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Thursday, June 27, 2002

NATURAL SELECTIONS

A mammalian conflict

Male genes influence fetal food supply


What do a pie invented almost 2,000 years ago by the Roman statesman Cato the Elder and the organ most intimately connecting a mother and her unborn child have in common? They are both called placenta (and in some places, both are still eaten). "Placenta" comes from the Greek word plakous, meaning flat cake.

Mice and various other mammals often eat their placenta after giving birth. Human placenta apparently smells like liver and tastes like chicken, and is reportedly great raw or in a stew with garlic and red peppers. Mouthwatering though that may be, what really gives food for thought is a paper in Nature this week in which scientists describe work on genes active in the placenta.

We have two copies of each gene, one from our mother and one from our father. Both copies are used as we grow, and their effects are blended. The same is true for the genes at work in the placenta, but for some of them, so-called imprinted genes, only one copy of the gene is active; the other copy is inactive or "silent" -- it might as well not be there. Sometimes the paternal copy of the gene is switched on, sometimes the maternal copy. And when the mother's and father's genes both want a say, there can sometimes be a conflict of interest.

The food a fetus gets from the placenta determines its birth weight. Babies with low birth weights (less than 2.5 kg) have an increased chance of physical or mental development problems and a greater risk of heart disease, type-2 diabetes and certain respiratory problems in later life.

So the placenta is there to supply the developing baby with nutrients and oxygen and remove waste and carbon dioxide. How could there be cause for conflict in that?

The conflict arises when you look at the genes that control how the fetus is fed.

The size of the placenta is influenced by the amount of a hormone called insulin-like growth factor II in the blood. The gene for this growth factor, written as Igf2, is turned on in the fetus and in the placenta. It is especially active in one key area of the placenta -- the labyrinthine trophoblast -- where maternal and fetal blood mix, and where nutrients are exchanged. The maternal copy of Igf2, it turns out, is "silent" and only the paternal copy is used. Geneticists say that Igf2 is "paternally imprinted."

Why should the father have control of such an intimate part of the mother-fetus interface? It doesn't make sense until you think about conflict.

Both the male and the female "want," in an evolutionary sense, to produce a healthy baby. But few mammals are monogamous, so it's unlikely that any future babies a given female produces will be fathered by the same male. It is therefore in the father's best interest that the mother produces a big fat baby, all the better to increase the chances of getting the father's genes into the next generation. So the father's Igf2 gene stimulates the placenta -- and so the fetus -- to grow.

From the mother's point of view, however, it's silly to invest so much in the present fetus that she doesn't have enough energy left for future ones. So she deploys her own set of imprinted genes to combat the effect of the male Igf2 gene and keep the growth of the placenta in check. Thus, there is conflict between males and females (a kind of genetic tug of war), even before the baby is born.

The conflict theory is supported by the work of Miguel Constancia at the Laboratory of Developmental Genetics and Imprinting, part of The Babraham Institute in Cambridge. Constancia and colleagues tested the theory by using gene manipulation to knock out the Igf2 gene from the placentas of mice. (Mice have placentas similar to those of humans, and in both species Igf2 is active in the placenta. This allows scientists to use mice as models and conclude that a similar thing occurs in humans.)

"Our work represents some of the most clear-cut experimental data obtained so far in support of the conflict hypothesis, since it directly addresses the question of the extraction of nutrients from the mother," said Constancia in an e-mail interview.

Pregnant mice without Igf2 had a smaller placenta, reduced nutrient transport across the placenta and fetuses smaller than normal.

"Imprinting seems to be closely linked to the evolution of placentation in mammals," said Constancia. "Imprinting appears to be absent in non-mammalian vertebrates, prompting the hypothesis that it arose after the emergence of mammals but prior to the divergence of placental and marsupial subclasses."

Birds lay eggs -- which contain a fixed amount of nutrients per embryo, but the mammalian embryo is continually "on-line," maintaining a connection to its mother. "Therefore it can influence its own growth [via its paternal genes acting in the placenta] at the expense of maternal resources," said Constancia.

In other words, the mammalian organ most intimately concerned with nurturing embryos comes with a potential conflict of interest built in. Now there's something to chew on.

For tasty placenta recipes, see mothers35plus.co.uk/plac_rec.htm For more science news from Nature, see www.nature.com You can e-mail Rowan Hooper at rowan@japantimes.co.jp


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