How do evolutionary novelties arise? The conventional explanation is that the first step is the chance formation of a genetic mutation, which results in a new phenotype, which, if it is favored by selection, may be fixed in a population. No one sensible can seriously argue with this idea—it happens. I'm not going to argue with it at all.
However, there are also additional mechanisms for generating novelties, mechanisms that extend the power of evolutionary biology without contradicting our conventional understanding of it. A paper by A. Richard Palmer in Science describes the evidence for an alternative mode of evolution, genetic assimilation, that can be easily read as a radical, non-Darwinian, and even Lamarckian pattern of evolution (Sennoma at Malice Aforethought has expressed concern about this), but it is nothing of the kind; there is no hocus-pocus, no violation of the Weissmann barrier, no sudden, unexplained leaps of cause-and-effect. Comprehending it only requires a proper appreciation of the importance of environmental influences on development and an understanding that the genome does not constitute a descriptive program of the organism.
We know intuitively that the latter is not the case. We can see that any time we look at a developmental mistake: biology is plastic, and tries to accommodate errors, even gross errors, and assemble a functional organism. For instance, it is fairly easy in the lab to induce two-headed organisms (and they happen spontaneously in the natural world often enough). This is obviously a radical change! As one class of problems, think of the plumbing: a single heart needs to supply blood to two brains, and the aorta has to sprout a series of carotid arteries. And it does. Muscles, nerves, guts, respiratory pathways…all have to reorganize themselves in a sensible way in the absence of any central genetic program specifically evolved to cope with such a surprising phenomenon. Development is a process that tries to respond in a constructive way to a series of inputs, and what comes out tends to have a functional logic to it.
This capability of the organism to respond developmentally to changes in its environment allows us to think in a different way about how novelties arise. Instead of appearing first as a genetic change in an individual ("genotype precedes phenotype" evolution), a new morphology may be a consequence first of a consistent response to a common environmental condition which is only later reinforced by the evolution of genetic causes (note: the genetic causes do not arise as a direct result of the environmentally induced condition, but instead the condition makes mutations that support it more favored by selection; this is not Lamarckism!). This is "phenotype precedes genotype" evolution.
The idea may feel counterintuitive to those of us steeped in the genecentric tradition of modern biology, but trust me, it has substantial popularity in the evo-devo crowd. It's a central theme of Mary Jane West-Eberhard's excellent Developmental Plasticity and Evolution, a book I can't recommend highly enough to anyone who wants to get into the details (it's not a book for casual readers, unfortunately—it's fairly dense and technical). There are a number of terms that are used liberally when discussing the concept, so I'm going to take some definitions straight from West-Eberhard's book and try to explain how they work.
Phenotypic accommodation: "the immediate adaptive adjustment of the phenotype to the production of a novel trait or trait combinations." My example of the two-headed animal is an example of phenotypic accommodation, as is the two-legged goat effect. Development will remodel morphology to a remarkable degree around almost any perturbation, whether the cause is genetic or environmental. We are very, very good at working around stresses in development. In a sense, that's why development has evolved.
Given that we can respond to variations in the environment with variations in the pattern of development, we then have the ability to acquire morphological innovations with no specific genetic cause at all. These cannot have any direct, long-term evolutionary effect in the classic sense, of course, because they aren't passed on to offspring (although we do often pass on our environment to our offspring...but let's not think about that right now. There are some possibilities for really radical evolutionary theories here.) What they can do is allow an organism to thrive in an environment which selects for new heritable traits, a phenomenon called the Baldwin Effect: "the idea that phenotypic accommodations to variable or extreme conditions can affect the direction of genetic evolution under natural selection, permitting survival in an unusual environment and allowing time for selection to favor adaptation to it." This is a key idea behind "phenotype precedes genotype" evolution. (Social Learning and the Baldwin Effect, by David Papineau, is a good online source if you want to learn more about the effect.)
The end result of all this, the part that brings this mode of evolution into full compatibility with neo-Darwinian ideas, is genetic assimilation: "a process by which a phenotypic character, which initially is produced only in response to some environmental influence, becomes, through a process of selection, taken over by the genotype, so that it is found even in the absence of the environmental influence which had at first been necessary." Where canalization refers specifically to increasing constraints on a developmental pathway, genetic assimilation is a broader term that refers to the acquisition of a genetic mechanism to support any developmental outcome; we could imagine assimilation of a genetic factor that widens flexibility, for instance.
A related concept is canalization: "an evolved reduction in developmental flexibility that renders the development of an adaptive phenotype resistant to environmental and genetic (e.g., mutational) perturbations that would produce deviations from optimal form." This is an idea advanced by Waddington. If a particular organismal morphology is particularly successful, mutations that make it robust and resistant to change would be advantageous; canalization is a conservative process that would oppose evolutionary change. One of the biases inherent in with working with many lab animals, such as Drosophila or the zebrafish, is that we suspect that development in these fast-growing model systems is highly canalized, i.e. relatively rigid and very strongly determined. Focusing on these organisms gives us an underestimate of the range of variation present in the development of less tightly constrained species.
There lies a problem. Demonstrating the details of the influence of the environment on the organism has been somewhat elusive, since lab animals have been chosen for the property of minimizing such influences, and most lab research involves reducing variables by reducing environmental variation. Expressing an adaptive trait in response to environmental influences exclusively should also be a transient feature in the evolution of a species, perhaps found only in localized populations.
I hope that overview convinces everyone that there is nothing unreasonable or heretical about genetic assimilation, and that there is no obstacle in principle to it occurring. The only question here is whether it is a significant factor in evolution, and that is where Palmer's paper comes in: he argues that we can see evidence of genetic assimilation in the evolution of a rather important feature in evolution, bilateral asymmetry.
A hallmark of the Bilaterians, like us and flatworms and fish and cows, is bilateral symmetry: we have left and right halves that are at least superficially mirror images of one another. However, underlying that is a secondary asymmetry. Our hearts are lopsided because one half has a harder job to do than the other; our livers are mostly on one side of our body; and some organisms, such as snails, have a characteristic handedness to their spiral form.
However, emerging from this diversity are two fundamentally different, yet easily distinguished, types: antisymmetry, in which dextral and sinistral forms are equally common within a species, and directional asymmetry, in which most individuals are asymmetrical in the same direction. These two asymmetry types differ in an important way. In antisymmetric species, direction of asymmetry is almost never inherited, whereas in directionally asymmetric species, it typically is.
Antisymmetry is the key case. There are organisms that exhibit bilateral asymmetries which are not determined genetically; different individuals have right- or left-handed organs, and the parental pattern is not passed on to their progeny. One of the things the paper does is catalog fossil and extant species that exhibit antisymmetry and ask how often a period lacking genetic control precedes the establishment of a fixed handedness, a situation illustrated diagrammatically below.
What he found was that roughly half the time, evolution has followed route b, with no sign of tight genetic control at first, followed by a more consistent handedness, indicating that genetic assimilation had occurred. The other half, route a, directional asymmetry is always present. However, genetic assimilation is going to be typically undercounted for reasons I've already mentioned, so occurrence in half of the cases is almost certainly going to be an underestimate.
Another analysis carried out in the paper is an examination of the molecular pathways behind known chordate asymmetries. There is an array of genes that are activated asymmetrically in the development of the heart, for instance, a pathway called the nodal signalling cascade. There are four highly conserved genes, Nodal, Lefty1, Lefty2, and Pitx2, that seem to be universal in function in the vertebrate lineage; you can think of them as the heart of the heart pathway. The curious thing, though, is that the genes that precede the nodal pathway vary in different animals, and also, there are many non-conserved genes downstream of nodal. While the core module is the same, it is activated in different ways and has divergent effects!
We've seen this pattern before, as the author notes.
Variation in the nodal cascade among vertebrates, like variation in mechanisms controlling primary axis formation, resembles an hourglass: a short, conserved core in the middle of the signaling pathway, the Nodal-Lefty1-Lefty2-Pitx2 pathway, with divergent elements upstream and downstream. Vertebrate embryos, therefore, appear to pass through a molecular phylotypic stage, a conserved stage that may provide clues about ancestral developmental pathways, during ontogeny, just as they appear to do morphologically.
How interesting and how odd. How could this have happened?
One suggestive observation is that urochordates and cephalochordates have some differences in the core heart genes, and that ascidian larvae have symmetrical hearts, while lancelet asymmetries seem to be the result of an asymmetrical cleavage pattern. The nodal pathway isn't used to generate heart asymmetries at all; instead, it seems to be crucial in defining brain asymmetries. The idea is that the heart initially exhibited antisymmetry, and that the mechanism of genetic assimilation involved the independent recruitment of a core brain pathway to add a layer of genetic control to the process.
I think Palmer has made a good case that at least some fundamental properties arose in evolution as a result of genetic assimilation, and that it ought to be better appreciated as a factor. He concludes by mentioning other examples of the process.
Is genetic assimilation as common among other traits as among biological asymmetries? Regrettably, because compelling evidence is difficult to obtain, rather few natural examples are known. They include (i) the shell shape in freshwater snails, which responds plastically to turbulence in some populations but not others; (ii) viviparity in reptiles, in which some optionally retain eggs in the oviduct and others consistently do so; (iii) sex determination in turtles, in which environmental control is ancestral, but genetic control has evolved six times; (iv) leaf form in buttercups, in which some populations produce aquatic or aerial leaves in response to growth conditions, but others grow only aerial leaves; and (v) antattracting extra-floral nectar secretion in Acacia trees, which occurs only after insect attack in some species but is continuous in derived (obligate ant-hosting) species. Genetic assimilation may be much more widespread than currently believed.
Palmer AR (2004) Symmetry breaking and the evolution of development. Science 306:828-833.
I'm currently slogging my way through "The Plausibility of Life" by Kirschner and Gerhart and Sean Carroll's book "Endless Forms Most Beautiful". I wonder if you have previously commented on either or both books, and how the two compare in your estimation.
Thanks for your time....Scott
I think this little blurb from the companion site to Scott Gilbert's textbook, which includes a brief description of the classic experiments by Waddington that led him to coin the term "genetic assimilation", might help make the basic concept a little easier for readers of this post to understand.
This post is on the right track. But if you say "genetic assimilation is a process by which a phenotypic character, which initially is produced only in response to some environmental influence, becomes, through a process of selection, taken over by the genotype, so that it is found even in the absence of the environmental influence which had at first been necessary", it IS kinda akward you then say "genetic assimilation is a broader term that refers to the acquisition of a genetic mechanism to support any developmental outcome; we could imagine assimilation of a genetic factor that widens flexibility, for instance." To me this is only compatible with the above if you argue that some environmental factor granted fleibility and has been replaced by some genetic factor. Does anything like that occur?
WW!!! gt vwls gn? ' ll try t bhv nw, prms.
Great post! Evolution has many hypotheses to be explored by the next generation. It may even turn out that ID is correct to the extent that some mechanisms are complex enough to require a complex designing process, and EVOLUTION IS THE DESIGNER.
We get one proof whenever a uterus creates a baby in 9 months out of nothing but fluids (3 per second around the globe). We see a better proof when something goes awry and a uterus creates functioning conjoined twins with two heads, two hearts, and a single pelvis. http://en.wikipedia.org/wiki/Conjoined_twins
hehe. That's really funny PZ.
PZ, could you update the internal links? Everything is pointed to the old website, which then gets redirected back to ScienceBlogs.
Hmmm, how do identical twins fit into something like this. They are the result of a zygote splitting into two separate embryos that develop fully, correct? Is there a genetic reason that this might occur (or at least occur more frequently) or is it entirely an environment related event? Are there species that regularly have identical twins (or triplets or whatever), and if so does this mean that genetic assimilation has occurred in these as well? It is often said that this type of animal or that always has twins (such as Pandas), but are they talking about fraternal or identical twins?
Anyway, a very fascinating post that makes me what to read more about evo/devo (well, I guess that I should say, makes me want to read about it even more. Thanks!
But PZ it still all comes down to natural selection and the relative fitness of organisms with different phenotypes that are produced by genetic variation. Phenotypic plasicity cannot be anything other than a genetic trait.
A fantastically cool (because it's in new-rons) example of antisymmetry just came out of Cori Bargmann's lab... two olfactory neurons that laterally inhibit each other via axon-axon contacts. here's the abstract
Scott, I'm reading Kirschner and Gerhart just after having finished Caroll and I'm enjoying it a lot more. Different intended audiences, I think.
Dr. John, there's a semantics problem there. In a sense, phenotypic plasticity is a genetic trait, but at the systems level. I don't think it can be considered in the same way as classic allelic selection and deserves separate attention.
Alexander, I'm not 100% sure I follow you, but maybe Sue Lindquist's work on heat shock proteins is the kind of thing you're looking for?
"In a sense, phenotypic plasticity is a genetic trait, but at the systems level. I don't think it can be considered in the same way as classic allelic selection and deserves separate attention. "
There are many models of classical type dealing with the evolution of phenotypic plasticity. Consult any literature database.
Genetic assimilation is mentioned in Falconer's textbook as selection on a quantitive character using two thresholds
I'm wondering whether sexual selection might be an example of how environmentally produced variation in the phenotype can become genetic. If the ladies (or the guys) like the new look, then mating success is improved. So if by random chance a genetic predisposition for the new look arises, then that genetic predisposition will become more common.
Scott Little: Yes. Armadillos.
Miko, well, environmental changes can also reveal hidden genetic variation much like loss of function of HSP90 does. Some population genstics models suggest an environmental change can expose hidden genetic variation without interfering with any HSP-like stabilizing mechanism, but as a result of general, standing epistatic interactions.
In any case I disagree with the concept of genetic assimilation defended in this post. I do not think genetic assimilation is an adequate term for a trait that increases its environmental sensitivity, even if this process depends on genetic change.
"Phenotypic plasicity cannot be anything other than a genetic trait"...bad mistake. In itself a contradictory statement. The idea of phenotypic plasticity is that the phenotype can be different despite sharing the same genotype, no?
Daryl McCullough wrote:
"I'm wondering whether sexual selection might be an example of how environmentally produced variation in the phenotype can become genetic. If the ladies (or the guys) like the new look, then mating success is improved. So if by random chance a genetic predisposition for the new look arises, then that genetic predisposition will become more common."
Such a scenario might not be as feasible as it sounds. The environmentally produced variation might be random or specific to the environment. If the environmentally produced variation is random, it should be random over offspring - so selection on any genetic mutant will be independent of the environmental variation. (This is the noise environmental variation in genetics)
Or, the environmental variation is due to a reaction norm. If offspring disperse at random over the environment, selection on the mutant might again be independent of the environmental variation. If animals stay in their parents' environment, where the preferred genotype is already produced environmentally, genetic variation might well be neutral. You'll have to write alternative models to get a grip on such a proposed mechanism.