Edge: GENOMIC IMPRINTING


In a 1974 paper on parent-offspring conflict Trivers pointed out that there was often an implicit assumption that what was good for a parent was also good for the offspring. In terms of genetic transmission, it would seem that offspring are parents' stake in the future, so parents should be doing their best for them. What Trivers argued, however, was that parents would be selected to maximize their total number of surviving offspring—which may be quite different from maximizing the survival of any particular individual offspring. He suggested that there is a tradeoff between producing lots of offspring and investing relatively little in them versus producing a small number of offspring and investing a lot in each. He thought that over evolutionary time offspring would begin to compete with their siblings for available resources. And in turn, sibling rivalry would result in conflict between offspring and parents, since over time offspring would be selected to try to get more than their fair share of resources from their parents—more than the parents were selected to supply—whereas parents would be selected to spread their resources more evenly over a larger number of offspring. Trivers's theory was that this could lead to evolutionary conflicts.

I was asked to talk at the National Institute of Health in a workshop on imprinting and human disease. My goal was to suggest how evolutionary theory would provide new insights into human disease. An obvious case was in human pregnancy, where Trivers's theory of parent-offspring conflict could help to understand why pregnancy is so often associated with medical complications. Since then, looking at maternal fetal interactions has been another area in my research.

Trivers's theory has a lot to say about why pregnancy doesn't work particularly well. If we look at most of the products of natural selection, like the hand, the liver, the heart, or the kidney, these are wonderful bits of engineering that function very well for 60 or 70 years. But why are there so many problems in pregnancy? Pregnancy is absolutely essential to reproduction, so you might expect that this would be one part of our human physiology that had been perfected by natural selection. But there is an important evolutionary difference between the function of the heart and what's going on in pregnancy. When we look at the selective forces acting on the function of the heart, there's no evolutionary conflict. All of the genes involved in the development and function of the heart belong to the same genetic individual and, in a sense, have the same genetic interest: the maximization of the number of offspring of that individual. In the absence of conflict we've got a simple optimization problem, and you get an optimal solution.

But in the relationship between mother and fetus—because of the parent-offspring conflict that Trivers pointed out—we've now got conflicting forces. The offspring is being selected to take a little bit extra from the mother, and the mother is selected to resist some of the offspring's demands. Those selective forces tend to act at cross purposes and cancel each other out.

One very important problem during pregnancy is the communication of information between mother and offspring. In communication within the body there's no conflict, since selection causes cells to send messages as cheaply and as efficiently as possible. But when you're looking at the exchange of messages between mother and fetus, there's a problem of credibility, since their interests are not identical. In some situations, there's an evolutionary incentive to send misleading messages, and corresponding selection for receivers to distrust messages being received.

One thing that's happening during pregnancy is that there's a lack of the usual feedback controls, checks and balances. I read grant applications for scientists proposing to study maternal-fetal relations, and they tend to portray it in very rosy terms, as an almost loving exchange of messages between mother and fetus. But in pregnancy an embryo implants itself in the abdominal cavity or in the fallopian tube—in a completely inappropriate position in the body—and develops autonomously in the absence of any appropriate maternal messages. I believe there's actually very little communication going on between the mother and the fetus during the pregnancy. Rather, you're looking at various fetal attempts to manipulate maternal physiology and metabolism for fetal benefits.

 

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