There are two primary points that need to be addressed in order to appreciate these findings.
In the first, we note the fact that the human body is host to over 100 trillion bacteria, both in and on us that are instrumental in maintaining health. These commensual bacteria outnumber our own cells by about 10 to 1 [the genetic ratio is 100 to 1 - often called the second genome]. Of late, it is becoming increasingly clear that these "partners" aren't merely casual elements of our existence, but are required for our very survival.
In this respect, the conventional view of life being controlled and driven by genes, is insufficient in producing a viable, healthy organism. While much is still unknown, there are strong implications regarding the relationship of these bacteria to the host organism, as well as the role of their genetic diversity.
It appears that bacteria are also responsible for "training" the host's immune system to recognize "friendly" versus pathogenic bacteria. Commensual bacteria also play a role in preventing pathogenic bacteria from taking up residence, killing nonindigenous bacteria, producing nutrients, and affecting tissue development (1).
In short, we can see that the role of the microbiota is quite significant. I am reluctant to simply consider the relationship as commensual, symbiotic or parasitic, but would rather consider it to be much more integrated than such definitions presume.
Now in considering the second part of this issue; human pregnancy, we find that body fat increases early in pregnancy, with a reduction in insulin sensitivity later. This reduction in insulin sensitivity is related to changes in immune status and appears to drive obesity-associated metabolic inflammation.
Of interest is that while excess accumulation of fat and loss of insulin sensitivity are normally detrimental to long-term health, they are beneficial within the context of a normal pregnancy, by supporting growth of the fetus and preparing for lactation.
Now for the good bit.
It appears that throughout pregnancy the gut bacteria (Proteobacteria and Actinobacteria) undergo a radical alteration [between the first trimester and the third] in population diversity such that the bacteria promote the changes necessary for a healthy pregnancy, despite their presence being detrimental in a normal healthy adult. Moreover, the bacterial diversity continues after birth for about one month in the mothers, while the infants return to normal levels (diversity similar to those of the mother's first trimester state) by 4 years of age. It is also important to note that this abrupt change in population diversity was present in the mothers, regardless of their individual states of health, so these changes cannot be attributed to be artifacts associated with any specific condition of the mother.
Further confirming the role of the gut bacteria was accomplished by transferring the bacteria to germ-free mice and noting the effect.
"The transfer of specific gut microbiotas to otherwise healthy germ-free wild-type mice is sufficient to induce symptoms of metabolic syndrome, which, in addition to inflammation, include reduced insulin sensitivity and excess weight gain."
"Dysbiosis, inflammation, and weight gain are features of metabolic syndrome, which increases the risk of type 2 diabetes in nonpregnant individuals. These same changes are central to normal pregnancy, where they may be highly beneficial, as they promote energy storage in fat tissue and provide for the growth of the fetus. Our work supports the emerging view that the gut microbiota affect host metabolism; however, the context (pregnant or not) defines how the outcome is interpreted (healthy or not). Metabolic changes are necessary to support a healthy pregnancy, which in itself is central to the fitness of a mammalian species. We hypothesize that, in mammalian reproductive biology, the host can manipulate the gut microbiota to promote metabolic changes. Thus, the origins of host-microbial interactions that skew host metabolism toward greater insulin resistance, and which underlie much of the present-day obesity epidemic, may lie in reproductive biology."
Cell 150, 470–480, August 3, 2012 ª2012 Elsevier Inc.In my view the significance of this study is in suggesting that the microbiota plays a fundamental role in supporting human fitness. This would have significant ramifications on simplistic views of what is being "selected for" by natural selection. This could provide a strong basis for considering living organisms as being much more integrated than is generally thought. Another avenue of consideration is that if the host is capable of manipulating the microbiota, then this also creates an interesting perspective since a host may be capable of taking advantage of a "trait" which is already present in another organism. As a result, this also would profoundly change the view of "selection". In the latter case, it is entirely possible that the genome may never "evolve" to contain the desired trait, but instead the organism becomes dependent on commensuals to fulfill that role [NOTE: This would be similar to many other instances where such bacteria provide the necessary mechanisms to digest food that would otherwise be indigestible].
Just as termites are dependent on symbiotic protozoa to digest the cellulose they eat, we find that the necessity of microbiota in organisms is a necessary condition for survival. This raises the point that selection of specific genetic traits is insufficient in establishing the fitness of an organism without correspondingly considering the coevolution of commensual organisms. What is becoming increasingly clear is that many organisms may acquire the necessary "adaptations" of their survival by exploiting commensuals rather than possessing those traits in their genes.
(1) For more information regarding the effect of microbes on host systems:
Citation: Omry Koren, Julia K. Goodrich, Tyler C. Cullender, Ayme ´ Spor, Kirsi Laitinen, Helene Kling Backhed, Antonio Gonzalez, Jeffrey J. Werner, Largus T. Angenent, Rob Knight, Fredrik Ba ¨ ckhed, Erika Isolauri, Seppo Salminen, and Ruth E. Ley, Cell, Volume 150, Issue 3, 470-480, 3 August 2012, 'Host Remodeling of the Gut Microbiome and Metabolic Changes During Pregnancy'