Natural Selection By Proxy

Here, I'll give a short summary of one of my favourite studies of recent decades: John Endler's ingenious field and laboratory experiments on small tropical fish¹, which in my (distinctly non-expert) opinion constitute one of the most compelling and 'slam-dunk' proofs available of the theory biological evolution by natural selection. After I've done that, in an act of unadulterated vanity, I'll suggest an extension to these experiments that I feel would considerably boost the information content of their results. That will be what I have dubbed 'selection by proxy'.

Don't get me wrong, Endler's experiments are brilliant. I first read about them in Richard Dawkins' delightful book, 'The Greatest Show on Earth,' and they captured my imagination, which is why I'm writing about them now.

Endler worked on guppies, small tropical fish, the males of which are decorated with coloured spots of varying hues and sizes. Different populations of guppies in the wild were found to exhibit different tendencies with regard to these spot patterns. Some populations show predominantly bright colours, while others prefer more subtle pigments. Some have large spots, while other have small ones. Its easy to contemplate the possibility that these differences in appearance are adaptive under different conditions. Two competing factors capable of contributing a great deal to the fitness of a male guppy are (1) ability to avoid getting eaten by predatory fish, and (2) ability to attract female guppies for baby making. Vivid colourful spots might contribute much to (2), but could be a distinct disadvantage where (1) is a major problem, and if coloration is determined by natural selection, then we would expect different degrees of visibility to be manifested in environments with different levels of predation. And so colour differences might be accounted for.

Furthermore, the idea suggests itself to the insightful observer that in the gravel-bottomed streams in which guppies often live, a range of spot sizes that's matched to the predominant particle size of the gravel in the stream bed would help a guppy to avoid being eaten, and that the tendency for particle and spot sizes to match will be greater where predators are more of a menace, and greater crypsis is an advantage. 

These considerations lead to several testable predictions concerning the likely outcomes if populations of guppies are transplanted to environments with different degrees of predation and different pebble sizes in their stream beds. These predicted outcomes are extremely unlikely under the hypothesis that natural selection is false. Such transplantations, both into carefully crafted laboratory environments, and into natural streams with no pre-existing guppy populations, constituted the punch line of Endler's experiments, and the observed results matched the predictions extraordinarily closely, after only a few months of naturally selected breeding. 

Its the high degree of preparatory groundwork and the many careful controls in these experiments, however, that result in both the high likelihood, P(D_p | H I), for the predicted outcome under natural selection, and the very low likelihood, P(D_p | H' I), under the natural-selection-false hypothesis. These likelihoods, under almost any prior, lead to only one possible logical outcome, when plugged into Bayes' theorem, and make the results conclusive.

The established fact that the patterning of male guppies is genetically controlled served both causes. Of course, natural selection can not act in a constructive way if the selected traits are not passed on to next generation, so the likelihood under H goes up with this knowledge. At the same time, alternate ways to account for any observed evolution of guppy appearance, such as developmental polymorphisms or phenotypic plasticity (such as the colour variability of chameleons, to take an extreme example), are ruled out, hitting P(D_p | H' I) quite hard.

Observations of wild populations had established the types of spot pattern frequent in areas with known levels of predation - there was no need to guess what kind of patterns would be easy and difficult for predators to see, if natural selection is the underlying cause. The expected outcome under this kind of selection could be forecast quite precisely, again enhancing the likelihood function under natural selection.

Selection between genotypes obviously requires the presence of different genotypes to select from, and in the laboratory experiments, this was ensured by several measures leading to broad genetic diversity within the breeding population. This, yet again, increased P(D_p | H I). (Genetic diversity in the wild is often ensured by the tendency for individuals to occasionally get washed downstream to areas with different selective pressures, which is one of the factors that made these fish such a fertile topic for research.)

The experiment employed a 3 × 2 factorial design. Three predation levels (strong, weak, and none) were combined with 2 gravel sizes, giving 6 different types of selection. The production of results appropriate for each of these selection types constitutes a very well defined prediction and would certainly be hard to credit under any alternate hypothesis, and P(D_p | H' I) suffers further at the hands of the expected (and realized) data.

Finally, additional blows were dealt to the likelihood under H', by prudent controls eliminating the possibility of effects due to population density and body size variations under differing predation conditions.

With this clever design and extensive controls, the data that Endler's guppies have yielded offer totally compelling evidence for the role of natural selection. Stronger predation led unmistakably to guppies with less vivid coloration, and greater ability to blend inconspicuously with their environment, after a relatively small number of generations.

I first read about these experiments with great enjoyment, but there was another thing that came to my mind: what the data did not say. It is quite inescapable from the results that natural selection of genetic differences was responsible for observed phenotypic changes arising in populations placed in different environments, but the data say nothing about the mechanism leading to those genetic differences. This, of course, is something that is central to the theory of natural selection. Indeed, we might consider the full name of this theory to be 'biological evolution by natural selection of random genetic mutations.' For the sake of completeness, we would like to have data that speak not only of the natural selection part, but also of the random basis for the genetic transformation.

I'm not saying that there is any serious doubt about this, but neither was there serious doubt about natural selection prior to Endler's result. (In fact, there is some legitimate uncertainty about the relative importance of natural selection v's other processes, such as genetic drift - uncertainty that work of Endler's kind can alleviate.) The theory of biological evolution, though, is a wonderful and extremely important theory. It stands out for a special reason: every other scientific theory we have is ultimately guaranteed to be wrong (though the degree of wrongness is often very small). Evolution by natural selection is the only theory I can think of that in principle could be strictly correct (and with great probability is), and so deserves to have all its major components tested as harshly as we reasonably can. This is how science honours a really great idea.

To test the randomness of genetic mutation, we need to consider alternative hypotheses. I can think of only one with non-vanishing plausibility: that at the molecular level, biology is adaptive in some goal-seeking way. That the cellular machinery strives, somehow, to generate mutations that make their future lineages more suitably adapted to their environment. I'll admit the prior probability is quite low, but I (as an amateur in the field) think its not impossible to imagine a world in which this happens, and as the only remotely credible contender, we should perhaps test it.

We could perform such a test by arranging for natural selection by proxy. That is, an experiment much like Endler's, but with a twist: at each generation, the individuals to breed are not the ones that were selected (e.g. by mates or (passively) by predators), but their genetically identical clones. At each generation, pairs of clones are produced, one of which is added to the experimental population, inhabiting the selective environment. The other clone is kept in selection-free surroundings, and is therefore never exposed to any of the influences that might make goal-seeking mutations work. Any goal-seeking mechanism can only plausibly be based on feedback from the environment, so if we eliminate that feedback and observe no difference in the tendency for phenotypes to adapt (compared to a control experiment executed with the original method), then we have the bonus of having verified all the major components of the theory. And if, against all expectation, there turned out to be a significant difference between the direct and proxy experiments, it would be the discovery of the century, which for its own sake might be worth the gamble. Just a thought.

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[1]	Natural Selection on Color Patterns in Poecilia reticulata, Endler, J.A., Evolution, 1980, Vol. 34, Pages 76-91 (Downloadable here)

Evolution of cooking

Or 'Food for thought'

What follows is a speculative idea about human evolution that occurred to me about two years ago. I’m not a biologist, but it’s a very simple idea, so its one I feel confident enough about to express it here. What is surprising, though, is that from the limited sources I have seen on the subject, none of the experts working in the relevant field has discussed this idea. I’d be delighted to hear from anybody who actually knows about biology whether the case I make here has anything going for it.

On the 2^nd of March, 2010 I watched a BBC ‘Horizon’ documentary outlining a controversial theory detailing the possible impact of the invention of cooking upon human evolution, in particular, suggesting that the cooking of food was originated by earlier hominids than usually accepted, and that this was instrumental in allowing Homo sapiens to evolve. (I made some quick notes the next days, which is why I know the date, but unfortunately I did not record the title of the program.)

According to wikipedia, ‘most anthropologists believe that cooking fires began only about 250,000 years ago.’ Here, however, you can read a brief summary of some evidence that cooking may have begun about 1.9 million years ago (substantially before H. sapiens appeared).

The main benefits of cooking food mentioned in the Horizon program were:

§     greatly increases the amount of energy gained from the food: > 20 % energetic profit for some foods studied

§     reduces the amount of energy needed to digest the food

These advantages are significant (and can be added to by the enormous saving in time required to chew a large meal of raw meat, compared to its cooked equivalent). One might well postulate that such advantages could have significant evolutionary effects. In particular, a reduction in size of the gut, and concomitant increase in size of the brain (not a necessary consequence, but perhaps enabled by it).

One of the major objections to the theory seems to be (according to the program) that the practise of cooking may not have been around for long enough to affect evolutionary change.

It seems to me, however, that a major piece of evidence on this front was overlooked by the program and by the experts who contributed to it. One of the professors advocating the theory even alluded to this evidence, but in a totally backwards way. In casually speculating on how the practice of cooking may have got started, he said something like “a man accidentally drops his meat into a fire, takes it out and tries it, only to find that it is delicious.” My question to that expert is this: why on Earth would that man have found the cooked food delicious?

Now a reasonable hypothesis space concerning the question of why cooking makes food taste good consists of 4 options:

1. The molecules in cooked food are intrinsically delicious
2. The good taste of cooked food comes from the same molecules as are present in raw food – they are just released more readily following the heating process
3. The experience of enjoyment occurring when we eat a cooked meal is something we learn over the course of our lifetimes, in response to habitually eating such things
4. The experience of enjoyment occurring when we eat a cooked meal is an evolved response, brought about by natural selection resulting from certain advantages to eating food in this form

Number 1 would seem to be manifestly preposterous.

About number 2, as a non-chemist, I’m going further out on a limb here, but I expect that the molecules contributing to the delicious taste and smell of cooked food are mostly totally different from those that are emitted by and contained in raw food. The Maillard reaction, for example between denatured proteins and sugars requires a temperature of over 150ºC, and is responsible for much of what tastes good when we eat cooked meat and some other cooked foods (unless it has been boiled, I suppose).

We could well imagine that an organism regularly eating raw meat would have receptors and neural circuits adapted to provide a pleasurable experience from the taste and smell of raw meat – it would be to its evolutionary advantage. But the smell and taste of cooked meat comes, I expect, not just from more of the same scent molecules, liberated more copiously by the cooking process, but mainly from totally different molecules, produced by the exposure to heat. The first individual to taste cooked meat would, therefore, have had no reason to experience enhanced pleasure, as there would have previously been no selective pressure to evolve any special response to those cooked scent molecules, to which the individual’s ancestors were never exposed.

Option number 3 is harder to quickly refute. It is clear that different nations and cultures have different ideas about what constitutes yummy. We can quickly confirm, however, that at least some reactions to tastes are innate, rather than conditioned. Many natural poisons taste very bad to us, even though we do not receive much childhood exposure to them. Conversely, some plants seem to use noxious tasting chemicals that are not poisonous as a defence against would-be grazers – they seem to make use of an animals innate expectation that something tasting like this is sure to be bad for you. Thus, we can see that a substantial part of an animal’s response to certain tastes is likely not due to learning acquired during the animal’s own experience. As I briefly discuss below, one can imagine experiments that might shed light on the extent of the influence of hypothesis number 3 for the current debate.

It seems to me then, that there is a reasonable argument in favour of possibility number 4, the theory that cooking has been in use for long enough to affect our evolution. Specifically, that it has led to the evolution of a rewarding experience of pleasure when we eat foods that are cooked. This feeling of ‘wow, that piece of scorched flesh was damn delicious,’ could easily be interpreted as a mechanism to overcome that urge: ‘god, I just spent the whole day chasing this bloody rabbit, can I really be bothered starting up a fire?’ The evolutionary advantage of overcoming this lazy urge is that the energy saved by not getting a fire going and preparing a cooked meal is much less than that gained by consuming the food in a partially pre-digested, cooked state.

If, as I suppose, the first people to eat cooked meat got no special pleasure out it (this holds for both hypotheses 3 and 4), one might well ask why they persisted in doing it. One must speculate here, but it is quite easy to hypothesize a good reason. We don’t even need to assume the ability to control fire, though it is quite possible that fire was controlled during the important period. It is known that humans have used fire as a tool for hunting – either for driving game, or as a means of killing game directly. In this way, early humans may have got into the habit of eating scorched foods, simply as a matter of convenience, thanks to this particularly efficient method of hunting. Alternatively, it may have been sufficient for our ancestors to make similar use of fires that started naturally. That there was a huge energetic bonus, on top of the efficiency of the hunting method, may have contributed to the evolution of mechanisms leading to enhanced satisfaction from eating food in this form. Maybe it was enough for some humans to recognise that cooked food is, in many cases, much easier to eat and takes less time to digest.

One aspect of the argument that might lend itself to experimental investigation is the question of whether an animal evolved for eating raw meat would prefer to eat cooked meat, given the opportunity. One might imagine experiments with such an animal placed an equal distance from two sources of hidden food, one cooked and one raw. One then simply needs to observe which food type the animal goes to first. A refinement of the experiment might be to replace the foods with standardized sources of scent molecules corresponding to the two different food types – standardized so that the concentrations in the air are equal for each. We can control for the influence of hypothesis number 3, above, by dividing the test subjects into two groups – one that has previously been fed exclusively on raw food, the other having been fed on cooked food. We could even imagine doing similar experiments on human babies, young enough that they have never tasted any meat: incorporate the flavours of raw and cooked meat into two bowls of rice porridge, and see which they prefer.