What Fodor and Piattelli-Palmarini got wrong – part 3: issues left dangling

In this final post on Fodor and Piatelli-Palmarini's book What Darwin got wrong I will deal with the bits and pieces that didn't really fit into my previous two posts.

Cutting down the tree of life?

The authors discuss the process of horizontal gene transfer, which they call non-Darwinian and non-adaptationist. Horizontal gene transfer refers to the transfer of genetic material from one organism to another in a manner different from the typical genetic inheritance by offspring. Bacteria can be genetically altered through uptake of DNA from their surroundings and lateral gene transfer can occur through cell to cell contact or through a virus. Fodor and Piatelli-Palmarini note that

...horizontal gene transfer is the rule, rather than the exception, in microorganisms, to the point that the very notion of a 'tree of descent' is being questioned. The preferred metaphor in microbiology is that of a bush or a network (Doolittle, 1999).

Is it time to cut down the tree of life? According to the New Scientist magazine (1-24-2009) the answer is yes! Moreover, this implies that Darwin was wrong according to New Scientist. 

There are really two issues here. First, is the tree of life still a good model for evolution? Second, is the tree of life Darwinian? When contemplating the tree of life model we need to realize that horizontal gene transfer as well endosymbiosis (the view that mitochondria and chloroplasts were originally 'free' bacteria that were taken inside a eukaryotic cell) primarily belong to the world of microorganisms. If we wish to hold on to the tree of life model we can take these complications into account. We would have something like this:

However, since these complications primarily occur in microorganisms we can simply ignore them when dealing with animals. For example, the whole evolutionary tree from fish to human remains unaffected. Perhaps that helps to place things into perspective.

Is the tree of life a Darwinian idea? Well, not long after his Beagle voyage he did contemplate the tree of life model:

This is taken from his own notes and the words "I think" show that this is very much a work in progress. When Darwin finally published his ideas two decades later he did not use the tree of life model, but rather he spoke of "descent with modification". David Penny makes this clear in a recent article published in PLoS Biolgy. According to Penny descent with modification encompasses a variety of processes including both horizontal and vertical gene transfer. 

Furthermore, Darwin's main legacy is of course the theory of natural selection. Whatever the mechanisms behind the modifications, natural selection is what largely determines which modifications will spread and which will not.

Adapting to an ecological niche

Fodor and Piatelli-Palmarini complain that evolutionary biologists use the fit between organisms and their ecological niche as evidence for natural selection. Of course organisms fit their ecological niche, because otherwise they wouldn't be with us today:

...a creature's ecology consists of whatever-it-is-about-the-world that makes its phenotype viable. That's to say: it is constituted by those features of the world in virtue of which that kind of creature is able to make a living in the world. In effect, the notions 'ecology' and 'phenotype' (unlike the notions 'environment' and 'phenotype') are interdefined. Since they are, it's hardly surprising that a creature's phenotype reliably turns out to be in good accord with its ecology.

But why are there still animals around? How does evolution deliver phenotypes that fit some ecological niche? Natural selection is Darwin's answer, but Fodor and Piatelli-Palmarini, who reject this solution,  admit that they do not know. Perhaps it's worth while to look at a few ways in which species make a living and ask "if not natural selection, then how did this species get this way?"

A famous example is the adaptive radiation of Darwin's Galapagos finches (and yes, the figure below represents an evolutionary tree).

Natural selection has an elegant and straightforward explanation of the differences between these strongly related bird species (none of which are found anywhere else). A single species made it all the way from South America and then it spread over the different islands and started to adapt to the different ecological niches. Mutations that affected the size and shape of the bird's beak made it better or worse at eating insects, seeds or eggs. We find similar adaptive radiations on other island groups. How to explain this if not be natural selection?

And what about evolutionary arms races?

Why did the cheetah evolve to run so fast and to turn so agile? To catch antelope that are also really fast and agile. Why did species of antelope evolve to run so fast and to turn so agile? Because cheetahs and other big cats are also so fast and agile. Circular reasoning? Yes, put like this it is, but it is of course a gradual process in which any mutation that increases speed or agility in big cats or antelope gives it a survival advantage against members of the same species without the mutation. This keeps on going until we get animals like the cheetah, with a ridiculous speed of 115 km/h, and the wildebeest and Thomson's gazelle with a speed of 80 km/h. Natural selection can make perfect sense of these evolutionary arms races. What is the alternative?

Another great piece of evidence for natural selection comes from mimicking animals. For example, take the butterfly papilio dardanus. Professor Armand Leroi explains the implications of mimicry in this marvelous BBC documentary (go to 25:35).





My personal favorite example of mimicry is the Indonesian mimic octopus:




What can explain the amazing mimicry of this octopus? Natural selection has an answer: it has evolved to act in specific ways in specific situations (see for example this press release from the California Academy of Sciences). When a mutation affects the way the octopus responds to certain stimuli then a response that mimics another species may influence its ability to escape predators, especially if the mimicked species is itself a predator or a venomous animal. The octopus is not aware that it is mimicking another species, it just does what it does because it works. If mimicry is not explained by natural selection then I really would like to hear a plausible alternative. Fodor and Piatelli-Palmarini certainly haven't offered one.

To conclude, the authors have not managed to prove Darwin wrong, at least not with regards to natural selection as the main driving force behind evolution. Sure, there were many things Darwin did not know. He was writing in the mid 19th century which makes it rather obvious that he couldn't be right about everything related to evolution. Yet, the theory of natural selection has stood up amazingly well to all critique. I think "What Darwin didn't know" is a much better way of phrasing the developments in evolutionary biology since Darwin. If you haven't yet had a chance I'd recommend watching the BBC documentary above that takes precisely this approach.

What Fodor and Piattelli-Palmarini got wrong – part 2: the 'selection-for' problem

In my previous post I discussed some developments in evolutionary theory that Fodor and Piatelli-Palmarini thought were problematic for Darwinism. I saved their main argument for another post. So what is their main argument? In their own words:

Because selection-for is intensional (or, if you prefer, because what are selected-for are not creatures, but their traits, and the individuation of traits is intensional) there can be coextensive but distinct phenotypic properties, one (but not the other) of which is conducive to fitness, but which natural selection cannot distinguish. In such cases, natural selection cannot, as it were, tell the arches from the spandrels. That being so, adaptationist theories of evolution are unable, as a matter of principle, to do what they purport to do: explain the distribution of phenotypic traits in a population as a function of its history of selection for fitness.

Their point is that some traits are linked so that a change in trait t1 will go together with a change in trait t2. In these cases t1 might have been selected for and t2 might be a free-rider (i.e. does not influence fitness), or t2 might have been selected for and t1 might be a free-rider. Natural selection cannot distinguish these two alternatives. The basis for this argument comes from a paper by Gould and Lewontin (1979). In the above quote Fodor and Piatelli-Palmarini allude to this paper when they say that "Natural selection cannot, as it were, tell the arches from the spandrels." What do arches and spandrels have to do with natural selection? Gould and Lewontin make an analogy between the free-riding of spandrels when building arches for a dome. The spandrels are the triangular shaped spaces between adjacent arches.

The point is that when the arches are designed the spandrels will appear as well. You cannot have arches without spandrels. Likewise, in evolution two traits might be linked such that selection for trait t1 will also produce the free-rider t2. The lesson is that we need to be careful when we try to discover what a trait was selected for, because the trait might just as easily have been a free-rider. At no point do Gould and Lewontin deny natural selection, but Fodor and Piatelli-Palmarini actually argue that the argument undermines natural selection.

The authors seem to be somewhat confused about how natural selection is supposed to work:

An important consequence of genetic pleiotropism is that, when a gene affects several traits at once, any change in that gene that is not catastrophic (any viable mutation) will affect all or most of its traits. Supposing that one such change in one such trait is adaptive, then natural selection will eventually fixate that mutation. But then all the other changes in all the other traits will also be stabilized, possibly opening up wholly different selective processes, eventually dwarfing the effects of the initial selection driven by the initially adaptive trait.

This line of argumentation is quite baffling and seems to be a consequence of thinking of an intensional force called natural selection selecting for traits on the basis of fitness. If two traits are genetically linked then natural selection cannot select for one of them only to be affected by the other trait at a later time. The correct way of thinking about natural selection was explained by Richard Dawkins in The selfish gene: Selection occurs at the level of the gene. When a genetic mutation increases reproductive success this mutation will spread through the population. It is irrelevant how many traits are affected by the mutation: natural selection will work on the overall outcome and not the individual traits. Traits are not selected, but genes are.

Not surprisingly, the authors return to a comparison between natural selection and operant conditioning (their other archnemesis) to explain the problem. What if we train a pigeon to differentiate a yellow triangle from an X. Whenever the pigeon pecks at the yellow triangle it gets a food reward, but when it pecks at the X it does not. The pigeon will then learn to peck at the yellow triangle. But, ask Fodor and Piatelli-Palmarini, what has the pigeon really learned? Did it learn to peck at anything yellow? Did it learn to peck at a triangle? Did it learn to peck at a yellow triangle? Take a look at this video if you will to see operant conditioning of a pigeon in action:

 



What has the pigeon learned? Has it learned to peck at the word "PECK" and to turn at the word "TURN"? Has it learned to peck at letter "P" or "E" or "C" or "K" and to turn at the letter "T" or "U" or "R" or "N"? Fodor and Piatelli-Palmarini think this is a problem and that the only way to solve this problem is to examine counterfactuals. For example, we could present the letter "T" without the whole word "TURN" and see what happens, or we could present "URN" and see what happens. Why is this relevant for natural selection? Well, just like the letter "T" and the word "TURN" are coextensive in the operant conditioning experiment, some traits are coextensive in evolution by natural selection. The problem, according to the authors is that we cannot examine counterfactuals, because we cannot examine t1 without t2 if t1 and t2 are coextensive. This is perfectly true, but I think the analogy shows that they are missing the essence of both operant conditioning and natural selection. While it is true that we cannot distinguish between learning "T" and learning "TURN" on the basis of this single experiment, it should be noted that this is not what researchers are interested in when they do these experiments (at least not primarily). There are many interesting and important things we can learn about operant conditioning without caring at all about the actual stimulus. For example, as Skinner explains in this video, we can learn about how different reinforcement schedules affect behavior. Whether they learn the letter "T" or the word "TURN" the effect of reinforcement schedules will be similar and this is what matters. This effect generalizes to other species including humans and we can learn about gambling addictions on the basis of these experiments.

Likewise, the phenomenon of linkage is really not the most important aspect of natural selection. Yes, some traits are genetically linked, but this in no way challenges natural selection. Darwin argued that there is (1) descent with modification and (2) evolution by natural selection. Indeed, we know that mutations occur and this underlies descent with modification. Regardless of what the modification is and regardless of how many traits are affected by the mutation this modification is then subjected to natural selection. We know that phenotypic differences can result in different reproductive success. This is natural selection and it is a fact. It may not be the only way evolution occurs (we also have genetic drift for example), but it certainly plays an important role in evolution.

I will conclude this post with a quote from Fodor and Piatelli-Palmarini concerning what I think is their real interest in their attack against natural selection:

...since the Otxi 'master' gene controls the development of the larynx, inner ear, kidneys and external genitalia and the thickness of the cerebral cortex, selective pressures sensitive to changes in the function of the kidneys (due to bipedal station, or different liquid intake and excretion resulting from floods or droughts), or the fixation of different sexual patterns, may have in turn secondary effects on the expansion of the cerebral cortex and the structure of the larynx. The peculiarity of the overall picture of the evolution of language and cognition in humans, should this reconstruction prove to be correct, has been stressed to us by Boncinelli (personal communication).

This speculative hypothesis by Boncinelli was precisely what Fodor and Piatelli-Palmarini were looking for, because of their disapproval of the field of evolutionary psychology. They do not like the idea that cognitive mechanisms in humans were adaptations, so any idea that the increased brain size in humans was 'free-riding' on a different adaptation is music to their ears. There are two points to stress here: First, even if this were true it is still completely consistent with natural selection. 'Selective pressures sensitive to changes in the function of the kidneys...' is natural selection in action. So perhaps the authors aren't really challenging natural selection per se, but the view that every single trait must be an adaptation. Well, linkage is a well-known concept in evolutionary biology, so if this is their point they are merely beating a straw man. Second, even if the linking of these features were really as simple as is proposed here (surely there are other genes involved in addition to otxi) then natural selection operates on the combined effect of all these changes. Since there are reasons to believe that an increased brain size (a development lasting a few million years mind you) gave our ancestors survival benefits, it is unlikely that this would have been a 'free-riding' effect. Rather, it would have contributed, together with the other changes (e.g. in the kidneys), to the spread of the underlying genetic mutation.

 

What Fodor and Piattelli-Palmarini got wrong – part 1: evo-devo and epigenetics

How can one ignore a book with a provocative title like “What Darwin got wrong”? Jerry Fodor and Massimo Piattelli-Palmarini argue that natural selection cannot be the driving force behind evolution. So here we have a book challenging the core of evolutionary biology, written bytwo cognitive scientists. It would seem like a futile exercise and unfortunately for the authors that is precisely what it is.

The authors make comparisons between the theory of natural selection and Skinner's theory of learning by operant conditioning. Fodor and Piattelli-Palmarini are after all cognitive scientists and cognitive psychology really took over from behaviorism and Skinner's theory of operant conditioning in the late 1950s and the 1960s. Operant conditioning theory describes modification of behavior as a result of learning associations between responses and reward or punishment. While it cannot be denied that operant conditioning provides a useful model for some forms of learning it is believed that behaviorists like Skinner took their theory too far and focused too much on stimuli and responses and ignored what happens in between, the mental states and cognitive processes that cognitive psychology holds so dearly. This is behaviorisms infamous back box. Fodor and Piattelli-Palmarini seem to be making the comparison between operant conditioning and natural selection, because they want to imply that natural selection essentially has the same kind of problems as operant conditioning. The whole comparison is really quite irrelevant; the theory of natural selection must be judged on its own merits.

The next step in Fodor and Piattelli-Palmarini's approach is to go through a number of developments in evolutionary biology, which they believe challenge Darwinism or neo-Darwinism (the synthesis of natural selection theory with Mendellian genetics). Among the developments discussed by the authors are epigenetics and evo-devo. I will focus on these developments here, but I will not deal with Fodor and Piattelli-Palmarini's arguments directly. In this section of their book they appear to be challenging a simple uni-dimensional evolutionary model, but this is not the essence of Darwinism. To challenge Darwinism one needs to show that Darwin was wrong about (1) descent with modification, or (2) natural selection as the main driving force behind evolution. I will argue that evo-devo and epigenetics pose no problem for Darwinism and natural selection. Fodor and Piattelli-Palmarini have a more direct assault against Darwinism in the remainder of their book and I will leave that for a later post.

Evo-devo, or evolutionary development, focuses on how genetic and epigenetic factors interact during the development of an organism. Epigenetics here simply refers to non-genetic (epi = besides, above) factors, or rather environmental factors that influence how a genome is expressed and how an organism develops into its phenotype.

In this picture, based on a photographic survey by Michael Richardson (see PZ Myers blog),  we see that there is remarkable similarity across vertebrate species in the phylotypic stage of development (top row). In this stage the basis for each subsequent vertebrate body plan is set. PZ Myers explains on his blog:

At this time in development, vertebrate embryos all express a suite of characters that are common to the entire vertebrate lineage: they have a notochord and a dorsal nerve cord, they have pharyngeal arches and a tail, and they have a repeating series of blocks of muscle called somites. Most of the features that distinguish different vertebrate groups, such as limbs or fins, hair or feathers or scales, and wings or forearms, haven't yet developed. In addition, we now know that this is the period during which a set of crucial pattern forming genes (the emx/otx/hox genes) is first expressed, and lay down the molecular blueprint of the body plan.

What evo-devo shows is that there are complex interactions between genes and that the effect of a certain mutation on the resulting phenotype is likewise complex. The simple unidimensional picture of a gene for x and a gene for y is to some extent misleading. Fodor and Piattelli-Palmarini are correct on this point. Does this in any way challenge Darwinism? Well, lets discuss two different ways in which development occurs. First, there's what is called canalized development, where a certain developmental trajectory becomes strongly regulated, so that is becomes less vulnerable to change. The activity of some genes can compensate for variability in other genes. Within such canalized developmental trajectories it can therefore occur that certain mutations of genes do not ultimately affect the phenotype. Why would some developmental trajectories become canalized? Ken Richardson explains in his book The evolution of intelligent systems:

Many environmental conditions are sufficiently constant from generation to generation to allow the development of fairly uniform structures in organisms, with little variation between individuals. This is the classical Darwinian natural selection scenario, and the beaks of Darwin's finches are good examples, along with numerous other aspects of all living things......... canalization has evolved for developmental adaptation to aspects of environment that, like seeds for finches, reliably occur across generations.

Canalization is completely understandable from a Darwinian natural selection perspective. At the opposite extreme from canalization we have developmental plasticity. This is where epigenetics comes in. It turns out that there are environmental influences on certain developmental trajectories. Because of this the same genotype does not necessarily result in the same phenotype. There are many interesting examples of how epigenetics influences development and one of these was presented to me as I was working on this blog post. While watching a recorded episode of the BBC program QI I saw a picture of the first cloned cat:

The cloned cat CC (for copycat) is in the top right picture and in the bottom picture together with its surrogate mother. The genetic donor is in the top left picture. As you can see the coloration is different (compare the top two pictures). So we have the same genotype, but a different phenotype. Unfortunately QI got their facts wrong as they only showed the bottom picture (clone plus surrogate mother) and claimed they were genetically identical. Getting something like CC from a tabby seems a bit too much to ask for epigenetic effects.

Epigenetic effects are seen in natural circumstances across the board. Lets start small and work our way up to humans. Richardson gives the example of the water flea Daphnia. If developing juveniles detect the presence of predatory midge larvae they develop protective neck spines or helmets. Interestingly, Daphnia with large helmets also produce offspring with helmets even in the absence of the midge larvae. The epigenetic effects are here transgenerational!

In the top picture we see a Daphnia with a clonal brood of offspring (i.e. genetically identical); in the bottom picture the Daphnia has developed a protective helmet (pictures from the NSF).

Epigenetic factors also influence the timing of life history events in amphibians (metamorphosis) and even mammals (birth). For example, Crespi and Denver (2005) found that tadpoles of the western spadefoot toad accelerate metamorphosis in response to water volume reduction or food restriction. The accelerated metamorphosis allows the toad to leave the aquatic environment so that it can find a more desirable environment, although this comes with a cost to its growth.

Crespi and Denver note that stressors such as maternal malnutrition, hypoxia or infection have effects in mammals that correspond to the accelerated development and early metamorphosis in amphibians. That is, fetal development is accelerated and the probability of preterm birth is dramatically increased. Humans are no exceptions. The 1944-1945 famine in the Netherlands caused many preterm babies and babies with lower birth weight. Maternal malnutrition also gave the children an increased chance of developing obesity and anti-social behavior. Even though these children did not experience malnutrition during their adult lives their children also turned out to have a lower birth weight. In other words, the epigenetic effects were to some extent transgenerational, just as the Daphnia protective helmets and neck spines.

Why do organisms respond to these external influences in these ways? Clearly, somehow the development is affected by chemicals, hormones and other signals that provide information about the environment. What determines how the organism responds to these signals? The answer here is natural selection. Far from being challenged by these findings, they make perfect sense from a Darwinian perspective. Chemicals and hormones from the external environment will interact with gene expressions in complex ways and the effects will naturally depend on which genes are being expressed. If there is a genetic mutation the external signals may have different effects. If the modified effect of the external signals somehow has a survival value then it will be favored by natural selection. It is of course no coincidence that Daphnia respond to chemical hormones of the predatory midge larvae by developing defense structures. This development was primed by natural selection. It is also no coincidence that tadpoles respond to low water levels or lack of nutrition by doing precisely what it should do to escape the pond, that is accelerate metamorphosis. Again this response must have been primed by natural selection. Finally, concerning the effects of maternal malnutrition during the Dutch famine of 1944-1945 it cannot be a coincidence that the effects on the developing fetus prepare the fetus for life outside the womb. These children favored fatty foods, precisely as you would expect if the child has been developmentally prepared for an environment in which food is scarce. Unfortunately this leads to obesity if it turns out that there actually is sufficient food in the environment. According to Dick Swaab the anti-social behavior might also be part of the preparation for an environment in which one needs to struggle to get sufficient food. How is it possible that the fetus prepares for the environmental conditions? Dick Swaab explains (my translation):

To conclude, the fetus appears to “think” only about short-term survival and adjusts to the difficult circumstances that it expects immediately after birth. Of course, the fetus doesn't “think” about these things. Millions of years unborn children have been exposed to these kinds of threats. One time a child had a mutation that allowed it to adjust better to the problems that were waiting for it, and this favorable mutation spread through the population.

I would suspect that there were multiple mutations involved and that some of them might even go back tens if not hundreds of millions of years, given that there are similarities in the way amphibians and mammals respond to environmental factors.

Epigenetics, and the field of evo-devo in general, do not appear to challenge the theory of natural selection one bit, regardless of what Fodor and Piattelli-Palmarini claim. Apart from the fact that epigenetic effects are just as much subject to natural selection as genetic effects, it should also be noted that the transgenerational effects of epigenetics generally appear to be limited. Authors report that the effects can last for a few generations, but how does that compare to genetic mutations, some of which have been with us for over hundreds of millions of years? Perhaps the limited transgenerational effects are to be expected as these epigenetic effects seem very suitable for modifications contingent on the current situation in the environment. They are part of the developmental plasticity that is needed for changing environmental conditions.

Although there have been many interesting findings related to epigenetics it appears that not all evolutionary biologists are impressed. In The greatest show on earth Richard Dawkins calls epigenetics “a modish buzz-word now enjoying its fifteen minutes of fame in the biological community." He also complains that its enthousiasts cannot even agree with themselves, let alone each other, what epigenetics actually means. Ouch! Here I've been using the term epigenetics as non-genetic effects during development that change the phenotype. It remains to be seen how the field of evo-devo will change evolutionary biology and what will become of epigenetics, but one trend certainly seems to be a greater appreciation for how organisms develop and how genes and environment interact in complicated ways to form a phenotype. My gut feeling is that an increased focus on evolutionary development is one good thing that has come out of this research.

Men having sex with men

Indian health minister Ghulam Nabi Azad has received a great deal of criticism for saying that gay sex is not only unnatural, but even a disease. Although homosexual intercourse was decriminalized by the Delhi high court in 2009, homophobic attitudes and plain ignorance die hard.

Recently my wife told me about a homophobic incident at our daughter's school in Lelystad. It was toy day, which means that the kids were allowed to bring a toy to play with at school. One of the boys had decided to bring a doll, much to the horror of a dad who had just arrived with his child. He went over to the mother of the boy and told her that it was a very bad idea to let the boy play with dolls because that could turn him gay!

I think homophobic dad and minister Azad should have a chat with brain researcher Dick Swaab who has done extensive research on sexuality and sexual orientation. They would learn about the brain differences (in the hypothalamus) between homosexuals and heterosexuals and they would learn that these brain differences are already determined before birth. It really doesn't matter much what happens to a child after birth; try what you will, you will not change its sexual orientation. In his book Wij zijn ons brein, Swaab also mentions the many unsuccessful ways in which people have tried to "cure" homosexuality: hormonal treatments, castrations, electroshock, epileptic insults, jail time, testis transplants, psychoanalysis, and brain operations. It was all to no avail even though some men under intense social pressure would pretend to be "cured".

What I find interesting about homosexuality is that there is also a strong genetic factor involved. You may wonder how that is possible. Surely natural selection would select against homosexuality if this leads to a reduced number of offspring? Jeremy Yoder recently wrote a really nice piece on this issue on a guest blog at Scientific American. This quote reflects his general idea:

Natural selection causes traits associated with having fewer children to become less common over time. But natural selection is not the only evolutionary process at work in natural populations. Mutation introduces new alleles even as natural selection removes them. Furthermore, the effects of random chance in small populations creates an effect called genetic drift, which can interfere with the expected operation of natural selection.

You really need to read the whole piece to understand what he means though. Yoder backs up his ideas with nice simulations, although they are just intended to clarify his ideas as the actual genetic conditions are likely different. For example, as Yoder himself admits the situation becomes quite different if multiple genes are involved. Indeed, if homosexuality is the effect of interactions between multiple genes then there might not even be selection against the individual genes, especially if they have other positive effects. As indicated by Yoder evidence for a positive effect of genes that cause homosexuality in males comes from the observation that genes that cause homosexuality in males may provide a fitness advantage for females.