More genetic variation within than between?

Research in human genetics has highlighted that there is more genetic variation within than between human groups, where those groups are defined in terms of linguistic, geographic, and cultural boundaries.

Statement 2. Guiding principles on using racial categories in human genetics (Soo-Jin Lee et al., 2008)

The above statement is part of an open letter to human geneticists, recently published in Genome Biology. The authors are a number of Stanford University scholars from the humanities, social sciences, life sciences, law and medicine.

Yes, the statement is true. It has been confirmed by a wide range of studies, the most well known being by Richard Lewontin (1972). At most human genes, there is far more variation within human populations than between them. Lewontin concluded that 85% of human genetic variation exists only between individuals and cannot be apportioned on a population basis. In this, he was repeating a conclusion that others had made before him, notably Frank Livingstone (1962), and that others still have since confirmed. Clearly, racial categories seem to be very hazy entities—so hazy, in fact, as to seem useless.

Or maybe not. It turns out that the same haziness exists between many species. When we compare pairs of species that are closely related but anatomically distinct, we often see more genetic variation within each species than between them, so much so, that we cannot reliably assign individuals to either by genetic criteria alone (see older post).

How come? When two populations diverge and eventually become separate species, they usually do so because they have adapted to different environments with different selection pressures. These selection pressures, however, do not act on the entire genome. In fact, they act only on a small set of genes—the ones that need to function differently in either environment.

We see the same thing with artificial selection. Kennel clubs maintain distinct dog breeds by insisting that dogs in any one breed meet various criteria. This distinctness disappears, however, when we look at their genomes.

… genetic and biochemical methods … have shown domestic dogs to be virtually identical in many respects to other members of the genus. … Greater mtDNA differences appeared within the single breeds of Doberman pinscher or poodle than between dogs and wolves. Eighteen breeds, which included dachshunds, dingoes, and Great Danes, shared a common haplotype and were no closer to wolves than poodles and bulldogs. These data make wolves resemble another breed of dog.

… there is less mtDNA difference between dogs, wolves, and coyotes than there is between the various ethnic groups of human beings, which are recognized as a single species. (Coppinger & Schneider, 1995)

Artificial selection uses a smaller set of criteria than does natural selection. Nonetheless, both forms of selection act on only a small fraction of the genome, partly because most genes are of marginal selective value and partly because many genes can function identically in a wide variety of species.

Of course, even at these other genes two populations may start to show diverging patterns of variation once they have become reproductive isolated species. But this is a long process that occurs through each of them slowly and separately accumulating its own mutations at genes of low selective value. This is not the case with our species. We began to spread out of Africa only 50,000 or so years ago.

References

Coppinger, R. and R. Schneider (1995). Evolution of working dogs. In J. Serpell (ed.), The Domestic Dog: Its Evolution, Behaviour and Interactions with People. Cambridge: Cambridge University Press, pp. 21-47.

Soo-Jin Lee, S., Mountain, J., Koenig, B., Altman, R., Brown, M., Camarillo, A., Cavalli-Sforza, L., Cho, M., Eberhardt, J., Feldman, M., Ford, R.,Greely, H., King, R., Markus, H., Satz, D., Snipp, M., Steele, C., and Underhill, P. (2008). The ethics of characterizing difference: guiding principles on using racial categories in human genetics. Genome Biology, 9, 404 doi:10.1186/gb-2008-9-7-404

Lewontin, R.C. (1972). The apportionment of human diversity. Evolutionary Biology, 6,
381-398.

Livingstone, F.B. (1962). On the non-existence of human races. Current Anthropology, 3, 279-281.