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Monday, July 22, 2019

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.

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
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

    -Synthesis apologetics
6. What "limits" adaptation?
7. Going forward
The 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).
"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-20th 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.


Larry Moran said...

I'm not sure if I agree with Arlin on everything so let me outline my view of the Modern Synthesis of 1959. You can see where Arlin takes me to task by reading: Arlin Stoltzfus explains evolutionary theory. That post contains links to and brief summaries of Arlin's posts on Mutationism from 2012.

Larry Moran said...

The first point I want to make concerns the minimal definition of evolution as "... a process that results in heritable changes in a population spread over many generations." [What Is Evolution]. The process focuses on changes in allele frequencies but the definition doesn't eliminate the necessity of introducing mutations into the population. Nevertheless, it's important to note that, strictly speaking, evolution can occur in the absence of mutation so the proponents of the Modern Synthesis were not wrong on that point. However, they were clearly wrong to imagine that mutation could be dismissed as just an inconsequential supplier of genetic variation over thousands of generations.

Larry Moran said...

The second point refers to the specific version of the Modern Synthesis that was promoted in 1959. That version emphasized natural selection as the only significant cause of changes in the frequencies of alleles in a population. Gould and others have pointed out that earlier versions paid lip service to genetic drift but by 1959 the Modern Synthesis had "hardened" to such an extent that drift was ignored.

Proponents of the Modern Synthesis strongly resisted Neutral Theory and Nearly-Neutral Theory because it meant that random genetic drift is an important cause of changes in allele frequencies. Even today, there are many evolutionary biologists who are uncomfortable with drift - often by relegating it to the domain of "molecular" evolution where nothing important ever happens. (See Arlin's post above.) This is the Dawkins' view of evolution that was promoted in his books on evolution.

I agree with Gould and others that the 1959 version of the Modern Synthesis is effectively dead [Is the "Modern Synthesis" effectively dead?].

Larry Moran said...

The third point concerns what has happened since the 1960s. There are many evolutionary biologists who still think that the 1959 version of the Modern Synthesis is actually the modern (2019) view of evolution. Some of them are attacking that view by promoting things like niche construction, epigenetics, plasticity, and other fuzzy concepts that aren't really an important part of general evolutionary theory. They seem to have missed the revolution that occurred in the 1960s when the Modern synthesis died.

However, there are some evolutionary biologists who are quite comfortable with drift, mutation, and molecular evolution but claim that the Modern Synthesis has evolved to incorporate these important concepts that were never a significant part of the 1959 version. Douglas Futuyma is an example. I think this is misguided but we must be careful not to lump these scientists in with those who missed the revolution. Futuyma and others like him are not reactionaries. I'm not so sure about some others like Francis Ayala and Walter Fitch [A "synthetic" view of the Modern Synthesis]

Joe Felsenstein said...

Walter Fitch is also effectively dead too. And actually.

Larry Moran said...

and Francis Ayala should be .... Francisco Ayala.

Arlin said...

Larry, I agree with you on a lot of basics, but not the big picture.

1. The EES was not set up to contrast MS1959, which has been forgotten. The EES Front is not criticizing the gene-pool theory or calling for more attention to drift and mutations. They are not emphasizing the non-MS1959 things that molecular and microbial evolutionists deal with every day-- lateral transfer, macromutations, irrational complexity, mobile elements, smart mutation, etc.

Instead, EES is set up to contrast a reductionist mainstream research program that focuses too narrowly on genetics and upward causation. People within this mainstream research program can have widely varying views, e.g., Michael Lynch and Richard Dawkins would both be targets of EES criticism. Lynch has said repeatedly that population genetics is primary and that everything comes down to population genetics. That's the kind of thing they want to change.

2. MS1959 is not dead-- it's undead. It's a zombie theory. It continues to shape evolutionary discourse, e.g., via the forces theory, even though no one defends it explicitly.

Arlin said...

A third point: the revolution, which I would like to re-articulate. Sorry that this is a bit long

Molecular and microbial evolutionists seem to look at evolution quite distinctly from most organismal biologists, more like mutationists than neo-Darwinians. It is not just about neutral evolution, but other things such as explanatory paradigms and approaches to novelty. The classic view of novelty is that new features are formed from gradual shifts, using the smallest possible changes, e.g., Jack-rabbit ears are an innovation, but the innovation can be explained by shifting the proportions of things gradually.

This way of thinking is no help at all if I'm trying to understand the origin of some interesting molecular feature, e.g., spliceosomal introns. New molecular features do not come together from gradual shifts driven by selection, one nucleotide at a time. Mitochondria did not come together gradually. Our world is discrete, and it changes in chunks that are formed by mutations. We cannot understand it any other way.

Futuyma labels things differently from Mayr, but his view is essentially the same. In his latest piece of Synthesis apologetics, his solution to Kimura's challenge of 1968 is to invoke the biblical language from Matthew 22:21-- "Render to Caesar the things that are Caesar's; and to God the things that are God's"-- except that he refers to Kimura and Darwin. For them, molecular evolution happens in a different domain and follows different rules, and this (in their interpretation) is entirely because of neutral evolution, an exception that (in their world) has no implications for the rest of evolution. That is, what you think of as a revolution is, for them, an isolated exception for neutral evolution at the molecular level.

I think we need to conceive of this revolution more broadly so that it cannot be dismissed as an issue of molecular evolution.

Neo-Darwinism is a powerful theory in the sense that it provides a way to explain any putatively adaptive feature as an end-point. The explanation is always the same: selection shaped the feature out of the raw materials of variation.

80 years ago we knew almost nothing about what is going on inside organisms, and so it was useful to have a theory that said that the internal details don't matter. MS1959 said that, to understand evolution, we just pay attention to the selective conditions relevant to the organisms in their natural habitat-- don't worry about the mutations, which are random. Just look at the outsides of organisms, and their conditions. The vast majority of biologists only knew organisms by looking at their outsides, e.g., Ernst Mayr spent his entire career looking at the outsides of birds, and studying their distribution relative to the environment. Of course he preferred a theory that says nothing matters besides what he sees right in front of his eyes. If the theory said that he needed to do genetics to understand evolution, he would have not been able to write any books.

But this powerful theory is only powerful for people who are operating in the dark about the details of biology. Today we are immersed in the internal details of organisms, their genetics, molecular biology, development, etc. We apply powerful methods to infer paths of descent. This changes everything. Neo-Darwinian can explain any feature as an endpoint, but it can't explain every historical path, because actual paths may include saltations and neutral changes.

Larry Moran said...

Arlin, I don't see why you are objecting to what I have said over the past 20 years. I agree with you that EES proponents are ignoring all the things that have made the MS1959 theory obsolete. For the most part, they are ignoring those things (drift, Neutral Theory, mobile genetic elements, lateral gene transfer, etc.) because they don't even know they exist.

Yes, it's true that their attacks focus on a gene-centric view of evolution. They claim that they want to extend that gene-centric/population genetic theory of evolution by adding a whole bunch of other things that sound more like observations about the history of life than fundamental evolutionary theory.

My main point about the big picture is that the EES crowd would have a lot more credibility if they could convince me that most of them actually understand the modern evolutionary theory that they are attacking. For example, although Richard Dawkins is a main target of their attacks, you would be hard-pressed to find any of them attacking Michael Lynch or Arlin Stoltfus because they have no idea what those scientists are saying about evolutionary theory.

John Harshman said...

It seems odd to say that Mayr, who had a big thing about co-adapted gene complexes and genetic revolutions, was interested only in outsides or in infinitesimal changes.

Arlin said...

It would help to cite some sources for this. Did Mayr invoke the genetic revolutions to explain or predict saltations?

John Harshman said...

Well, it's the theoretical basis for punk eek, which has been accused of being saltationist. Close enough?

Arlin said...

Ah, I see. You're upset that the EES Front doesn't even care about all that molecular stuff.

I agree that they don't mention this in their critique of orthodoxy, but again, this follows roughly from their platform. It isn't irrational. The EES Front has accepted the flexible Synthesis qua research program, so their position is that the Synthesis can claim anything that follows from a reductionist pop-gen approach.

Also, it may be important to consider the extent to which ignoring your issues-- the stuff that makes molecular and microbial evolution different-- is not unique to the EES Front. My impression is that most organismal biologists don't care about any of this. I think we still have a schism from 1969.

Arlin said...

My head is spinning. In Gould’s theory, the punctuations are merely rapid, not necessarily composed of non-infinitesimal increments. That is, punk eek does not require saltations, but only fluctuations in rate.

BTW, Simpson had some kind of theory of genetic catastrophism but it disappeared as he aligned himself more with neo-Darwinian orthodoxy.

Stebbins actually knew quite a lot about speciation by de Vriesian macromutations, in the sense of polyploidization in plants. However, his position was that these are always evolutionary dead-ends, i.e., they do not contribute to long-term evolution, higher taxa, etc. Some systematists took this same position for an entirely separate reason: wanting a clean hierarchical tree.

But today it is accepted that most animals and plants have ancestral polyploidizations in their lineages.

Arlin said...

Apropos of this, Soltis, et al 2014 provide an update on whole-genome-duplication. You have to read the paper to see that the constant references to Stebbins are legacy arguments to honor this hero for inspiring others to do actual research showing that he was wrong.

John Harshman said...

My point here is that Mayr does look inside the organism, at least in his head, and he doesn't assume that all necessary variation just exists in the population. To Mayr (and to Gould and Eldredge), the amount of change seen during speciation can occur only in special circumstances, i.e. when "coadapted gene complexes" are disrupted by, apparently, limited sampling of population variation in a peripheral isolate.

Arlin said...

Can you point me to some sources so that I can see exactly what he is saying?

People can articulate multiple conflicting theories, of course. In one passage on p. 603 of Animal Species and Evolution (1963), Mayr essentially re-articulates the orthogenesis position of Eimer, though he doesn't say the word, i.e., he goes totally completely off-script about the importance of evolutionary potential and says that this is necessary to understand parallel evolution.

Futuyma now cites this specific passage to show that the "Synthesis" includes developmental biases in variation. I always have a good laugh at Futuyma's tricks.

Mikkel Rumraket Rasmussen said...

Something about this argument of gradualism vs punctuation is pointless if one does not define exactly the magnitude of what constitutes an "infinitesimal" and a "saltation". Whole genome duplication is macromutation, or saltational, why? This must be defined beforehand, you can't just point to something after the fact and say "yeah this one is bigger than these other ones so it's saltational". No, you define what would be saltational first by specifying some limits, and then you see if you can find examples that satisfy that definition.

If A evolved into B by multiple successive rounds of mutation, how big must the magnitude of any one such mutation be to constitute an infinitesimal versus saltational mutation? And what exactly is it we are saying is big or small? The size-difference of some morphological attribute(if so, how much bigger or smaller must it become with one mutation to be infinitesimal, or saltational?), or it's effect on reproductive success, or the number of bases that are different between ancestral and descendant genetic locus, or genome size?

Arlin said...

The question of whether a particular episode of change is gradual or saltational can be resolved in various ways. One approach is to focus on historic examples. Chromosomal abnormalities, hybridization, and autopolyploidy have always been understood to be macromutations. The dominant dwarfism of Ancon sheep is an example of saltation cited by Darwin and many others. Homeotic mutations like antennapedia were understood to be macromutations. Meanwhile, the change in coat color of hooded rats in the Castle experiment, and various examples of quantitative changes in livestock and crops, represent gradual change under the multiple-factor model.

This approach is very clear, but is limited in scope. It doesn't tell us whether a lateral transfer is a macromutation, because no one talked about them 100 years ago.

Fisher concluded that the smallest possible changes are the most likely basis for adaptation. This also represents a very clear standard. Lateral transfers clearly violate this standard. In the gradualist version of lateral transfer, a new gene would be moved from one genome to another in many small steps, rather than one giant leap.

A different approach is used in quantitative genetics. If two species differ in a trait by X, then it might be the case that this maps to differences at 200 loci, each with an effect of X / 200. That would clearly be consistent with gradualism. But if there is one locus that accounts for 50 % of X, this is called a "major effect" locus.