How the woman got her period

Guest post by Suzanne Sadedin. This is reposted from Quora.

Suzanne got her PhD in biology from Monash University, and has done postdoctoral research at Monash University, University of Tennessee, Harvard University, and KU Leuven.

What is the evolutionary benefit or purpose of having periods?

 I'm so glad you asked. Seriously. The answer to this question is one of the most illuminating and disturbing stories in human evolutionary biology, and almost nobody knows about it. And so, O my friends, gather close, and hear the extraordinary tale of:

HOW THE WOMAN GOT HER PERIOD

Contrary to popular belief, most mammals do not menstruate. In fact, it's a feature exclusive to the higher primates and certain bats*. What's more, modern women menstruate vastly more than any other animal. And it's bloody stupid (sorry). A shameful waste of nutrients, disabling, and a dead giveaway to any nearby predators. To understand why we do it, you must first understand that you have been lied to, throughout your life, about the most intimate relationship you will ever experience: the mother-fetus bond.

Isn't pregnancy beautiful? Look at any book about it. There's the future mother, one hand resting gently on her belly. Her eyes misty with love and wonder. You sense she will do anything to nurture and protect this baby. And when you flip open the book, you read about more about this glorious symbiosis, the absolute altruism of female physiology designing a perfect environment for the growth of her child.

If you've actually been pregnant, you might know that the real story has some wrinkles. Those moments of sheer unadulterated altruism exist, but they're interspersed with weeks or months of overwhelming nausea, exhaustion, crippling backache, incontinence, blood pressure issues and anxiety that you'll be among the 15% of women who experience life-threatening complications.

From the perspective of most mammals, this is just crazy. Most mammals sail through pregnancy quite cheerfully, dodging predators and catching prey, even if they're delivering litters of 12. So what makes us so special? The answer lies in our bizarre placenta. In most mammals, the placenta, which is part of the fetus, just interfaces with the surface of the mother's blood vessels, allowing nutrients to cross to the little darling. Marsupials don't even let their fetuses get to the blood: they merely secrete a sort of milk through the uterine wall. Only a few mammalian groups, including primates and mice, have evolved what is known as a “hemochorial” placenta, and ours is possibly the nastiest of all. 

Inside the uterus we have a thick layer of endometrial tissue, which contains only tiny blood vessels. The endometrium seals off our main blood supply from the newly implanted embryo. The growing placenta literally burrows through this layer, rips into arterial walls and re-wires them to channel blood straight to the hungry embryo. It delves deep into the surrounding tissues, razes them and pumps the arteries full of hormones so they expand into the space created. It paralyzes these arteries so the mother cannot even constrict them.

What this means is that the growing fetus now has direct, unrestricted access to its mother's blood supply. It can manufacture hormones and use them to manipulate her. It can, for instance, increase her blood sugar, dilate her arteries, and inflate her blood pressure to provide itself with more nutrients. And it does. Some fetal cells find their way through the placenta and into the mother's bloodstream. They will grow in her blood and organs, and even in her brain, for the rest of her life, making her a genetic chimera.

This might seem rather disrespectful. In fact, it's sibling rivalry at its evolutionary best. You see, mother and fetus have quite distinct evolutionary interests. The mother 'wants' to dedicate approximately equal resources to all her surviving children, including possible future children, and none to those who will die. The fetus 'wants' to survive, and take as much as it can get. (The quotes are to indicate that this isn't about what they consciously want, but about what evolution tends to optimize.)

There's also a third player here – the father, whose interests align still less with the mother's because her other offspring may not be his. Through a process called genomic imprinting, certain genes inherited from the father can activate in the placenta. These genes ruthlessly promote the welfare of the offspring at the mother's expense.

How did we come to acquire this ravenous hemochorial placenta which gives our fetuses and their fathers such unusual power? Whilst we can see some trend toward increasingly invasive placentae within primates, the full answer is lost in the mists of time.

Uteri do not fossilize well.

The consequences, however, are clear. Normal mammalian pregnancy is a well-ordered affair because the mother is a despot. Her offspring live or die at her will; she controls their nutrient supply, and she can expel or reabsorb them any time. Human pregnancy, on the other hand, is run by committee – and not just any committee, but one whose members often have very different, competing interests and share only partial information. It's a tug-of-war that not infrequently deteriorates to a tussle and, occasionally, to outright warfare. Many potentially lethal disorders, such as ectopic pregnancy, gestational diabetes, and pre-eclampsia can be traced to mis-steps in this intimate game. 

What does all this have to do with menstruation? We're getting there.

From a female perspective, pregnancy is always a huge investment. Even more so if her species has a hemochorial placenta. Once that placenta is in place, she not only loses full control of her own hormones, she also risks hemorrhage when it comes out. So it makes sense that females want to screen embryos very, very carefully. Going through pregnancy with a weak, inviable or even sub-par fetus isn't worth it.

That's where the endometrium comes in. You've probably read about how the endometrium is this snuggly, welcoming environment just waiting to enfold the delicate young embryo in its nurturing embrace. In fact, it's quite the reverse. Researchers, bless their curious little hearts, have tried to implant embryos all over the bodies of mice. The single most difficult place for them to grow was – the endometrium.

Far from offering a nurturing embrace, the endometrium is a lethal testing-ground which only the toughest embryos survive. The longer the female can delay that placenta reaching her bloodstream, the longer she has to decide if she wants to dispose of this embryo without significant cost. The embryo, in contrast, wants to implant its placenta as quickly as possible, both to obtain access to its mother's rich blood, and to increase her stake in its survival. For this reason, the endometrium got thicker and tougher – and the fetal placenta got correspondingly more aggressive.

But this development posed a further problem: what to do when the embryo died or was stuck half-alive in the uterus? The blood supply to the endometrial surface must be restricted, or the embryo would simply attach the placenta there. But restricting the blood supply makes the tissue weakly responsive to hormonal signals from the mother – and potentially more responsive to signals from nearby embryos, who naturally would like to persuade the endometrium to be more friendly. In addition, this makes it vulnerable to infection, especially when it already contains dead and dying tissues.

The solution, for higher primates, was to slough off the whole superficial endometrium – dying embryos and all – after every ovulation that didn't result in a healthy pregnancy. It's not exactly brilliant, but it works, and most importantly, it's easily achieved by making some alterations to a chemical pathway normally used by the fetus during pregnancy. In other words, it's just the kind of effect natural selection is renowned for: odd, hackish solutions that work to solve proximate problems. It's not quite as bad as it seems, because in nature, women would experience periods quite rarely – probably no more than a few tens of times in their lives between lactational amenorrhea and pregnancies**.

We don't really know how our hyper-aggressive placenta is linked to the other traits that combine to make humanity unique. But these traits did emerge together somehow, and that means in some sense the ancients were perhaps right. When we metaphorically 'ate the fruit of knowledge' – when we began our journey toward science and technology that would separate us from innocent animals and also lead to our peculiar sense of sexual morality – perhaps that was the same time the unique suffering of menstruation, pregnancy and childbirth was inflicted on women. All thanks to the evolution of the hemochorial placenta.

Links:
The evolution of menstruation: A new model for genetic assimilation
Genetic conflicts in human pregnancy
Menstruation: a nonadaptive consequence of uterin... [Q Rev Biol. 1998]
Natural Selection of Human Embryos: Decidualizing Endometrial Stromal Cells Serve as Sensors of Embryo Quality upon Implantation
Scientists Discover Children’s Cells Living in Mothers’ Brains

Credits: During my pregnancy I was privileged to audit a class at Harvard University by the eminent Professor David Haig, whose insight underlies much of this research. Thanks also to Edgar A. Duenez-Guzman, who reminded me of crucial details. All errors are mine alone.

*Dogs undergo vaginal bleeding, but do not menstruate. Elephant shrews were previously thought to menstruate, but it's now believed that these events were most likely spontaneous abortions.

**One older published estimate for hunter gatherers was around 50, but this relied on several assumptions that suggest it's a significant overestimate. In particular, it includes 3 whole years of menstruation before reproduction (36 periods) for no obvious reason.

We can make an estimate from studies of the Hadza of Tanzania, who reach puberty around 18, bear an average of 6.2 children in their lives (plus 2-3 noticeable miscarriages) starting at 19, and go through menopause at about 43 if they survive that long (about 50% don't). Around 20% of babies die in their first year; the remainder breastfeed for about 4 years. So this is 25 years of reproductive life, of which about 20 are spent lactating, and 4.5 pregnant. That would leave only about 6 periods, but amenorrhoea would cease during the last year of lactation for each child, so this figure is too low. On the other hand, this calculation ignores the ~50% of women who died before menopause, miscarriages, months spent breastfeeding infants who would die, and periods of food scarcity, all of which would further reduce lifetime menstruation. Stats from: http://www.fas.harvard.edu/%7Ehb...

Not dead yet: When do we give up on an idea?

Guest post by Carina Baskett written in response to Angela Moles and Jeff Ollerton's post on Dynamic Ecology: Is the notion that species interactions are stronger and more specialized in the tropics a zombie idea?

Carina Baskett is a PhD candidate at Michigan State University in the Department of Plant Biology and the Ecology, Evolutionary Biology, and Behavior Program. She posts photos from her fieldwork and occasional articles about tropical natural history, among other things, at Wandering Nature.

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If you’ve traveled to the tropics, you know the drill. Get your shots for typhoid and yellow fever, and your meds for malaria (try to avoid the one with psychotic side effects). Don’t drink the water, and avoid the lettuce.

This over-abundance of diseases and parasites in the tropics is not just because sanitation is lacking in developing countries. Both diversity and severity of human parasites are higher in the tropics (Cashdan 2001; Guernier, Hochberg et al. 2004).

Could the same be true for plant enemies? What about other biotic interactions, like predator-prey relationships, and plants and pollinators? And why?

The first person to suggest that biotic interactions are somehow different in the tropical and temperate regions was Alfred Russell Wallace. Not only did he independently conceive of natural selection around the same time as Darwin (during a malarial fever in Malaysia, speaking of tropical diseases!), he was also a great tropical naturalist.

In the book Tropical Nature in 1878, he said, “Equatorial lands must always have remained thronged with life; and have been unintermittingly subject to those complex influences of organism upon organism, which seem the main agents in developing the greatest variety of forms and filling up every vacant place in nature.”

The “biotic interactions hypothesis” to explain high tropical diversity* is a descendent of Wallace’s beautifully stated explanation, with contributions from Dobzhansky (1950), Fischer (1960), and Schemske (2009). At its core, skipping over tangents about coexistence and specialization, today’s conception has three testable parts:

1. The relative contribution of biotic interactions to variation in relative fitness of organisms is greater at lower latitudes.
2. Biotic selective agents drive faster divergence of allopatric populations than abiotic selective agents due to coevolution.
3. Therefore, isolated populations speciate faster when the main selective agents are biotic.

For parts B and C, I’ll just tease you with some references that explore or show evidence for these hypotheses in very different ways: Farrell, Dussourd et al. 1991; Schemske 2009; Paterson, Vogwill et al. 2010; Jablonski, Belanger et al. 2013.

I’ll focus the rest of this on part A, which was recently labeled a “zombie:” false, dead, disproven. I’ll try and convince you that it’s nowhere near dead yet. I’m NOT trying to convince you that the hypothesis is true, because I think the answer is very much up in the air, but rather that it’s plausible and that we need more data.

First, the dissection. Part A is represented graphically in Figure 1 (Schemske 2009). Each arrow is the proportion of variation in fitness for the focal species caused by different selective agents: mutualists, antagonists, and the abiotic environment. A wider arrow is a greater proportion. A solid line shows a positive effect on fitness, while a dashed line is negative. (Note that the arrows go both ways for the biotic agents. They coevolve, while abiotic agents do not, which gets into parts B and C of the hypothesis.)

Here’s what this abstract figure would look like on the ground. This past winter here in Michigan was, to put it lightly, a doozy. Two years ago, it was so mild that I was told that my first Michigan winter didn’t even count. It’s not hard to imagine that even after lineages have evolved to tolerate freezing (which is a big deal—it kills cells!), there can still be a lot of variation in fitness depending on the weather.

Think of a plant that lives for a few years, flowering in the summer, producing fruit in the fall, and dying back over winter. Let’s assume that there’s a resource tradeoff between manufacturing antifreeze and producing fruits.** This past winter, plants that invested a lot in antifreeze would have had high relative fitness in the population, because they alone survived. Two years ago, that same strategy would have had low relative fitness, because plants that produced less antifreeze would have survived the winter too, but had higher fruit production. In this hypothetical situation, there is some variation in fitness due to herbivores and pollinators etc., but most of it is due to the wildly variable weather.

In contrast, imagine a similar plant in a tropical habitat, growing in full sun. It experiences temperature stress too. The sunshine is actually more intense in the tropics because it’s hitting the Earth straight on instead of at an angle, so its energy is concentrated in a smaller area. It’s HOT! But it’s hot almost every single day of the year, so all the plants in the population invest in tolerating the heat to the same degree. Temperature isn’t contributing much variation in fitness in this population.

Life here is more like the Hunger Games. Who can grow the fastest? Who can avoid death by enemy herbivores and diseases? Who can form the strongest alliances with pollinators and fruit dispersers? Competition, antagonism, and mutualism is what determines fitness here, not the weather.***

Now that I’ve painted a picture of what Figure 1 could hypothetically look like in the real world, how can we figure out whether or not it’s true?

Ideally, you would pick a focal species and do an observational or experimental path analysis (e.g., Schemske and Horvitz 1988) to determine the relative contributions of various selective agents at different latitudes. Make sure you have an army of assistants, because you’ll need massive sample sizes. Did I mention you’ll have to do it for many years? You won’t want to miss important events like unusually bad winters or pest outbreaks. By the way, even though this kind of study would probably be impossible in animals, it’s also nigh-impossible to find an abundant plant species whose native range encompasses tropical and temperate latitudes, avoiding really dry places and high altitude. (If you know of one, please let me know!!)

Needless to say, filling in Figure 1 with real data has not yet been done, and given our funding climate, it probably never will. But, there are other ways to approximately test the hypothesis (Schemske, Mittelbach et al. 2009).

What we CAN ask is, what is the “intensity” of the interaction today? What do today’s traits tell us about selection in the past? And what is the frequency of an interaction in the community?

To illustrate each question in terms of pollination, we can ask how much do tropical plants rely on self-pollination vs. outcrossing; do tropical plants invest more in pollinator attraction and reward; and, do tropical plant communities show a higher frequency of animal vs. wind pollination? Fill in the blanks with your favorite interaction.

To build a relatively complete approximation of Figure 1, we should be asking these questions in many systems, across many types of interactions, and at many spatial and phylogenetic scales. For example, asking these questions within widely-ranging species (Salazar and Marquis 2012) is quite different from asking them at the community level, with disparate habitats, community membership, and growth forms (Moles, Wallis et al. 2011). Both approaches are needed, because each has huge advantages and severe limitations.

The most comprehensive review of the available data is a 2009 Annual Reviews paper by Schemske et al. (see their Table 1). They noted that the data was insufficient for meta-analysis. Nevertheless, they found that most interactions show greater “importance” at lower latitudes; that is, the interaction is more intense currently, the traits show that it was more intense in the past, or it is more frequent. None of the interactions shows greater importance at higher latitudes.

For example, in the tropics, predation rates on birds’ nests are higher. Ant predation rates on insect bait are higher. Parasite pressure is higher. Palatability of marine worms, salt marsh plants, leaves, and butterfly larvae is lower. The frequency of animal pollination, animal seed dispersal, ant-plant mutualisms, endophytes, and cleaning symbioses is higher. The review also finds that herbivory rates are higher and plants are better defended at lower latitudes, but a recent meta-analysis on herbivory came to different conclusions (Moles, Bonser et al. 2011).

Although the results are necessarily qualitative and we can’t put a p-value on this statement yet, this review shows that looking across many types of interactions, many ways of quantifying their importance, and over many spatial and phylogenetic scales, the weight of the available evidence supports Figure 1.

But I would be the last person in the world to tell you that we’re done testing part A of the biotic interactions hypothesis. Much of the available data was not generated to explicitly address it, so there’s always something missing. For example, herbivory rates could be the same at different latitudes, but tropical plants may be better defended, indicating that greater herbivore pressure has selected for stronger defense. You need both pieces of the puzzle, preferably measured at the same time on close relatives, to be able to say whether herbivore pressure is greater in the tropics.

I’ve spent the last three years thinking about how we can fill in the missing gaps. There are so many ways to test these questions, so many interactions and species to choose from. Each approach is limited in some key way; otherwise, the end-all, be-all experiment would have already been done! One could easily spend a lifetime chipping away at this question from different angles, without even addressing the bigger picture of whether this has anything to do with the latitudinal diversity gradient. (I’m working on that too though!)

Therefore, I was dismayed when I woke up on Tuesday to a post on a widely-read ecology blog that claimed that the hypothesis that biotic interactions are stronger in the tropics is a “zombie idea.” Meaning that it’s dead, it’s been disproven, we can all go home now, and anyone who studies it is just wasting their time.

Whoa. Not enough data for a meta-analysis, but we’re done with this question? A recent review concluded that there is support for the hypothesis, but now it’s been totally debunked? Did I miss something here?

In fact, I haven’t missed anything. As with any scientific controversy worth its salt, there are contradictory reviews, there are people who are highly skeptical, there is massive confusion about what the hypothesis is and how to properly test it. That’s all fine and good. It’s exciting, even.

What is not fine and good, in my book, is to proclaim from the rooftops that we’re done with a question that we’ve barely begun to address. To claim that a handful of publications on latitudinal gradients in herbivory are the end-all, be-all, period end of story of decades of research. To claim that any one of us has the final authority on how to define, test, and interpret an area of science.

A debate about an idea can be constructive and fun. But both my scientific and journalistic selves cry fowl when a story is presented hyperbolically from one point of view. I believe that it’s irresponsible and polarizing to instigate a debate by claiming that the problem is solved and there is no debate.

I’m glad that people are talking about the topic, though I wish it had been inspired by less inflammatory language. I hope the conversation inspires us to clarify what our questions are and how we can test them. I hope also that you agree that we don’t need more catchy metaphors (zombies, old clothes, lemmings, sheep). We need more data and more conversation. Period. But not the end of the story.


*There are so many species in the tropics! There are over 22,000 tree species in the Amazon, compared to 620 in temperate North America (Currie and Paquin 1987; Fine and Ree 2006). This pattern of higher species diversity in the tropics is remarkably consistent across different types of organisms and through time and space. How can the same underlying processes of ecology and evolution produce such different outcomes? We don’t really know! Sure, there are ideas. In fact, Palmer (1994) lists 120 hypotheses to explain it! But given the massive scale of space and time, it’s really hard to test these hypotheses, so a definitive answer remains elusive. See Mittelbach, Schemske et al. (2007) for a great review.

**For any of this to matter for evolution, we are also assuming that allocation strategies are not very plastic; that they are heritable; and that there is genetic variation for these strategies in the population.

***Why am I focusing so much on temperature? Lots of studies show that climatic variables, especially temperature, are tightly correlated with global diversity patterns (e.g., Currie, Mittelbach et al. 2004). In my opinion, for a few reasons, the biotic interactions hypothesis is the only latitudinal diversity gradient hypothesis that provides a plausible mechanism by which temperature can affect diversity. But actually, the hypothesis is generalizable to any gradient in abiotic stress. Although it was proposed to address the LDG, it applies to other gradients in abiotic stressors that covary with species diversity: altitude, ocean depth, precipitation, etc (Schemske, Mittelbach et al. 2009). This is a practical strength because components of the biotic interactions hypothesis can be tested in other systems, which may be more tractable than latitude. More importantly, it is a theoretical strength because confirming this hypothesis could revolutionize our approach to studying the origins of diversity in many systems.

References:

Cashdan, E. (2001). "Ethnic diversity and its environmental determinants: Effects of climate, pathogens, and habitat diversity." American Anthropologist 103(4): 968-991.

Currie, D. J., G. G. Mittelbach, et al. (2004). "Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness." Ecology Letters 7(12): 1121-1134.

Currie, D. J. and V. Paquin (1987). "Large-scale biogeographical patterns of species richness of trees." Nature 329(6137): 326-327.

Dobzhansky, T. (1950). "Evolution in the tropics." American Scientist 38: 209-221.

Farrell, B. D., D. E. Dussourd, et al. (1991). "Escalation of plant defense: Do latex and resin canals spur plant diversification?" American Naturalist 138(4): 881-900.

Fearnside, P. M. (2005). "Deforestation in Brazilian Amazonia: History, rates, and consequences." Conservation Biology 19(3): 680-688.

Fine, P. V. A. and R. H. Ree (2006). "Evidence for a time-integrated species-area effect on the latitudinal gradient in tree diversity." American Naturalist 168(6): 796-804.

Fischer, A. G. (1960). "Latitudinal variation in organic diversity." Evolution 14: 64-81.

Guernier, V., M. E. Hochberg, et al. (2004). "Ecology drives the worldwide distribution of human diseases." Plos Biology 2(6): 740-746.

Jablonski, D., C. L. Belanger, et al. (2013). "Out of the tropics, but how? Fossils, bridge species, and thermal ranges in the dynamics of the marine latitudinal diversity gradient." Proceedings of the National Academy of Sciences of the United States of America 110(26): 10487-10494.

Mittelbach, G. G., D. W. Schemske, et al. (2007). "Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography." Ecology Letters 10(4): 315-331.

Moles, A. T., S. P. Bonser, et al. (2011). "Assessing the evidence for latitudinal gradients in plant defence and herbivory." Functional Ecology 25(2): 380-388.

Moles, A. T., I. R. Wallis, et al. (2011). "Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes." New Phytologist 191(3): 777-788.

Palmer, M. W. (1994). "Variation in species richness: towards a unification of hypotheses." Folia Geobotanica & Phytotaxonomica 29(4): 511-530.

Paterson, S., T. Vogwill, et al. (2010). "Antagonistic coevolution accelerates molecular evolution." Nature 464(7286): 275-U154.

Salazar, D. and R. J. Marquis (2012). "Herbivore pressure increases toward the equator." Proceedings of the National Academy of Sciences of the United States of America 109(31): 12616-12620.

Schemske, D. W. (2009). Biotic interactions and speciation in the tropics. Speciation and Patterns of Diversity. R. K. Butlin, J. R. Bridle and D. Schluter. Cambridge, United Kingdom, Cambridge University Press: 219-239.

Schemske, D. W. and C. C. Horvitz (1988). "Plant-animal interactions and fruit production in a neotropical herb: a path analysis." Ecology 69(4): 1128-1137.

Schemske, D., Mittelbach, G., Cornell, H., Sobel, J., & Roy, K. (2009). Is There a Latitudinal Gradient in the Importance of Biotic Interactions? Annual Review of Ecology, Evolution, and Systematics, 40 (1): 245-269 DOI: 10.1146/annurev.ecolsys.39.110707.173430.