Selection and lactase persistence

I received a letter about lactase persistence that motivated me to a fairly long reply; I thought I would share the question and answer:

I read with interest your article in the current Scientific American (Still Evolving). I do have one serious puzzle: While not a biologist (or an anthropologist), my understanding of the logic of Darwinian selection is that mutations are random and that they only have a chance of sticking around if they give the species some benefit for survival in the context of the current environment; and that survival translates primarily into the capacity to produce enough healthy offspring to continue (and maybe sometimes produce more offspring than before).
Now, when it comes to protection, even moderate, against malaria, this makes sense. But I do not see how lactose tolerance would fall into that category. My impression is that humans who are lactose intolerant and drink milk do not appear to have a life-threatening reaction. They may be miserable at the extreme, but they live. Certainly, being lactose tolerant in a population that raised dairy cows (goats, etc.) would improve one’s quality of life, but I need some help in understanding how this would benefit our species survival ability.

This is a great question; I had a very prominent geneticist ask me the same thing some years ago.

It can be difficult for people in today’s industrialized societies to perceive the depths of the nutritional challenges faced by most people throughout history – sadly even though the same nutritional challenges are still faced many people living today. Nutritional shortfalls impede reproduction in many ways. Women on calorie-restricted diets have lower fertility, and take longer after the birth of a child to conceive again. Adolescent girls with restricted caloric intake take longer to reach sexual maturity.

The lactose in milk amounts to approximately a third of its caloric content. That means that a person with lactase persistence can get up to 50% additional energy from milk. Milk can be processed by microbes to reduce its lactase content – many yogurts and cheeses can be consumed by adults who do not have a persistence of lactase. But these methods are time-consuming and reduce the amount of energy available from a given volume of milk.

In a milk-consuming population, otherwise nutritionally limited, lactase persistent women would have reproduced earlier and have had larger families. Our best estimate is that this advantage was on the order of 10% during the last few thousand years in northern Europe. This kind of advantage could accure by lactase-persistent women starting their reproductive lives around 2 years earlier, or spacing their children around three months closer together. That kind of change in birth spacing or maturation need not be genetic itself; it can emerge simply as a result of better nutrition.

Lactase persistence worked especially well in societies where it was part of a system. Milk is a very efficient use of domesticated animals; milking animals yields much more energy over the long run than raising them for meat. Some ancient populations relied extensively on the milk produced by their herds; this was a much more important component of the diet in areas that were too arid or too cold for the earliest domesticated grain crops. Those areas, like northern Europe, Arabia, and the Sahel, are where different lactase persistence mutations most took hold.

Once such a system got started, people who carried the original, non-digesting lactase allele would have been even worse off. Consuming moderate quantities of milk can lead to digestive distress in people who do not produce lactase. The resulting diarrhea reduces energy intake even more and can cause worse health problems. That side-effect of milk drinking might initially have deterred people from adopting milk in their diet. But for any group where milk drinking had been established already, the bad consequences of lactose intolerance would increase the selective pressure toward lactase persistence.