18 Neutral or Adaptive Evolution in Humans: What Drives Evolution of Our Traits?

18.1 Background

Understanding the role of natural selection and genetic drift in human traits requires a look at several key aspects:

• Heritable variation: a trait can only evolve (by drift or by selection) if individuals differ in it and some of those differences are inherited.
• Selection vs drift: selection acts when variation in a trait is correlated with variation in survival or reproduction. Drift is chance change in allele frequencies, and it acts in every finite population.
• Role of environment: the environment can change the strength, and even the direction, of selection on a trait.

First ask: is the variation heritable? Some traits vary a lot but are hardly inherited at all. For example, the fine texture of the iris and the detailed ridge patterns (minutiae) of fingerprints differ even between identical twins: they are mostly the result of chance events during development. Variation like this cannot evolve by drift or by selection, because it is not passed on.

Neutral and adaptive evolution are two ends of a continuum. In the lecture on genetic drift we defined neutral evolution. Suppose a trait varies, individuals vary in reproductive success, and the trait is inherited, but the trait is not (or only very weakly) correlated with reproductive success. The trait still evolves, but by chance: this is neutral evolution, caused by genetic drift. When the correlation between the trait and reproductive success is strong, we get adaptive evolution, caused by natural selection. Most traits lie somewhere in between.

Population size also decides where a trait sits on this continuum. Drift acts on the alleles that affect a trait, and its strength per generation is about \(1/(2N_e)\), where \(N_e\) is the effective population size. Selection on those alleles is effective only when the selective advantage, \(s\), is clearly larger than roughly \(1/(2N_e)\). So weak selection that is effective in a large population can be swamped by drift in a small one. Whether a trait evolves “neutrally” therefore depends on population size as well as on the environment.

When selection is moderate or strong, a trait tends to be held close to some optimal value (stabilising selection) or to change in a consistent direction (directional selection): adaptive evolution. When selection is weak or absent, the alleles that affect the trait change in frequency at random, and the trait drifts: neutral evolution. Both require heritable variation to begin with: if there is little heritable variation, the trait will not respond much even if selection is strong.

Finally, the strength of selection depends on the environment. A trait may be important in some environments but not others, and may be selected for in one environment but against in another. For example, the skin pigment melanin protects against intense ultraviolet (UV) radiation, including UV damage to the vitamin folate, so darker skin is favoured where UV is intense. Where UV is weak, lighter skin allows more vitamin D to be made in the skin (Jablonski & Chaplin 2010, PNAS). Ancient DNA shows that some of the main light-skin alleles became common in Europe only within roughly the last 8,000 years (Mathieson et al. 2015, Nature). Exactly which selective pressures mattered most, and when, is still debated.

The objective of this exercise is to develop an intuitive understanding of the effect of selection and genetic drift on traits.

Figure 18.1: Two present-day human environments: Hadza men returning from a hunt in the dry savanna woodland of northern Tanzania (left) and Nyhavn in Copenhagen (right). Both photographs show people living today: all living human populations are equally evolved, and all are still subject to natural selection. How would selection on each trait differ between these environments? Photos: Andreas Lederer (left) and Jorge Láscar (right), both CC BY 2.0, via Wikimedia Commons.

Learning outcomes:

• Decide whether a trait can evolve at all, by asking whether its variation is heritable.
• Place traits on the continuum from neutral evolution (genetic drift) to adaptive evolution (natural selection), and justify each placement with evidence or reasoning.
• Explain how the environment (foraging societies vs modern industrialised countries such as Denmark) and population size change the strength of selection on a trait.
• Predict which differences between human populations gene flow would erase, and which local selection could maintain.
• Use correct scientific terminology when arguing for your categorisation in a group.

18.2 Key idea

Traits like resistance to infectious disease are likely to face strong selection in environments where the disease is common. Heritable variation with little or no effect on survival or reproduction (for example, many DNA differences at synonymous sites, which do not change the protein) is more likely to change by drift.

18.3 Your task (30 minutes)

You are given a short list of eight human traits (below). They were chosen to cover the whole range, from traits that are probably drifting, through traits with little heritable variation, to traits under strong selection in some environments but not others. In small groups:

1. Write the traits on PostIt notes.
2. Discuss and categorise the traits based on the strength of natural selection in foraging (hunter-gatherer) societies, like those in which most of human evolution took place (10 minutes).
3. Repeat the exercise for modern industrialised societies like Denmark (10 minutes). In Denmark today, most people survive to adulthood, so ask how each trait might affect the number of children people have: selection still acts, but now mainly through differences in reproduction rather than survival.
4. Gene flow between populations (10 minutes). Human populations exchange migrants, and gene flow pulls their allele frequencies together. In the lecture on migration and gene flow we saw that very few migrants (about one per generation) are enough to stop drift making populations very different, but that local selection can keep populations different if it is strong compared with the migration rate (\(s\) larger than \(m\)). For each trait, ask:
   • Does the trait differ between human populations living in different environments?
   • Would gene flow erase those differences (as expected for neutral traits), or could local selection hold them apart? Good places to start: skin pigmentation and UV; lactase persistence (digesting milk sugar as an adult), which became common in populations that keep milk-producing animals; and the sickle-cell allele (HbS), which protects carriers against malaria.
   • Remember that most human genetic variation is found within populations rather than between them.

For steps 2 and 3, order the traits from those likely influenced by GENETIC DRIFT to those evolving through ADAPTIVE EVOLUTION via NATURAL SELECTION. For each trait, start with the question “is the variation heritable?”.

18.3.1 The traits

Trait	Description
Metabolic efficiency	How effectively your body converts food into energy.
Eyesight acuity	Sharpness of vision.
Height	Standing height.
Birth canal (pelvic) shape	The shape of the bony opening through which a baby is born.
Resistance to bubonic plague	Immunity or resilience against bubonic plague.
Eye colour	The colour of the iris (brown, green, blue and so on).
Earwax type	Wet or dry earwax, set by a single DNA change; dry earwax is common in East Asia and rare in Europe and Africa.
Face symmetry	The balance and proportionality of facial features.

18.4 Discussion (10 minutes)

After the exercise, discuss as a class:

• Were there any traits that were categorised differently between the two types of societies? Why?
• Which traits did you decide had little or no heritable variation, and so could not evolve by drift or by selection?
• Which differences between human populations would gene flow erase, and which are maintained by local selection?
• Did the exercise challenge any preconceived notions you had about trait evolution?
• Can you think of any other traits that would be interesting to add to this exercise?

18.5 Takeaways

• A trait can only evolve if its variation is heritable.
• Neutral and adaptive evolution are two ends of a continuum: where a trait sits depends on how strongly it affects survival or reproduction, and on population size (\(s\) compared with \(1/(2N_e)\)).
• Selection strength depends on environment and context, not just on the trait itself, and different environments can reverse which traits are favoured.
• Humans are still evolving: in industrialised societies, selection acts mainly through differences in the number of children.
• Gene flow erases neutral differences between populations, but local selection can maintain differences in traits such as skin pigmentation.