Chapter 18
Darwinian Medicine: We Evolved
to Require Continuing Contact
with the Microbiota of the Natural
Environment. Evolution Turns
the Inevitable into a Necessity
Graham A. W. Rook
Abstract The immune system requires data inputs, especially in early life. A lack of
these inputs contributes to increases in immunoregulatory disorders such as those in
which the immune system attacks inappropriate targets (harmless allergens, selfcomponents, or gut contents) or fails to switch off unnecessary background inflammation (resulting in chronically raised biomarkers of inflammation, and cardiovascular, metabolic, and psychiatric disorders). We can use an evolutionary approach to
identify inputs that the immune systems of evolving humans inevitably received,
because these are the inputs on which we may be in a state of “evolved dependence”.
The maternal microbiota is clearly one major source of data for the developing
immune system, and we now understand that caesarean deliveries, lack of
breastfeeding, unvaried diets, and misuse of antibiotics are distorting mother-tochild transmission of the microbiota. However, the main focus of this essay is the
crucial role of inputs from the natural environment, which have received much less
attention despite the fact that epidemiology reveals strong health benefits of contact
with nature. These inputs from nature, received via the airways, gut, and skin,
provide crucial signals that set up immunoregulatory circuits. The natural environment also provides other inputs including epitopes to guide retention and expansion
of useful lymphocyte clones, information about the microbiota of the environment
into which the individual is born, signals that drive background activation of the
innate immune system, spores of gut-adapted strains that can replace those lost
because of antibiotics or poor diet, bacteriophages that modulate the microbiota,
and DNA via horizontal gene transfer that increases metabolic flexibility of the gut
microbiota. By analysing these microbial inputs and their mechanisms of action,
while also identifying the lifestyle changes that are disrupting them, we can expect to
discover novel prophylactic and therapeutic strategies.
G. A. W. Rook (*)
Centre for Clinical Microbiology, Department of Infection, UCL (University College London),
London, UK
e-mail: g.rook@ucl.ac.uk
© Springer Nature Switzerland AG 2021
C. J. Hurst (ed.), Microbes: The Foundation Stone of the Biosphere, Advances in
Environmental Microbiology 8, https://doi.org/10.1007/978-3-030-63512-1_18
327
Darwinian Medicine: We Evolved
to Require Continuing Contact
with the Microbiota of the Natural
Environment. Evolution Turns
the Inevitable into a Necessity
Graham A. W. Rook
Abstract The immune system requires data inputs, especially in early life. A lack of
these inputs contributes to increases in immunoregulatory disorders such as those in
which the immune system attacks inappropriate targets (harmless allergens, selfcomponents, or gut contents) or fails to switch off unnecessary background inflammation (resulting in chronically raised biomarkers of inflammation, and cardiovascular, metabolic, and psychiatric disorders). We can use an evolutionary approach to
identify inputs that the immune systems of evolving humans inevitably received,
because these are the inputs on which we may be in a state of “evolved dependence”.
The maternal microbiota is clearly one major source of data for the developing
immune system, and we now understand that caesarean deliveries, lack of
breastfeeding, unvaried diets, and misuse of antibiotics are distorting mother-tochild transmission of the microbiota. However, the main focus of this essay is the
crucial role of inputs from the natural environment, which have received much less
attention despite the fact that epidemiology reveals strong health benefits of contact
with nature. These inputs from nature, received via the airways, gut, and skin,
provide crucial signals that set up immunoregulatory circuits. The natural environment also provides other inputs including epitopes to guide retention and expansion
of useful lymphocyte clones, information about the microbiota of the environment
into which the individual is born, signals that drive background activation of the
innate immune system, spores of gut-adapted strains that can replace those lost
because of antibiotics or poor diet, bacteriophages that modulate the microbiota,
and DNA via horizontal gene transfer that increases metabolic flexibility of the gut
microbiota. By analysing these microbial inputs and their mechanisms of action,
while also identifying the lifestyle changes that are disrupting them, we can expect to
discover novel prophylactic and therapeutic strategies.
G. A. W. Rook (*)
Centre for Clinical Microbiology, Department of Infection, UCL (University College London),
London, UK
e-mail: g.rook@ucl.ac.uk
© Springer Nature Switzerland AG 2021
C. J. Hurst (ed.), Microbes: The Foundation Stone of the Biosphere, Advances in
Environmental Microbiology 8, https://doi.org/10.1007/978-3-030-63512-1_18
327
