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The placenta and the pace of life

The poor old placenta. It really doesn’t get much public attention. And yet it does a crucially important job - acting as the interface between the mother’s blood supply and that of her developing foetus.

Every molecule of glucose, oxygen and many other essential compounds consumed by the voracious offspring passes across the placenta - from the mother’s blood to the foetus'. And waste products pass back the other way to be detoxified and excreted by the mother’s organs.

Given these roles, one might be tempted to see the mammalian placenta as a discreet anatomic servant, working tirelessly, unseen and largely without thanks for the mutual good of mother and foetus. Only to be discarded or eaten after birth and spared no further thought.

And occasionally be venerated in YouTube videos with mystical soundtracks:

But such a view underrates one of the most interesting organs that ever evolved.

For one thing, the placenta varies more among mammal species than almost any other organ. And research published today in the Proceedings of the National Academy of Sciences of the USA provides some clarity on how this diversity evolved.

This research was led by Dr Michael Garratt, my colleague in the Sex Lab at UNSW, in collaboration with Jean-François Lemaître and Jean-Michel Gaillard (from France’s Université de Lyon and Laboratoire de Biométrie et Biologie Evolutive), and me.

Eutherian (the mammals other than marsupials, echidnas and platypus) placentas vary in a number of properties but we focussed on two of the most dramatically variable ones: “inter-digitation” and “invasiveness”.

The “inter-digitation” of a placenta describes the folding of the membranes between the mother’s and the foetuses blood. The more folded, the greater the surface area and thus the more opportunity for exchange of nutrients, dissolved gases and wastes to move between the foetus and the mother.

In some species the folds resemble fingers meshing with one another, but in others the folds are so much more dramatic, looking more like a complex tangle between two mops. These “labyrynthine” placentas have much greater surface areas than the less dramatic “villous” ones.

Highly “invasive” placentas burrow so intimately into the endometrium of the mother’s uterus, often remodelling the mother’s own arteries, that the fetal cells in the placenta bathe directly in the mother’s blood. Humans have this kind of hemochorial placenta, and other research suggests the first eutherians did too.

But other mammals have evolved less invasive placentas. In endotheliochorial placentas the thin wall of the maternal blood vessels remains, keeping the fetal tissues and maternal blood apart. And epitheliochorial placentas, the least invasive, have three layers of maternal tissue separating the foetus from maternal blood.

Conflict

Why has evolution not settled on a single, most efficient placental design?

To answer this question, we first need to set aside romantic notions of the placenta and materno-fetal relations. Because the placenta acts as both an interface for cooperation and a battleground for conflict.

A developing foetus always wants more than the mother wants to give it. And we know from studies of this battle in humans that the placenta sides decisively with the foetus.

The human placenta “invades” the mother’s endometrium, remodelling her arteries to weaken her ability to limit the flow of blood across the placenta membranes. The placenta, acting on behalf of the foetus, can release hormones directly into the mother’s blood vessels, raising her blood pressure and preventing her from reducing the levels of glucose in her blood.

The mother’s body resists too deep and profound an invasion - wanting the foetus to get as much nourishment as it needs, but not to be able to manipulate her circulation or blood sugar levels too completely.

Through most pregnancies mother and foetus push and pull in a gestational tug-of-war, but neither side prevails over the other. And yet we see the symptoms of this conflict in conditions such as gestational diabetes, pre-eclampsia and even pregnancy sickness.

The idea that pregnancy entails as much conflict as it does cooperation, and that the placenta plays for the foetus' team, numbers among the most important insights that evolutionary biology has granted to the medical sciences.

And so it is no surprise that theories of placental evolution focus squarely on conflict. Perhaps the different placenta types represent different outcomes of an evolutionary arms-race between mothers and foetuses?

That is an intriguing idea, but it does not entirely mesh with the fact that placentas have evolved several times to be come less invasive and less profoundly interdigitated.

Fast and slow

Studies of placenta-like structures in live-bearing fishes have suggested that these structures have evolved in response to changes in the number and timing of reproduction.

When resources are unpredictable or predation is high, then often parents are best served by having plenty of offspring and casting them to the four winds. Rabbits and mice, for example, are famous for their ability to proliferate rapidly.

They do so because they inhabit an uncertain world of predators and disease in which each embryo has a tiny chance of making it to adulthood and reproducing.

Whereas humans, elephants and other long-lived species have many chances to reproduce and have evolved to take the long view on reproduction. We nurture and teach our offspring and only have one every few years. We are down the slow end of something called the “fast-slow life history continuum”.

Mike, Jean-François and Jean-Michel combed the scientific literature to gather details of the placenta morphology of 155 species of mammal, from anteaters to zebras. They also searched for accounts of how many offspring they have, how long they live, how old they are when they start to reproduce and at what age they start to experience the symptoms of old age.

Interestingly, evolutionary changes in placental invasiveness and interdigitation seem to have occurred at about the same times - back in the long history of mammals - as the life-history either slowed down or speeded up.

Changes making the placenta area smaller are associated with a slow-down in life-history, including later onset of reproduction and longer life. The evolution of structures that enhance surface area have the opposite effect.

The change from highly invasive to less invasive placentas tends to be associated with a speeding up in the pace of life - producing lots of offspring at a young age, and dying young. So both interdigitation and invasiveness seem to change when there are big shifts in the pace-of-life. But a study like this one cannot provide definite answers about which change - if any - tends to come first.

Where does this leave the idea that placental evolution is shaped by mother-foetus conflict?

The telling detail is that accelerations in the pace of life accompanied transitions to less invasive placentation. Pace-of-life increases when life becomes uncertain and mothers do best by spreading their risks across many offspring (think rabbits, not elephants).

And when that happens, the interests of the mother and each of her sprogs come into greater conflict. Each foetus still benefits from getting as much investment from mama as possible. But mum does best by giving as little as possible to each foetus, thus allowing her to produce more.

As we put it in the paper:

We predict that selection for a faster pace of life intensifies parent–offspring conflict, and that the repeated evolution of less-invasive placental structures might have allowed mothers to wrest back control of gestation from the [foetus] and alter their relative allocation to offspring production across life.

Mothers seem to be prevailing, evolving the capacity to resist the offspring’s demands and manipulation.

Where does this leave humans?

We tend to produce only one offspring every few years, and invest heavily in each. The conflict between mother and foetus, and later between mother and child (at weaning time, for example), powerful as it is, is far less profound than it might be in faster-paced species.

We only see the potent ructions caused by mother-offspring conflict because the uterus allows the placenta to invade so deeply. And it does so because the evolutionary interests of the mother and the foetus are not all that different. At least when compared with other mammals.