuyma algorithm after X years always has the property that it has lasted X years. This algorithm is not informative about the theories that shaped evolutionary discourse, because it leaves out discarded ideas such as the creativity of selection and the role of recombination in the gene pool.

To the extent that science proceeds in Popperian fashion, by rejection, these discarded ideas serve as the mile-posts of progress. For instance, when Provine reflected back on the Modern Synthesis in the 2001 re-issue of his 1971 classic, he said that it "came unraveled for me during the period since 1980."  He rejects the notion that macroevolution is a simple extension of microevolution, rejects the idea that evolution depends on recombination rather than mutation as the proximate source of variation, and refers to the gene pool as "one of the most artificial concepts of population genetics."

Nevertheless, the Modern Synthesis of 1959 remains valuable, as does neo-Darwinism, when we apply them as models-- as conceptual tools with specific functions, in the manner that neutral models are applied by contemporary scientists. Such theories provide ongoing guides to thought and to hypothesis-generation. Their successes and failures may be used to demarcate our substantive knowledge of how evolution actually occurs.

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