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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.

Join the conversation

35 Comments sorted by

  1. Dale Bloom

    Analyst

    Rather offensive calling children “sprogs”, but I think that is the nature of evolutionary biology.

    In all, probably another article designed to mention the word “mother” without mentioning the word “father”, and there does seem to be plenty of such articles.

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    1. Dale Bloom

      Analyst

      In reply to Rob Brooks

      Still not willing to mention the word "father"?

      Paternal is close, but with some effort, the word "father" may be written at some time.

      Much easier to call children "sprogs"

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    2. Andy Saunders

      Consultant

      In reply to Rob Brooks

      I score that reply as the most effective I've ever seen on The Conversation, Rob.

      I've always been intrigued (although ill-informed) on the parallel evolution of placental gestation in sharks as compared to mammals. I suppose it is the more primitive sharks (Port Jackson etc) that are egg-laying, and the more advanced that use live-birth. Do live-bearing sharks have a similar variation in inter-digitation and invasiveness as do mammals?

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  2. Pat Moore

    gardener

    Thanks for another fascinating subject of investigaion Rob.

    This occulted "uterine cake" has been vastly under investigated for such an interesting and mysterious entity. It is so much like a blue jellyfish. As the blood channeling interface between mother and the fish-like embryo in a liquid environment it has an aspect of a subaquatic marine plant, the pregnant uterus like a safe harbour and the baby floating like a deep sea diver or an astronaut in space via the life giving umbilical cord…

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  3. Bao-Luo Zhidao

    logged in via Facebook

    But it's not about the size of the placenta, it's how efficient it is! I can't imagine how many foetus's you have offended with the article - I can hear their collective kicks sound like pitter-pattering rain falling on soft grass outside the local OBGYN's. ;)

    As someone with a year 10 biology background a bit of wikipedia reading on your area of expertise, I had never come across the concept (or had it occurred to me) that the underlying life forces between a developing offspring (and the placenta acting on behalf of it) and its mother are actually separate and different. Can such an interaction happen in any other way between two life forces within the same organism? The more I think about it, the more validity it gives to the idea to the pro-choice argument that a foetus is a parasite.

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  4. George Harley

    Retired Dogsbody

    In an evolutionary turf war between between foetus and mother, surely there will only be one winner? I can't see much future for aggressive foetuses that remove less resistant mothers from the gene pool.

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    1. Rob Brooks
      Rob Brooks is a Friend of The Conversation.

      Professor of Evolutionary Ecology; Director, Evolution & Ecology Research Centre at UNSW Australia

      In reply to George Harley

      Correct up to a point. Winning doesn't have to involve killing the other party.
      The mother has an interest in the foetus being born viable and strong, and the foetus has an interest in having a mother who can and will care for it after birth. The negotiation is over the middle ground between the foetus being basically viable (leaving the mother resources to have more kids) and being as big and strong as it possibly can be (leaving the mother worse off and less able to have more kids).

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    2. George Harley

      Retired Dogsbody

      In reply to Rob Brooks

      Thanks Rob, If I had said that aggressive foetuses, over evolutionary time frames, will eventually reduce the propensity for mothers to produce aggressive foetuses, is that valid? Along the lines of "Don't sh*t in your own nest?" if you will excuse the less than scholarly proverb.

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    3. Rob Brooks
      Rob Brooks is a Friend of The Conversation.

      Professor of Evolutionary Ecology; Director, Evolution & Ecology Research Centre at UNSW Australia

      In reply to George Harley

      Within limits, George. Mothers adapt to limit the damage caused by over-aggressive foetuses, but the foetus should still evolve to take what it can from the mother. As Jenny Graves points out below, this is really a battle between the mother's genes (in the foetus and placenta) and the father's genes (also in the foetus and placenta). In an interesting way the foetus is at war with itself.

      I promise to write more about this fascinating and most basic of all evolutionary conflicts.

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    4. George Harley

      Retired Dogsbody

      In reply to Rob Brooks

      Thanks Rob (and others) I too look forward to further articles on this fascinating debate. Almost a Stephen J Gould Did Pot v You Are wearing The Wrong Genes. Regards.

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  5. Tim Kottek

    logged in via Facebook

    Hi - to make use "discarded or eaten after birth" more comprehensive consider Bali, there the placenta is buried in the village to affirm a tie to the community.

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    1. George Harley

      Retired Dogsbody

      In reply to Tim Kottek

      And if a USA community wished to wear a placenta on their heads to divert the waves from the government satellite probes, should we "consider" them as well?

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    2. George Harley

      Retired Dogsbody

      In reply to Suzy Gneist

      The cultural/spiritual/symbolic significance that some humans (usually female) attach to a waste product of an evolutionary process that just happened to work more efficiently than others is worthy of study. Right after we crack those homeopathy and chiropractic riddles.

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    3. Suzy Gneist
      Suzy Gneist is a Friend of The Conversation.

      Multi-tasker at Graphic Design & Montville Coffee

      In reply to George Harley

      I was under the impression the comment referred to different cultural understandings. You seem to imply a gender view difference as well as that a 'usually female' perspective (a group which includes half the population) is somehow 'unscientific' and therefore inferior, is this correct?

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  6. Chris Booker

    Research scientist

    Interesting article Rob,

    I don’t research the placenta, but became particularly intrigued about the co-opting of a viral gene in placenta function after reading ‘Virolution’ by Frank Ryan at about the same time as this paper was published by Cornelis et al:
    Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora.
    Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Véron G, Mulot B, Dupressoir A, Heidmann T…

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    1. Rob Brooks
      Rob Brooks is a Friend of The Conversation.

      Professor of Evolutionary Ecology; Director, Evolution & Ecology Research Centre at UNSW Australia

      In reply to Chris Booker

      Thanks Chis,
      The idea and the Cornelis paper sound fascinating. looking forward to reading their paper and considering the implications. The idea that a transition could come from recurrent endogenization of a protein- as you explain it - need not be problematic for the associations we document. We genuinely don't know the direction of causation either, though if I had to bet I would say life-history changes might drive placental changes. Could easily be true that the incorporation of the protein enabled the life-history changes.
      Thanks again,
      Rob

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  7. David Tuck

    Scientist

    Very unique and interesting article Rob. I wanted to add something about the idea of an evolutionary arms race between mother and offspring but you seem to have mostly answered it in your last paragraph. What I was thinking is that the 'predator' in the evolutionary arms race scenario effectively stops the 'prey' organism from passing on its genes, whereas in the one described the offspring is the embodiment of those genes. Humans must have found a good balance in the sharing of resources between mother's and foetus' given our position in the food chain. Also, great to see you responding to posts, I'd love to see more of that at The Conversation.

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  8. Rachana Shivam

    logged in via Facebook

    It heartens me to have somebody pay such attention to the amazing placenta. I have been discovering and exploring its importance and incredible impact for the past 30 years. It is my ever developing understanding that our relationship to this organ of high intelligence lays the foundation to our sense of self and other and that it is this primary relationship that eventually translates into our relationship with others. I think that much of what we consider is our psychology is actually based on…

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    1. emily vicendese

      undergrad

      In reply to Rachana Shivam

      "...this organ of high intelligence"? Also, are you saying that because some ancient cultures revered the placenta that that is evidence of its "power"?

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  9. Jenny Graves

    Distinguished Professor of Genetics at La Trobe University

    Really interesting article. Only one thing missing – the source of conflict with the mother is not just the foetus, but its father. Or more properly, the father’s genes and the interests of the father’s genome to propagate itself, even at the expense of the mother.

    This make sense of the strange class of genes that we call “imprinted.” These genes are silenced when they come from either the mother (“maternally imprinted") or the father (”paternally imprinted”). Maternally silenced genes, active only when inherited from the father, tend to be genes that favour growth of the foetus at the expense of the mother. Paternally silenced genes, active only when inherited from the mother, tend to be genes that limit foetal growth.

    So the placenta is really the battleground for the wars of the sexes.

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    1. Rob Brooks
      Rob Brooks is a Friend of The Conversation.

      Professor of Evolutionary Ecology; Director, Evolution & Ecology Research Centre at UNSW Australia

      In reply to Suzy Gneist

      You got there first, Suzy.

      Dale may wish to know that Professor Graves is an evolutionary biologist. Arguably Australia's most distinguished one at that. And yet she had the audacity to mention father four times in one short comment!

      This article was too short to touch on the genetic conflicts Jenny writes about here, but when I did write about these conflicts last year - on the occasion of HRH The Duschess of Cambridge's hospitalisation - Dale didn't seem to appreciate what I was saying either.

      He's so hard to please!

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    2. Dale Bloom

      Analyst

      In reply to Jenny Graves

      So the father is battling the mother so that he can continue his genes?

      Seems like something out of feminism, and such a theory doesn’t account for why 50% of babies are born female.

      Women are quite easy to battle and really can't fight much at all, and if the theory was correct, there should be only a few females born for breeding purposes only.

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    3. Dale Bloom

      Analyst

      In reply to Rob Brooks

      By now, there must have been 1000’s of theories developed by evolutionary biologists, often based on the worst research, and I don’t think one of those theories has ever been proven.

      It seems to be a system of believe an evolutionary biologists, or get called names.

      BTW. How is your “sprog”.

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    4. Tim Kottek

      logged in via Facebook

      In reply to Dale Bloom

      Hi dale
      Help me find a proven theory - post Popper!

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    5. Dale Bloom

      Analyst

      In reply to Tim Kottek

      1 + 1 = 2
      1 + 2 = 3
      1 + 3 = 4
      etc.

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    6. Tim Kottek

      logged in via Facebook

      In reply to Dale Bloom

      Sad to see a comment from someone who doesn't know what Popper wrote about or perhaps lacks the understanding of it. There is a huge difference between an axiomatic logical system and a scientific theory. By the way in Binary 1 + 1 = 10

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    7. Dale Bloom

      Analyst

      In reply to Tim Kottek

      If a theory is any good, it can become a scientific law.

      Most scientific laws (if not all) can be proven mathematically.

      Evolutionary biology is now suffocating under the sheer weight and number of its own theories that are never proven.

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    8. Tim Kottek

      logged in via Facebook

      In reply to Dale Bloom

      Nice pre Popper response!
      Newton's so called laws of motion were and still are a useful theory in that they are open to invalidation - as Einstein's Theory (not law) of relativity adequately demonstrated the limits of. There isn't a provable theory post Popper but clearly you don't get that so I'll no longer bother responding

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    9. Dale Bloom

      Analyst

      In reply to Tim Kottek

      Life suddenly evolved from chemicals, (according to evolutionary biologists) so study up on the laws of chemistry, and then get back to me.

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  10. Deirdre Whitford

    Un-Worker

    It's gratifying to find so many comments (including prose poems and perspectives ranging from philosophy to comparativle anthropology) inspired by an article about brand new scientific knowledge.
    I gratefully anticipate that this compelling research will continue to fuel a frenzy of interdisciplinary speculation wherever it goes.
    (Disclosure of interest: non-mother, ex-foetus, humanities-leaning.)

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