Thursday, March 26, 2015

The 'obstetric dilemma' hypothesis unraveled

Right now I'm giving this talk at the annual meetings of the American Association of Physical Anthropologists. Here's the link to Session 15. Costly and Cute: How Helpless Newborns Made Us Human, where you'll see the participants, their talk titles and abstracts. This symposium evolved out of a seminar at the School for Advanced Research back in the summer of 2014 when I was very pregnant and on the cusp of facing my own obstetric dilemma.

Let’s see how far we can unravel this epic hypothesis in 15 minutes or less. To start, here are the two most important seeds I hope to plant today in hopes that you’ll read up on these things further:  One. The obstetric dilemma is a hypothesis, not a fact. And… Two. The obstetric dilemma is an elegant idea, and would be an extraordinary example of human exceptionalism if true.  But it bears the burden of proof. So what is the obstetric dilemma hypothesis? In a nutshell…

We use it to explain at least these two observations, and often there are more: First, childbirth is difficult and risky. And, second, humans are born with only about 30% of our adult brain size, but for chimps it’s 40%.  Why? The “obstetric dilemma” hypothesis. Constrained by bipedalism, the human pelvis constrains gestation length and fetal brain and body growth, while making childbirth difficult and dangerous.  Which, put differently, is the hypothesis that the unique human pelvis uniquely impacts human parturition and life history. Here’s a good example of how the obstetric dilemma is often presented as a common fact, even in a book that aims to have us rethink old assumptions:

“You can’t give birth to large-brained infants and also walk on two legs trouble-free, no matter how hard you try.” Alright so, locomotion’s running the show, but does it deserve to? That is, does selection for bipedalism limit the birth canal from widening and relieving a laboring mother’s difficulty?

As of now, even taking a new dynamic approach over the old static one, like Anna Warrener and her colleagues do, there is no strong history of support for the idea that wide or women’s hips are costlier or less efficient than narrow or male’s hips. This is, at present, the best approach to the question of whether women are presently at an upper limit in pelvic dimensions that selection for bipedalism will allow. And although it does not test the obstetric dilemma directly, it demonstrates that our perspective on sexual dimorphism has been biased toward seeing female bodies as compromised compared to a male ideal. 

Relatedly, recent additions to the hominin fossil record have lifted us from the temptation to see a progressive march through time to arrive at our bipedal perfection. There are numerous reasons the hominin pelvis evolved over the last several million years, making it unlikely that our present anatomy is what is “required” for bipedalism as is so often phrased. We can only assume that the few pelvic specimens in the hominin fossil record are testament to the variable morphology that has worked both for bipedalism as well as childbirth over the last several million years. Still, if bipedalism isn’t limiting the birth canal and causing childbirth difficulty, what is? Or, asked another way, there is an explanation for why chimpanzees have it so much easier than we do. So what is it?

The answer could still be that selection for bipedalism is constraining the pelvis and it has not yet been demonstrated.  The biomechanics of pregnancy may adaptively constrain pelvic dimensions, along the lines of what Katherine Whitcome and colleagues described for the spine. Further, limitations to tissue strength and other such properties of soft tissues of the pelvic floor may constrain pelvic dimensions, especially during pregnancy or as a result of it. But it must be noted that pelvic prolapse occurs in cows and sheep, not just bipeds.   Other significant contributors to childbirth difficulty include, but are not limited to: position of the laboring woman, position of the fetus and the umbilical cord, function of the placenta, uterus and cervix, muscular and bodily weakness, slow labor progression, multiple fetuses, preeclampsia, gestational diabetes, and age at first birth, young or old. At present, our impressions of hellish human childbirth are biased to a degree by Hollywood as well as the medical industry. So we may have to place some heavy blame on culture for our having it so much harder than chimpanzees. However, the rise in c-section rates from 5% to around 30% over the last several decades is not entirely due to unnecaesareans, as there has been a concurrent secular increase in neonatal size in hospitals as well. And that recent trend may be best explained by work being done by Jonathan Wells and his colleagues…

Although the tight fit between fetus and mother’s pelvis may have occurred millions of years prior, agriculture has had a remarkable and perhaps the most dramatic effect. Agriculture’s influence on diet and overall health has affected both the development of the female pelvis and the growth of her fetus during gestation. Undernourished mothers can birth relatively large babies due to adaptive responses to protect fetal growth during pregnancy, and regardless of maternal condition, larger babies are associated with longer labors and higher incidences of medical interventions. It is highly likely that there was never more childbirth difficulty than there is now and in recent history.  Plasticity has been both a blessing and a curse. Okay, so if childbirth difficulty may be new and is due to a complex vortex of proximate and ultimate explanations, not due solely or largely to locomotor selection on birth canal size, then what about our being born with only 30% of our adult brain size? 

Could the obstetric dilemma explain our relative immaturity at birth?  Which is to say, does the human pelvis uniquely influence gestation length and fetal growth? 

Or are we born early to experience a rich period of stimulation and learning, crucial to the development of human cognitive and neuromuscular function as Portmann hypothesized? According to the extra-uterine spring hypothesis, the pelvis does not limit gestation and fetal growth, the benefits to life outside mother do. These two hypotheses for gestation length and fetal development have humans born early or underdeveloped. A third does not. 

When the energetic and metabolic costs of pregnancy and lactation are considered, gestation ends and the birth process is initiated when pregnancy reaches a critical point at which the mother can no longer support her growing fetus. Fetal energy demands (black circles) increase exponentially during gestation.  Maternal energy expenditure (grey squares) rises during the first two trimesters but reaches a metabolic ceiling in the third, as total energy requirements approach 2.0x basal metabolic rate.  Projected fetal energy requirements for growth beyond 9 months (dark, dashed line) quickly exceed the maximum sustainable metabolic rates for human mothers (horizontal, dashed line).  After parturition, infant energy demands increase more slowly, and maternal energy requirements while lactating do not exceed the maximum sustainable metabolic rates. The hormonal cascade that is involved in triggering human birth has been described by Peter Ellison’s metabolic crossover hypothesis. We suggested that although the data are far better for humans, this broad and more ultimate hypothesis that we called EGG likely applies to other species since, among placental mammals, maternal body size (a proxy for metabolism) is a good predictor of gestation length, fetal mass, and fetal brain mass as the work of Bob Martin and others work has demonstrated. Still, this doesn’t answer the question as to whether humans are born early or underdeveloped. But it doesn’t need to because folks have known for a while that ….

Human gestation is not short and seems to be even longer than expected for a primate of our body size. Relatedly, a human mother does not invest less in pregnancy than expected; she bears a large infant with a large infant brain for a primate of her body size. Humans are born with absolutely larger brains than other primates. How can we explain all this? Here’s one hypothesis:

[Text redacted to avoid spoilers. See abstract for Herman Pontzer's talk this morning here.]

One of the most common reactions to the EGG hypothesis and in defense of the obstetric dilemma is that …

… lactation is even costlier than gestation!

And this is coming, I think, from the point of view of lifetime life history theory where we assume that mammals maximize gestation length to put off lactation unless there is something adaptive about shortening gestation and sucking up those extra lactation costs. For many, this is assumed to be why we push gestation right up to pelvic limit. But then what’s adaptive about starting lactation early for all the other great apes which don’t gestate to the pelvic limit? Why not, instead, hypothesize that pregnant apes reach their EGG limit prior to their pelvic one and pregnant humans reach our EGG limit closer to our pelvic limit. In other words, our birth canal has been selected to be as adequately capacious but not as comfortable as theirs. Another common reaction to the EGG hypothesis has been…

… but the tight fit is too much of a coincidence to ignore. And I have a cheeky retort that involves my nostril and my finger, but kindly and seriously…Okay…

Well then let’s not ignore the other coincidences in other primates that clearly aren’t equipped with our bipedal pelvis. What explains their tight fits at birth? Could those explanations apply to humans? That would be the spirit of the EGG hypothesis which we have only modeled for humans so far but deserves to be tested by building the same model with other primates. Yet another common reaction I hear is…

… but why doesn’t the birth canal get bigger to make childbirth easier? And I’ve touched on this already in different ways. But another way to address this is…

It has. That we have sexual dimorphism in the bony dimensions of the birth canal and that everyone in here knows which one is male and which one is female speaks directly to the notion that the female pelvis (and not the male’s) has adapted to accommodate our relatively big babies. The adaptation works terrifically in a sort of no pain, no fitness gain kind of way. And this last common reaction I want to share is, again, all about that 30% of adult brain size at birth.

… but humans are clearly born premature!

 Well then, so are other primates and with and without a tight fit at birth, without habitual bipedalism, and without our level of encephalization. Comparing humans to altricial mammals (like carnivores, rodents, and lagomorphs) is arguably more poetic than scientific. Among anthropoids, Fragaszy and colleagues have described capuchins as relatively altricial too, given how they are only able to thermoregulate within a narrow temperature range, and have less postural control and locomotor ability just after birth compared to Old World monkeys and many platyrrhines with comparable available studies. It cannot be coincidence that neonatal capuchins have the smallest relative brain size (~50%) of all primates save for chimpanzees (~40%) and humans (~30%), meaning that they, like us, have more postnatal brain growth to accomplish compared to other primates. Now, for fun, let’s take humans out of the equation and marvel at chimpanzees instead…

Why are chimpanzees born with only 40% of their brain size when capuchins are born with 50%?! Among anthropoids, chimpanzee infants are even more helpless with their slow development and long period of dependency. For the first few months of their lives, chimpanzee infants are actively alert for only 10 percent of the day. As we’ve seen, it’s not their pelvis forcing them out early. It could be the extrauterine spring hypothesis; they’re born when they’re born to receive adaptive stimulation outside of the womb. But it could boil down to the fact that pregnant placental mammals can only grow a fetus up to a limit and then getting out there into the world is a wonderful thing for developing all there is to mammalian sociality as well. Given the trend toward greater altriciality among encephalized primates, capuchins, chimps, and humans might be better described as “less precocial” rather than singled out as somehow altricial. 

And maybe we drove ourselves to this state. Maybe we’re relatively helpless as infants because we can be, that is, because of the relaxed selection afforded by hominin caregivers. Apes are infant coddlers, and assuming our shared ancestors were too, this could have ramped up long ago, with meddling, manipulative parents and alloparents relaxing selection on infant independence, allowing them to evolve paddled feet, weak muscles, fat heavy bodies, and huge heavy heads. A scenario like this would push the origins of helicopter parenting back, potentially, into the Pliocene.

Many of our questions, even the most ultimate evolutionary ones, would be answered if we knew what triggered labor in humans and other primates. Ellison’s metabolic crossover seems to be the strongest hypothesis, but this is a research area that begs our attention. . Of course the clinical implications are significant but such knowledge would also shed light on why chimpanzees and many other primates and mammals give birth so far in advance of reaching a pelvic limit. If there is one labor trigger for all of us, how do we explain this variation in birth weight and gestation length in this large human sample? Is it metabolism and energetic throughput alone? Most probably not. It’s more likely that labor is a reaction to any number of stressors and included in that could be the size of the pelvis, but then this trigger would be a unique development in humans that would not explain the end of gestation in any species without a tight fit. Getting even more evolutionarily complex… if it all comes down to a fetal timer, then each and every species would have its specifically timed fetal timer to end gestation, and that, although not impossible, just doesn’t seem like a strong hypothesis when compared to a maternal metabolic and energetic constraint.

There is so much more to discuss, there are so many remaining questions, but I’ll end here and leave you with this: Without increasing ability to make nonhuman primate comparisons, there is little hope for knowing how bipedalism, adiposity, taillessness, encephalization, culture, etc. contribute to the evolution of pregnancy, childbirth, infancy, and how we parent and alloparent.  Live primate studies (and those of all placental mammals that pertain to these questions) are crucial if we are to explain how humans have such costly infants yet have much shorter inter-birth intervals than the rest of the hominoids. Without more detailed comparison we cannot know how costly our pregnancies and the resulting infants truly are. Primates that birth twins and practice cooperative breeding, like marmosets, hold great potential for answering many questions about reproductive physiology, metabolic limits and behavioral correlates. But for now, as far as the obstetric dilemma hypothesis goes, intense childbirth and intensive parenting are not so easily explained by bipedal pelvic anatomy. Gestation length, fetal growth, childbirth processes, and neonatal helplessness are all connected to the bipedal hominin pelvis one way or another, but whether they are fundamentally influenced by it is not an easy argument to make. The way I see it, as far as human evolutionary hypotheses go, the obstetric dilemma has gone from top dog to underdog. Support for the obstetric dilemma requires much deeper digging. And we anthropologists are great at that. Thank you.

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Terry Salad said...

Thanks for post this. Very interesting!

Ken Weiss said...

Another coup, Holly! I wish I could have been there to see the presentation, but I wasn't able to make the AAPAs this year.

Stacy said...

This was awesome! Thoroughly enjoyed being there live.

Maureen said...

This is fascinating and fits well with my Milk Hypothesis, outlined in a book entitled Milk matters: infant feeding and immune disorder. I think that we need to upend the idea of lactation as costly and infants as immature and see instead see lactation as protective (of infant and mother) and infants as being as mature as they need to be to do those essentials they need to do in order to adapt to the environment they are being born into. Milk is the unique bridge from womb to world - a sort of continuing umbilical cord for the newborn, but also the medium of exposure to the specific environment, and supporter of adaptation to that environment. As well, its mutual feedback mechanisms create bonds that ensure caregiving is personalised and ongoing, rewarding both partners. We have strayed so much from responsive breastfeeding that this seems quaint and unreal to some, but to women who have experienced the power and pleasure of normal breastfeeding for normal lengths of time, years not months, (deemed prolonged by many) it makes sense. Read the book and see how this resonates and fits with what you're discussing here.