Do not personify natural selection

Natural selection is not an entity like Cher, Lady Gaga, or the Statue of Liberty, and it is not a force like wind. It is more correctly characterized as a description of a mechanism of differential survival of individuals in a lineage, rather than the cause itself. In his later years, Darwin regretted using the term in a causal sense, rather than sticking with the more forthright ‘struggle for existence’. Natural selection, personified as a force that acts on organisms, becomes little more than a rhetorical equivalent of a Deity when placed in sentences such as ‘Natural selection would favor the acquisition of such-and-such a feature’. Substitute ‘God’ or ‘elves’ for ‘natural selection’ and the emptiness of this rhetoric becomes clear, even though, with evidence, the statement about what was favored could be supported (Figure 9). The problem is in writing as if you were ascribing the ‘favoring’ of a trait to an actual, personified third party, rather than explaining the circumstances by which it was favored. Language like this is really not much different than that used by the advocates of ‘Intelligent Design’. Yet Darwin used it many times himself in The Origin of Species.

Figure 9 The problem with personifying natural selection is that it always seems to come to have an identity of its own. In this way it is little different from the narrative actions committed by gods or even leprechauns. Full size image

How better to phrase this? Darwin’s own formulation was to explain that the traits in any given lineage at any given time showed considerable variation. Some of these variations worked better than others at the time, for whatever circumstantial reasons. Their bearers were more likely to survive to leave offspring with these same variations. In the struggle for existence, they were better able to persist. We would call that entire process natural selection. This is more accurate than saying ‘natural selection favored this particular trait’.

An extension of this kind of personification is when an author says, ‘Natural selection would have favored the acquisition of such-and such a trait’. Nobody knows in advance what ‘natural selection would favor’, because virtually everything we know about the effects of natural selection is in hindsight. This phraseology suggests a naïve faith in the optimality of evolutionary processes, and some omniscience on the part of the author, in continuing to personify natural selection as if it were a conscious being. Of course, scientists do not really think these things (do we?); we just write as if we do. Natural selection is a description of a process, not an actor; we recognize it as a post hoc outcome of the struggle for existence.

Natural selection is not ‘creative’

Remembering the previous point, it is more accurate to say that in the struggle for existence, some individuals are weeded out before they can reproduce. This process is not creative, any more than a lawnmower is creative with your backyard grass. Recombination of features through sexual reproduction might - might - be analogized as ‘creative’, except that the recombination is entirely random. (In contrast, the pigment splashes on a Jackson Pollock painting only look random; they are actually highly creative.) And really: why push it? The term is anthropomorphic. Leave creativity to the artists.

Avoid ‘evolved for’

Teachers knowledgeable about evolution have a very hard time with this expression. It is almost obvious as soon as you say it. We all know that structures do not ‘evolve for’ some function. But this sloppy diction gives the uninitiated the impression that there is a direction to evolution that is manifestly teleological. Yes, there are evolutionary trends of many kinds; but organisms do not want to get to one point on an evolutionary continuum and look backward with the idea that life has been a long struggle to get to that point, as if consciously.

For example, feathers did not evolve ‘for’ flight. They were already performing several functions for the dinosaurs that had them before one lineage happened to use them aerodynamically. Among the earlier functions were insulation, color patterns (display or camouflage or species recognition), and even brooding on nests (Padian 2008c). The evolution of features in a group of organisms can be like the man who got up on his horse and rode off in all directions. There was not a goal in sight, so it is better to avoid language that suggests it.

Evolution is not universally a question of ‘pressure’

There is no doubt that individuals in nature face enormous selective pressure throughout their lives - the result of competition, predation, insufficient resources, and environmental stress. However, when we think about new adaptations that seem to have contributed so much to the success of varied groups of organisms, we get a different picture. Most of the critical ‘inventions’ in evolutionary history do not seem to have happened because there was intense pressure for something like that to happen. At least, we cannot find much evidence for this, except perhaps in cases such as the evolution of dense fur by mammals as ice ages encroached. (We presume that natural variations in the length and thickness of fur were favored in the struggle for existence.) Rather, these ‘inventions’ evolved because organisms found an opportunity to exploit a new way of doing things. For example, we do not think that birds evolved flight because they were forced to do so. However flight evolved, it was an opportunity to turn the structure and functions of forelimbs and feathers to new purposes.

;One way to explain this is through economics. Given that analogies are only teaching tools; they do not represent a real material connection. Nevertheless, students understand it when you explain that microwave technology was developed during World War II as a way to try to detect aircraft activity; and now we have ovens that use this technology in virtually every home and office. There was not an economic ‘pressure’ to develop microwave ovens; it was an opportunity that manifested itself, based on an incentive to solve a completely different problem. In evolution we call this exaptation, and it is one of the most important concepts in the field, even though it was only identified in One way to explain this is through economics. Given that analogies are only teaching tools; they do not represent a real material connection. Nevertheless, students understand it when you explain that microwave technology was developed during World War II as a way to try to detect aircraft activity; and now we have ovens that use this technology in virtually every home and office. There was not an economic ‘pressure’ to develop microwave ovens; it was an opportunity that manifested itself, based on an incentive to solve a completely different problem. In evolution we call this exaptation, and it is one of the most important concepts in the field, even though it was only identified in One way to explain this is through economics. Given that analogies are only teaching tools; they do not represent a real material connection. Nevertheless, students understand it when you explain that microwave technology was developed during World War II as a way to try to detect aircraft activity; and now we have ovens that use this technology in virtually every home and office. There was not an economic ‘pressure’ to develop microwave ovens; it was an opportunity that manifested itself, based on an incentive to solve a completely different problem. In evolution we call this exaptation, and it is one of the most important concepts in the field, even though it was only identified in 1982 by Stephen Jay Gould and Elisabeth Vrba.

‘Fitness’ is not about how many offspring you leave

Darwin (1859) used the word ‘fitness’ to describe how well-suited an organism is for its environment. If a horse were more fit, it could better outrun its predators (or at least outrun the horse next to it, who became someone’s breakfast). On the face of it, this concept does not seem to be related to leaving offspring, so let us see how the concept of ‘fitness’ became for so many evolutionary biologists ‘how many offspring you leave’.

In the early days of the Modern Synthesis of Evolution, nearly 1 century ago, mathematical biologists were struggling with ways to quantify the ability of some individuals to survive better than others. Darwin called this ‘fitness’. But how were these modelers to quantify an adaptive advantage? The advantage needed to be hereditary, but there were no obvious genes for ‘adaptive advantage’, even though coefficients of selection for given alleles were used even in the earliest literature of the Modern Synthesis (Provine 2001).

Consider the larger picture. Those individuals that were better adapted, Darwin and Wallace said, would be more likely to survive and reproduce, passing their traits to the next generation. The mathematicians took a shortcut, redefining ‘fitness’ to represent the number of offspring that an individual left. That became the ‘mean fitness’ or ‘w’ of a population.

But here is the problem. What is important is not that individuals who are better adapted will leave more offspring. (They do not always.) It is that they are more likely to survive to reproductive age and leave offspring. What’s more, their offspring will be better adapted to environmental conditions than other offspring. What is the difference between these ideas? Plenty. Consider that in any population there could be genes for higher and lower fecundity (the production of offspring). In other words, how many offspring you produce is independent of how well adapted they will be to their surroundings.

The corruption of the Darwinian term ‘fitness’ can be shown mathematically. Consider two lineages, A and B. B has 1.2 times the fecundity of A, but in hard times B has only 0.60 the survivability of A, which is a better competitor. In times of relaxed selection, B will out-reproduce A by 20% per generation. But if selection pressure is strong, that increased fecundity will be diminished by a 60% survival rate, so compared to lineage A, lineage B will have a survival rate of 1.2 × 0.6, or 72% of that of lineage A. It is not about the number of offspring you produce; it’s about their survivability (Figure 10).

Figure 10 Why fecundity (the Neo-Darwinian index of ‘fitness’) alone does not assure better representation in the next generation. It depends on survivability, that is to say, adaptive ‘fitness’, which is what Darwin was talking about. The underlined numbers convey the differential in success under hard and soft selection. See text for explanation. Full size image

This would have been obvious to Darwin and Wallace, who were (like all other literate people of their time) well steeped in Malthus’s (1803, among many editions) Essay on Population. The poor, Malthus wrote, are profligate with their offspring, irrespective of their means of support or future prospects. But it does not make them more successful.

By this reasoning, the number of offspring you leave cannot be regarded as a proxy for your adaptive ‘fitness’, because those offspring could be competitively inferior. If the ‘struggle for existence’ is particularly difficult, few of them (if any) will survive, so fecundity alone is not a virtue. (In fact, it could be a disadvantage if many offspring have to compete for the same limited resources.) When Darwin speaks in the Origin about leaving more offspring, he is presuming that these offspring carry inherited traits that are better adapted for the environment; and the reason their parents are leaving more offspring is that more of them are surviving to reproductive age than the individuals who were less well adapted.

What, then, is fitness? The population biologists appropriated the term long ago, so we are stuck with regarding it as related to reproductive success (essentially, fecundity) rather than individual adaptiveness, as Darwin used it - unless it is implicit that the success carries with it better genes, not simply more offspring. It is therefore a question of the quality of the offspring, a reflection of their inherited characteristics. Individuals with features better adapted to their surroundings will pass on those features to their offspring, who are likely to be better adapted than others who lack them. But the reason that they have better adapted offspring is that they have passed on more advantageous features to the next generation.

Now we can see our way through a classic evolutionary pdox, notably pointed out by the evolutionary geneticist C.H. Waddington (1967). In the diction of the Modern Synthesis, he noted, ‘survival of the fittest’ becomes a tautology. The ones who leave the most offspring are the most fit; and how do we know they are the most fit? Because they leave the most offspring. Creationists seized on this circular reasoning to embarrass evolutionists, and the definition of the Modern Synthesis provided no way out of it.

But there is a way out. The missing logical step, as Waddington said, is the one that the population modelers omitted (see above): the most fit (that is, prolific) individuals - those who leave the most offspring in the next generation - are assumed to be the ones whose traits are best adapted to their environments. That is a testable hypothesis. We can test whether the traits that we think are most advantageous were really preferentially inherited by the next generation. If not, the hypothesis of natural selection is not sustained in a particular case. Without testing whether presumably better adapted individuals are the ones with greater reproductive success, natural selection is an assumption rather than a scientific hypothesis.

Sexual selection is not a kind of natural selection

Darwin faced a problem when he was writing his great treatment on natural selection that eventually was distilled to On the Origin of Species. He could explain, he thought, why features that improved the ability of an organism to survive and carry out its functions would be favored and passed along in future generations. But he knew it would be harder to explain why some features (such as the famous peacock’s tail) persisted and were often strongly conspicuous, even though they seemed to have no purpose in helping an organism to survive. He observed that in nearly all cases, these features were useful in the struggle for mates, rather than in the struggle for existence. And for this reason he septed this phenomenon, which he called sexual selection, from the process of natural selection.

Although some authors state that sexual selection is ‘a kind of’ natural selection, this view is incorrect (Padian and Horner 2011a, 2011b). Darwin not only explicitly septed the two concepts; he acknowledged that they were quite often in conflict (what if the peacock’s long tail makes it easier for a predator to catch it?). He even wrote a book about it: The Descent of Man, or Selection in Relation to Sex (1871). He clearly felt that sexual selection was as important in the evolution of humans as natural selection was. And, although he acknowledged that the roles of some morphological structures of animals are difficult to determine, he was adamant about how to recognize when they had a role in sexual selection (Figure 11). This brings us to the next point.

Figure 11 Darwin regarded sexual selection, a concept he originated and defined precisely, as something very different than natural selection. In this hierarchy of terms related to social recognition in lineages, it can be seen that sexual selection is only a small and very specialized syndrome within a larger context of choosing and competing for mates. Full size image

Sexual selection requires sexual dimorphism

Despite extensive confusion in the recent literature, Darwin was clear about what sexual selection is, and what the role of sexual dimorphism (conspicuous differences between males and females) is in it (Padian and Horner 2011a, 2011b). He stated in the plainest language in the Origin of Species (pp. 79–80):

‘Thus it is, I believe, that when the males and females of any animal have the same general habits of life, but differ in structure, colour, or ornament, such differences have been mainly caused by sexual selection; that is, individual males have had, in successive generations, some slight advantage over other males, in their weapons, means of defence, or charms; and have transmitted these advantages to their male offspring’.

Because Darwin invented sexual selection, and because he based it on observations that have never been falsified, his definition cannot be wrong. It has three components: (1) it explains why sexual dimorphism exists, and its central role in sexual selection; (2) the dimorphic structures or behaviors are used by one gender to attract mates or repel rivals for mates; and (3) these structures and behaviors help the bearer gain access to mates (not necessarily leave more offspring, but to leave offspring more competitive in mating; Figure 12). Darwin needed to define this concept as he did because he knew that opponents would complain that natural selection (which was a description of how the adaptive, Darwinian ‘fitness’ of individuals should increase through generations) could not account for bizarre structures that were used to enhance mating success, but could be a liability to one’s survival, as we have seen in the previous point. Sexual selection was invented precisely to explain unusual dimorphic structures used in mating, and therefore dimorphism is essential to it.

Figure 12 Darwin stressed that sexual dimorphism was the linchpin of sexual selection; indeed, this was the only way he could explain the evolution of bizarre features in one sex - because they were used either to attract mates or repel rivals. Full size image

Again, as with natural selection, sexual selection is not simply a matter of producing more offspring. It is about leaving more offspring in the next generation who have the features that are desired by potential mates, or competitive in attracting them. This advantage should eventually allow the numbers game to take care of itself in future generations; it is not simply a matter of fecundity.