How it does a body good: The selective advantage of drinking milk depends where you drink it

I am a super-powered mutant. For a given value of "super-powered" and "mutant," anyway: I am an adult human who can drink milk. This is unusual among mammals, but as those (in retrospect, somewhat creepy) PSAs that used to run during my Saturday morning cartoons said, milk has a variety of nutritional benefits, if you can digest it. Which of these is behind the evolution of adult milk digestion in humans? According to a new paper in this week's PLoS ONE, the benefit you get from drinking milk depends on where you live.

Originally, every human on Earth was lactose intolerant, like most mammals. That is, they lost the ability to digest lactose, the major sugar in milk, when their bodies stopped producing the necessary enzyme lactase after weaning. Then, some populations of humans domesticated milk-producing animals, and this seems to have generated strong natural selection [PDF] for a form of the lactase gene that remains active in adults.

Photo by bensonkua.

In fact, milk-drinking populations in Europe and Africa have evolved "lactase persistence" independently [$-a]. This parallel evolution of a single trait motivates the new study by Gerbault et al. -- drinking milk might have different advantages for African pastoralists and Northern European farmers. Milk has two major dietary benefits:

• It's generally nutritious as a source of protein and calories, and
• Lactose can aid in calcium uptake in lieu of Vitamin D.

The main source of Vitamin D, for humans, is sun exposure -- the UVB rays in natural sunlight stimulate production of the vitamin. In Africa, close to the equator, it's easy to get plenty of direct sunlight; but in northern Europe, sunlight is less direct -- so it's harder to produce enough Vitamin D. (This is actually thought to be one reason for geographic differences in human skin color [$-a]: under lots of direct sunlight, dark skin is favored to minimize cancer risk; but under indirect sunlight, light skin is favored to allow more Vitamin D production.)

If the benefit of milk is calcium, not protein, then we would expect adult-active forms of the lactase-producing gene to be common in northern populations, and to decrease in frequency with decreasing latitude. This has been observed in a survey across Europe [$-a] -- but while the north-south pattern supports the calcium-benefit hypothesis, it is not conclusive evidence. This is because the same pattern could arise without any natural selection acting on the gene -- populations generally tend to be less genetically similar if they're farther away from each other, a phenomenon called isolation by distance, or IBD [PDF]. In fact, Gerbault et al. find that the north-south pattern of genetic similarity is replicated in genes that probably aren't under selection arising from life at high latitudes, suggesting that IBD, not selection, is responsible for the pattern in the lactase gene.

Photo by tricky.

For a more conclusive test, Gerbault et al. developed computer simulations of the evolution of early European communities. By simulating populations' evolution with different strengths of selection acting on the lactase gene, they could estimate how probable a particular value of selection was given the present-day frequency of lactase persistence in the real population -- but also take into account the population genetic forces that create IBD. They found that in southern Europe, no natural selection was necessary to explain the present frequency of lactase persistence -- but in the north, selection coefficients as high as 1.8% were needed. That is, in northern Europe, lactase persistence is so common that the simulations only produced the observed frequency when people who could not drink milk as adults had, on average, 1.8% fewer children than those who could.

In contrast to Europe, African communities don't show the same gradual transition from frequent to rare lactase persistence, so IBD is less likely to explain the observed patterns. To explain the frequency of lactase persistence in African populations, the authors compared it to the frequency of pastoralism -- and, finding a strong positive correlation, they concluded that lactase persistence evolved in Africa because it allowed shepherds to derive more nutrition from the animals they kept.

In short, widespread lactase persistence evolved in Africa because milk is a good source of protein; but it seems to have evolved in Europe because milk is a good source of bone-building calcium. Human populations on separate continents arrived at the same evolutionary solution, but for slightly different reasons.



Update, 18 October 2009: I've submitted this post to the NESCent competition for a travel award for the ScienceOnline 2010 conference in Durham, NC, January 14‐17th, 2010.

Update, 15 December 2009: Ye gads. I won!

References

Diamond, J. (2005). Evolutionary biology: Geography and skin colour Nature, 435 (7040), 283-4 DOI: 10.1038/435283a

Gerbault, P., Moret, C., Currat, M., & Sanchez-Mazas, A. (2009). Impact of selection and demography on the diffusion of lactase persistence PLoS ONE, 4 (7) DOI: 10.1371/journal.pone.0006369

Ingram, C., Mulcare, C., Itan, Y., Thomas, M., & Swallow, D. (2008). Lactose digestion and the evolutionary genetics of lactase persistence Human Genetics, 124 (6), 579-91 DOI: 10.1007/s00439-008-0593-6

Swallow, D. (2003). Genetics of lactase persistence and lactose intolerance Annual Review of Genetics, 37 (1), 197-219 DOI: 10.1146/annurev.genet.37.110801.143820

Tishkoff, S., Reed, F., Ranciaro, A., Voight, B., Babbitt, C., Silverman, J., Powell, K., Mortensen, H., Hirbo, J., Osman, M., Ibrahim, M., Omar, S., Lema, G., Nyambo, T., Ghori, J., Bumpstead, S., Pritchard, J., Wray, G., & Deloukas, P. (2006). Convergent adaptation of human lactase persistence in Africa and Europe Nature Genetics, 39 (1), 31-40 DOI: 10.1038/ng1946

Wright, S (1943). Isolation by distance Genetics, 28, 114-38 Other: http://www.genetics.org/cgi/reprint/28/2/114