The Meaning of Fitness

Thanks to the phrase “survival of the fittest”, fitness is quite a prominent idea in the popular perception of evolution. The description was originally coined by Herbert Spencer after he read On the Origin of Species; Darwin adopted it in later editions and it’s been popular ever since. Unfortunately, this glib phrase often eclipses a more accurate depiction of evolution, leading to some common misunderstandings. This confusion arises because “fitness” has a different meaning in evolutionary biology than it does in general usage.

What is fitness?
In its common usage, the term “fitness” is connected with the idea of being in shape and associated physical attributes like strength, endurance or speed; this is quite different from its use in biology. To an evolutionary biologist, fitness simply means reproductive success and reflects how well an organism is adapted to its environment. There are several ways to measure fitness; for example, “absolute fitness” measures the ratio of a given genotype before and after selection while “relative fitness” measures differential reproductive success — that is, the proportion of the next generation’s gene pool that is descended from a particular organism (or genotype) compared with competing organisms (or genotypes). Leaving those details aside, the point is that fitness is simply a measure of reproductive success.

This kind of fitness — differential reproductive success — doesn't always depend on traits such as strength and speed; reproductive success can also be achieved by mimicry, colorful displays, sneak fertilization and a host of other strategies that don’t correspond to the common notion of “physical fitness”. It's important to realize that the fittest organisms in a particular context won't necessarily be the ones that satisfy our cultural ideals. In fact, they'll often be the manipulative, well-hidden, keep-your-head-down-and-reproduce type of creatures — not exactly the spitting image of a Hero (or Heroine). We call them 'fit' because of how successfull they reproduce, not how well they do at athletic events.

Is natural selection a tautology?
So what are we to make of the phrase “survival of the fittest”? After all, if fitness just means “relative reproductive success”, then the phrase becomes “survival of the successful reproducers”; since evolutionary survival can also be understood as reproductive success, this simply becomes “reproductive success of the successful reproducers”, reducing the vaunted theory of evolution by natural selection to a circular argument — a tautology. Of course, evolution doesn’t actually reduce to a simple bit of circular reasoning. The flaw in this argument is the idea that “survival of the fittest” describes the mechanism of evolution. Fitness is just book-keeping; survival and differential reproduction result from natural selection, which actually is a driving mechanism in evolution. Organisms which are better suited to their environment will reproduce more and so increase the proportion of the population with their traits. Fitness is just a metric to keep track of this process. There is no circular argument because “fitness” is simply a measurement of survival (which is defined as reproductive success); it’s not the mechanism driving survival. Organisms (or genes or replicators) don’t survive because they are fit; rather, they are considered fit because they survived.

In my opinion, the gene-centered population biology view of evolution often fails to appreciate that fitness is just a metric. By treating changes in gene frequencies as the heart of evolution rather than as a readout of the process, this approach risks over-simplifying evolution in the interest of idealism. Fitness isn’t a property of a given gene or genotype; it’s always contextually dependent on the interaction between the gene of interest and a range of other factors. While I appreciate the oft-quoted importance of genes as fundamental units of replication, I think it’s a mistake to confuse the process of evolution with keeping count of replicators. This approach has certainly generated valuable insights, but such a strict reductionist approach can also generate unnecessary constraints. Realizing that fitness is simply a metric of the underlying process of natural selection does more than just liberate evolutionary biology from false accusations of circular reasoning; it also provides the intellectual space to discuss and consider things like macro-evolution and selection operating at different levels, subjects which seem to be an endless source of controversy and debate, and which touch on aspects of theoretical & experimental biology as well as philosophy.

The best of all possible worlds?
It's also important to realize that natural selection doesn't usually create perfectly adapted organisms. To succeed in evolutionary terms doesn't mean finding the best possible solution to a problem, but one that's 'good enough'; it's about having a reproductive edge on your competitors, even a very slight one. The solutions available in the course of evolution are also generally constrained by developmental programmes and evolutionary history, as well as trade-offs between different selective pressures. Far from the Panglossian picture of perfection, evolution creates a world of creatures just getting by the best they can, struggling to do a better job of reproducing than the rest of their species, even by means that don't match the common conception of being 'fit'.

[This post is adapted and expanded from a piece I wrote a few years ago for Inspiring Science.]