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Life history theory and the microbiome

This is a re-post of a previous entry, now updated.

Life history theory, a concept first described by Yale evolutionary biologist Stephen Stearns, is the application of evolutionary biology to the entire life cycle from birth to death. It includes the hypothesis that features of life are shaped by natural selection in ways that might have maximized fitness (in the Darwinian sense) during our evolutionary past.

These life features include: the long (9 month) gestation period of humans, the relative helplessness and dependence on parental protection of the human infant (altriciality), our long childhood, the timing of reproductive maturity (menarche and adrenarche) and sex differences in development, body size, the timing and existence of menopause, how we age, and the timing of death. So yeah, pretty much everything.

According to Thom McDade, “a fundamental assumption of life history theory is that resources are limited, and that they can be invested in three primary areas: growth, reproduction, and maintenance. Resources can also be invested in storage for future use. According to the allocation rule, resources used for one purpose cannot also be used for another, and trade-offs are therefore inevitable.”

Life history, then, is all about tradeoffs. Some of these tradeoffs involve the timing of reproduction. 

Consider the fact that human women have a long post-reproductive lifespan. That is, humans have a menopause. Menopause has been medicalized so that physicians have labelled it “premature ovarian failure” akin to other kinds of organ failure or deficiency syndromes. Treating menopause as a disease instead of a normal part of life has serious consequences. For example, hormone replacement therapy (HRT) for post-menopausal women was belatedly discovered to be linked with higher rates of ovarian cancer and breast cancer. I was dismayed to find out that my own mother was taking HRT well after this cancer link was publicized. (She is not now.)  Menopause is not a disease, although it can cause uncomfortable symptoms in some women. Understanding the evolutionary reasons for menopause might help some patients and their physicians avoid unnecessary treatments.

The onset of reproduction involves other tradeoffs. In girls undergoing puberty, reproductive maturity is accompanied by a surge in estrogen production. Increased estrogen causes the the growth plates in long bones to close (epiphysial closure), arresting bone growth. The coincidence of these two events is not accidental. Because of resource constraints and limited energy, girls can invest their body resources in growth – becoming taller – or instead invest those limited resources preparing the body for reproduction. Other tradeoffs exist between growth and reproduction, between body maintenance and reproduction, and between growth and defense against infection (just to name a few). The tradeoff between reproduction and body maintenance was beautifully described in this piece about the death habits of female octopus. We are not the same as an octopus, of course.  However, dramatic tradeoffs exist in our physiology and in human development. These tradeoffs suggest that during human evolution, we were energy constrained; i.e. there were not enough calories to invest maximally in everything at once. Something had to give. This tradeoff is still evident in our bodies and in our development.

Another important tradeoff that has been uncovered by evolutionary anthropologists involves infants who are born small or premature. These children develop differently than normal weight babies. Most importantly, they have more inflammation, more cardiovascular disease, and more diabetes.

This relationship first came to light when David Barker documented a curious association between birth weight and adult cardiac events in British men. Babies born small had a higher risk of chronic inflammatory diseases as adults. These small babies have been described as adopting a “thrifty phenotype.” That is, nutrient deprivation as a fetus is thought to have shaped the developmental trajectory in these individuals. This shift results in reduced expenditure on muscle and increased energy storage as fat.

These developmental adjustments have been called “thrifty” because muscle has much greater metabolic fuel demands than does fat. In addition, these small babies are also known to differ in the composition of their adipose tissues: they store fat primarily as visceral fat.  Visceral fat is the “unhealthy” abdominal fat which predisposes to diabetes and atherosclerosis. However, visceral fat has the advantage of being readily mobilized in the setting of stress or infection. The combination of metabolic thriftiness, reduced outlays devoted to costly muscle tissue, and increased ability to mobilize energy during times of stress is posited to promote survival. In terms of human development, the thrifty phenotype also preserves priority energy access for key organs, such as the brain. Most importantly, accumulation of visceral fat helps protect animals against invasive pathogens from the microbiome, as we discussed recently in this post. In other words, babies born small undergo a variety of developmental and physiologic changes. This physiologic flexibility makes the best of a bad job – it protects vulnerable babies, but it comes with a late-life cost. That cost includes Barker’s observation of more heart disease in babies born small. This is a classic example of a tradeoff between body functions that affects development. It is also the genesis of the notion of developmental origin of health and adult disease (Dohad).

Mary Jane West Eberhard sketched a scenario in which the these tradeoffs are primarily driven by selection from infectious disease. That was the topic of this podcast episode. As I  discussed with West Eberhard later, it is possible that the microbiome has much to do with this tradeoff, and that natural selection has shaped our propensity to become fat or have heart disease, because of early life microbial exposures and infection risk from the microbiome. The bottom line is this: kids born small have a higher risk of dying of infection. They make necessary adjustments to development that prioritize inflammation and immune defense. The immune system is tuned in a way that makes obesity more likely and also contributes to chronic low grade inflammation. That, in turn, increases the risk of diabetes, stroke and heart attacks.

Because infants inherit their microbiota from their mothers, and are bathed in microbial cues even in utero, microbes are well positioned to play a role in developmental programming. Microbiota transfer from mothers is a key determinant of the composition of babies’ gut microbiota. This has durable effects, and it follows that microbiota transfer offers a method of intergenerational transfer of immunity, and of phenotype.

The developing fetus is bombarded with cues of microbial environment of its mother, both before and after birth, These microbiota will become the babies’ microbiome, part of which may stay with the individual for life.

It turns out that exposure to certain microbes triggers a response that adjusts the development of the immune system to allows it to better deal with future infectious threats from within and without.  Transfer of microbiota, from maternal skin, breast milk, GI tract, and saliva, play a huge role in determining whether an infant has allergic diseases, metabolic disorders, and autoimmune diseases. That, my friends, is one way in which the microbiome affects life history traits.

Late Update: Jessica Metcalf et al. wrote a terrific piece on microbiome involvement in life history transitions, triggering developmental changes in multiple species, ranging from tree frogs, to mustard plants, to mosquitos. The article, titled Why Evolve Reliance on the Microbiome for Timing of Ontogeny?, also discusses how microbial influence over hosts’ development is not always benign. Microbes can hijack the process, as when parasites castrate their hosts (thereby preventing reproduction, causing increased body size, and promoting parasite fitness.) Metcalf et al write: “When the benefits of using microbiome cues outweigh the costs of potential exploitation emerging from misaligned incentives is a question ripe for detailed investigation.” I agree.

Copyright © Joe Alcock MD

Categories: Uncategorized

Joe Alcock

Emergency Physician, Educator, Researcher, interested in the microbiome, evolution, and medicine

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