Kevin Laland's new view of evolution

The recent meeting at the Royal Society in London was organized by The Royal Society (UK) and The British Academy. The theme of the meeting was, "New trends in evolutionary biology: biological, philosophical and social science perspectives." The main organizers were Denis Noble, Nancy Cartwright, Patrick Bateson, John Dupré, and Kevin Laland. The point of the meeting was to discuss new evolutionary theory.

It's difficult to describe everything that went on at the meeting because so much of it was details about individual research results. These scientific talks were often presented as an alternative to modern ways of thinking about evolution. The general theme was that the Modern Synthesis was out-of-date and needed revision or, perhaps, replacement. There was very little discussion of evolutionary theory and how best to interpret those results. The data was supposed to speak for itself.

The only serious objections came from scientists who claimed the Modern Synthesis had already incorporated the ideas of niche construction, plasticity, epigenetics etc. This message was promoted mainly by Douglas Futuyma and Russell Lande. They weren't very successful.

I think that was the wrong message. I think the Modern Synthesis is effectively dead. It died 45 years ago when the importance of non-Darwinian evolution became evident. I'm certain the vast majority of participants were completely ignorant of molecular evolution and random genetic drift. They missed the revolution [see Is the "Modern Synthesis" effectively dead?].

Here's a quotation from Douglas Futuyma's textbook Evolution (2nd edition, 2009).

Since the evolutionary synthesis, a great deal of research has elaborated and tested its basic principles, and these principles have withstood the tests. But progress in both evolutionary studies in other fields of biology has required some modifications and many extensions of the basic principles of the evolutionary synthesis, and has spurred additional theory to account for biological phenomena that were unknown in the 1940s....

As molecular and computational technology has become more sophisticated and available, new fields of evolutionary study have developed. Among these fields is molecular evolution (analysis of the process and history of change in genes), in which the Neutral Theory of Molecular Evolution has been particularly important. This hypothesis, developed especially by Mootoo Kimura (1924-1994), holds that most of the evolution of DNA sequences occurs by genetic drift rather than by natural selection, but it provides a foundation for detecting effects of natural selection on DNA sequences. Because entire genomes can now be sequenced, molecular evolutionary studies have expanded into evolutionary genomics, which is concerned with variation and evolution in multiple genes or even entire genomes.

Let's look at an article by Kevin Laland published in New Scientist at the end of September (2016). It was obviously intended to publicize the meeting.

Laland is a professor at the University of St. Andrews in Scotland (UK). His main research interest is the evolution of human behavior and he promoted the importance of niche construction at the meeting. The New Scientist article was published as part of a series on "Evolution: Selfish genes aren't in control after all. Organisms help direct their own evolution."

Laland's article is "Evolution Evolves: Darwin's and Wallace's brainchild is still spawning radical ideas. Kevin Laland describes a vision of evolution for the 21st century." The online title is: Evolution evolves: Beyond the selfish gene For more than 150 years it has been one of science’s most successful theories, but we need to rethink evolution for the 21st century.

The article begins by explaining that "Darwin’s beautiful idea explains why there are hundreds of thousands of species of beetles and flowering plants, why birds’ feathers are ideal for flight and insulation, and why a desert plant possesses hairy leaves to reduce water loss."

That's only partly true. The Theory of Natural Selection (Darwin's beautiful idea) may explain feathers and hairy leaves but it certainly does not explain diversity. That's the first problem.

As we look more closely at Laland's ideas we actually see two problems. The first is that he is attacking a strawman version of evolutionary theory—one that's extremely adaptationist. The second problem is thinking that Dawkins' view of the selfish gene is the dominant metaphor in modern evolutionary theory. We see this second strawman in statements like,

Yet all scientific theories must incorporate new ideas and findings, and evolution is no exception. In recent years, our understanding of biology has taken huge strides. Advances in genetics, epigenetics and developmental biology challenge us to think anew about the relationship between genes, organisms and the environment, with implications for the origins of diversity and the direction and speed of evolution. In particular, new findings undermine the idea, encapsulated by the “selfish gene” metaphor, that genes are in the driving seat. Instead, they suggest that organisms play active, constructive roles in their own development and that of their descendants, so that they impose direction on evolution.

I was surprised to discover in London that none of these "revolutionaries" could define "evolution" in any meaningful way. They give me the impression they are unsatisfied with "changes in allele frequencies in a population" but they have no reasonable alternative.¹ If niche construction just affects changes in allele frequencies then what's the fuss all about? Lots of things influence genetic changes in populations.

But let's concentrate on the first strawman that Leland is tilting at. He says,

Our current framework for thinking about evolution emerged only in the 1940s, with the integration of new knowledge about evolutionary processes and biological inheritance. This so-called modern synthesis is at the heart of how most people understand evolution. According to this view, the evolution of the features of an organism – collectively known as its phenotype – comes down to random genetic mutation, genetic inheritance and selection of those gene variants that bestow traits best adapted to the environment.

The modern synthesis has served us well: evolutionary biology is developing and thriving. But discoveries made over the past two decades are starting to reveal cracks in some of its central ideas.

Really? The "current framework" dates back to the 1940s and only considers selection? The only challenge to this view comes from discoveries that began in 1996?

This is the problem. Somewhere between the 1940s and 1996 there must have been a few advances in knowledge about evolutionary theory, right? (cough, King and Jukes, 1969).

Now it's one thing to consider non-Darwinian evolution and all the new ideas that were promoted in the 1960s, 1970s, and 1980s and then reject them in favor of the old-fashioned view of the adaptationist Modern Synthesis. I can respect that even though I think it's indefensible. But it's quite another thing altogether to be completely ignorant of all those ideas while advocating a revolution in 2016!

That's what Kevin Laland is doing and so are most of the other participants at the Royal Society meeting.

We can see it clearly because in Laland's article he gives us a nice summary of the "Modern vs Postmodern" views of evolution. Judge for yourself whether you think this is someone who's an expect on modern evolutionary theory.

Modern vs postmodern
Orthodox ideas about how evolution works are being challenged by new discoveries in genetics, epigenetics and developmental biology. This has led some researchers to propose that the current framework, known as the modern synthesis, be broadened into an extended evolutionary synthesis. The fundamentals remain the same, but they rest on quite different assumptions:

Modern synthesis
The major directing influence in evolution is natural selection. It alone explains why the properties of organisms are adapted to match those of their environments.

Extended evolutionary synthesis
Natural selection is not solely in charge. The way that an organism develops can influence the direction and rate of its own evolution and its fit to its environment.

The problem here is that Laland is not wrong about the Modern Synthesis. He's just wrong about the fact it represents the modern view of evolution. As Douglas Futuyma pointed out at the meeting, all modern textbooks have chapters on random genetic drift and plenty of discussion about nonadaptive evolution, especially at the molecular level. It makes you wonder whether the biologists at the Royal Society meeting ever read a modern textbook on evolution.

That's the part that really bothers me about this debate. However, let's pretend that Laland actually understood modern evolutionary theory. Does it make any sense to propose that it needs rethinking in light of the fact that organisms affect the environment they live in? No.

Modern synthesis
Genes are the only widespread system of inheritance. Acquired characters – non-genetic traits that develop during an organism’s lifetime – are not inherited and play no role in evolution.

Extended evolutionary synthesis
Inheritance extends beyond genes to include epigenetic, ecological, behavioural and cultural inheritance. Acquired characters can be passed to offspring and play diverse roles in evolution.

He's correct here about the Modern Synthesis and about modern evolutionary theory. The modern view does not recognize that changes in the frequency of non-genetic characteristics of a population over time counts as biological evolution.

Epigenetics, which has been around for 50 years, is not a major new player in evolution. To the extent that it's important, it's genetic. Cultural and behavioral evolution are real phenomena but they're not biological evolution.²

Modern synthesis
Genetic variation is random. Mutations that occur are not necessarily fitness-enhancing. It is mere chance if mutations give rise to features that improve the ability of organisms to survive and thrive.

Extended evolutionary synthesis
Phenotypic variation is non-random. Individuals develop in response to local conditions, so any novel features they possess are often well suited to their environment.

Almost all evolution is ultimately due to mutation of one sort or another. Many people believe that the chance occurrence of mutation is the dominant theme of evolution. The statement about the Modern Synthesis is perfectly correct, to a first approximation. (We can quibble about details.)

The idea that phenotypes change according to local conditions—for example, the lac operon is expressed in the presence of lactose—is hardly revolutionary and doesn't require a change in our understanding of modern evolutionary theory.

Modern synthesis
Evolution typically occurs through multiple small steps, leading to gradual change. That’s because it rests on incremental changes brought about by random mutations.

Extended evolutionary synthesis
Evolution can be rapid. Developmental processes allow individuals to respond to environmental challenges, or to mutations, with coordinated changes in suites of traits.

Is it possible that Kevin Laland is completely unaware of the debate over gradualism, hybridization, symbiosis, horizontal gene transfer, homeotic mutations, saltation, and macromutations? Is it possible that he's never thought about punctuated equilibria, and hierarchical theory?

It's true that the old-fashioned views of Ernst Mayr and company ("Modern Synthesis") rejected all those ideas but evolution has moved on since the 1950s. It's no longer restricted to just gradual small steps.

The "revolutionaries" think mutations can be directed with an ultimate goal in view. The basic idea of enhanced mutation rates under certain conditions has been actively debated for a very long time (before 1996). It's not thought to be a major feature of evolution except in the sense of increasing the rate of "random" mutations.

Modern synthesis
The perspective is gene-centred: evolution requires changes in gene frequencies through natural selection, mutation, migration and random losses of gene variants.

Extended evolutionary synthesis
The view is organism-centred, with broader conceptions of evolutionary processes. Individuals adjust to their environment as they develop, and modify selection pressures.

This description of the Modern Synthesis is the only time I've seen Kevin Laland mention something that resembles random genetic drift. It's clearly not part of his normal worldview.

I agree that modern evolutionary theory is "gene-centered" in this way. That's because we DEFINE evolution as a change in allele frequencies in a population. I don't know what it means to shift to a view that's "organism-centered" in the way Laland describes. It's certainly true that individual cyanobacteria adjust to their environment as they grow and develop and it's certainly true they can change the environment. In this case, they caused an increase in oxygen levels that affected all living species.

Cyanobacteria evolved to adjust to their environment by random mutations and changes in allele frequencies in the population due, in part, to selection. Many became extinct. How is that a change in our view of evolution?

Modern synthesis
Micro-evolutionary processes explain macro-evolutionary patterns. The forces that shape individuals and populations also explain major evolutionary changes at the species level and above.

Extended evolutionary synthesis
Additional phenomena explain macro-evolutionary changes by increasing evolvability – the ability to generate adaptive diversity. They include developmental plasticity and niche construction.

It was a basic tenet of the Modern Synthesis that macroevolution can be efficiently explained as just lots and lots of cumulative microevolution. Modern evolutionary biology textbooks discuss other features of macroevolution that require additional input, especially in speciation. The old idea that microevolution is sufficient to account for macroevolution is no longer the axiom in evolutionary biology and hasn't been for many decades [see Macroevolution].

Modern textbooks discuss all kinds of things that influence the long-term history of life (= macroevolution). Things like mass extinctions, stasis, allopatric speciation, constraints, etc. Evolvability has been actively debated for half-a-century and it's well-covered in most textbooks. (See Futuyma, 2nd ed. p. 599). Evolvability is hardly a new idea that's going to revolutionize evolutionary theory. In fact, the consensus view, after much debate and discussion, is that evolvability flounders on the shoals of teleology. The theory just doesn't hold up to close scrutiny.

Organismal selection for traits that confer differential reproductive success in the ecological moment simply cannot generate, in any active or direct manner, a set of features that achieves evolutionary significance only by imparting flexibility for change in the distant future. We cannot deny that these features of evolvability deeply "matter" in the history of lineages; but how can benefits for futures arise by any causal process in the here and now? (Gould, 2002 p. 1274)

It's disingenuous to imply, in an article intended for the average reader, that a subject like evolvability is recent and hasn't been thoroughly vetted, and rejected, in the theoretical literature on evolution. The same thing applies to the concepts of plasticity and niche construction. They aren't new concepts. The knowledgeable experts in evolution—the ones who have read, and written, the textbooks—have examined these ideas and rejected them as major factors in evolutionary theory.

Kevin Laland may disagree with those analyses but as a scientist he has an obligation to at least mention them when he writes articles promoting a radical change in evolutionary theory. He has a responsibility to declare his bias.

But I'm making an assumption that may not be warranted. Maybe he doesn't know that his views have already been debated, discussed, and, for the most part, rejected. In that case, his omission isn't because he's deliberately misleading his readers about the controversy. There's another reason.

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1. The focus on heritable change (alleles) is part of the current minimal definition of evolution. It's very different than the "selfish gene" perspective promoted by Richard Dawkins. Those who fail to see the difference are just not paying attention.

2. I wonder how "cultural evolution" works in cyanobacteria and maple trees? The major participants at the Royal Society meeting have an extreme bias toward evolution of complex multicellular organisms—mostly animals and mostly mammals. This greatly colors their perspective on evolution. They tend to uses examples that apply only to their species of interest as levers to tip over all of evolutionary theory.

King, J. L., and Jukes, T. H. (1969) Non-darwinian evolution. Science, 164:788-798. PDF