Developmental plasticity is not Lamarckism

Sometimes, people email me with good questions. Here's one.

When I was a kid, my own visualization of evolution was Lamarckism.

But I didn't know it. In reading Dawkins and others, I know it doesn't exist. But it seems this article is claiming it does to some extent. Can you comment? I'm curious as to the current consensus as I've been reading a lot about genes that can be turned on and passed to offspring. Can you take a look?

This is a fairly common question. Looked at naively, developmental plasticity seems to be Lamarckian -- we're talking about organisms responding with morphological changes to their environment, just like Lamarck's example of the giraffe stretching its neck. But that's only the first step; the transmission of a distribution of traits to the next generation is purely Darwinian.

The article that prompted the question is about an experiment in Polypterus, in which the fish were raised in a terrestrial environment, and consequent changes in their limbs and behavior were observed.

A species of fish native to Africa could shed light on the evolutionary process that led fish to move on to dry land. The Dragon fish, Polypterus senegalus is not a normal fish – it has two lungs, and can survive outside of water. In a new eight-month experiment researchers have shown that if a Dragon fish is raised outside of water, the fish changes notably. The fish raised out of water showed differences in their bones and muscles involved in movement not shown in those raised in water.

Fish moved on to dry land and evolved into quadruped vertebrates around 400 million years ago, and it is thought that the Dragon fish is a living demonstration of a phenomenon known as developmental plasticity. This theory states that a creature’s physiology can be changed by environmental factors, and that overtime, these changes are incorporated in to the animal’s genome.

Hans Larsson, of McGill University’s Redpath Museum says that the aim of the experiment was to see the physical changes on Dragon fish that are raised out of the water.

“We wanted to push them in this new environment to see if we could reveal this cryptic variation, and if it works, what does it look like?”

Here's a video of the animals, illustrating the outcome of the experiment.

Very cool, right? But it doesn't contradict modern evolutionary theory at all -- in fact, it doesn't require any new concepts, but only the marriage of an understanding of evolution and development. Let's take those concepts step by step.

Most genetic variation is neutral or nearly so -- it has no detectable effect on the phenotype or on viability. Genetic variation can accumulate by drift, but if the differences don't have any differential effect on survival or reproduction, selection doesn't care. Most of the variation between humans, for instance, is cryptic: you don't see it, it doesn't do much of anything that we can see, but if you look at genes or proteins directly, you can find little differences. Consider blood types, for example: you can't tell by looking at someone whether they are type A, B, AB, or O, and mostly these don't seem to matter to the individual (I'm glossing over immunological effects -- there is evidence that the blood groups may have arisen in response to malaria infections, for instance).

In order for selection to work, genetic variation has to be visible to it. These cryptic variations only matter if they are made visible to selection. Blood types didn't have a major effect on people UNTIL blood transfusions became common responses to major injuries…and then having a rare blood type became a detriment. (Again, or until people are otherwise immunologically challenged by parasites with a differential response to blood antigens)

Organisms are plastic: that is, they change their patterns of gene expression in response to the environment. We don't change blood types, so developmental plasticity is not going to be a major factor there, but other properties of our body are amenable to change. Exercise regularly, your muscles get bigger; eat lots of candy bars, you accumulate fat. There are also genetic differences within these responses. Some people build muscle easily when working out, others are slow to change; some people can eat lots of calories without storing it all as fat, others have metabolisms that shunt most of their intake directly into fat production.

Changing the environment leads to plastic changes in gene expression, which exposes genetic variation to selection. If candy bars were not readily available, the different degrees of fat storage in different people would not be an issue -- nobody has the surplus calories, so everybody has the same lean body. You can't select for the variants either way. Dump a load of candy bars on that population, though, and selectable differences will emerge.

The experiments with Polypterus show something similar. The animals have an inherent capacity for building stronger limbs that is not visible when they are raised continuously in an aquatic environment, but when they are raised in a terrestrial environment, they tend to reinforce bones to a degree that resembles that of fossil fishopods. This is not surprising, any more than it would be surprising if you grew stronger pecs if I forced you to do pushups every day, all day. It also isn't Lamarckian if you work out and bulk up.

Where it has evolutionary consequences is in the opportunities it opens for selection. If early fish had a propensity for building more robust bones in a terrestrial environment, which allows them to live longer or be more mobile on land, the act of living on land first creates an opportunity for variants that increase terrestrial mobility to be operated on by selection. These variants would be invisible if the animals were always living in the water, after all.

So this is why when we talk about genetic assimilation and say the phenotype comes first, then the genotype arises to consolidate the adaptation, we aren't talking about anything contrary to standard Darwinian modes of selection. Developmental plasticity creates situations in which otherwise invisible genes can become subject to selection.