18.1 Introduction: Evolution and Exposure to Microbes
Hints that human health might depend on certain types of contact with the natural
environment can be traced back to the nineteenth century when it was noted that hay
fever was uncommon amongst farmers (Blackley 1873). This observation had been
forgotten more than a century later when it was observed that children with multiple
older siblings had a reduced risk of developing hay fever (Strachan 1989). It is now
widely accepted that lifestyle changes that have reduced our interactions with
microorganisms have contributed to faulty regulation of the immune system, and
several overlapping hypotheses (for example, hygiene hypothesis, old friends
hypothesis, and biodiversity hypothesis) have been developed to explain these
observations (Strachan 1989; Rook et al. 2004; von Hertzen et al. 2011). The defects
in immunoregulation have contributed to startling increases in two types of illness
(Rook et al. 2013). First, there are disorders where the immune system is attacking
targets that it should not attack, such as our own tissues (autoimmune disease), gut
contents (inflammatory bowel disease), or harmless allergens (allergic disorders).
Secondly, there are disorders associated with a failure to terminate redundant
inflammatory responses. This leads to persistently raised biomarkers of inflammation, and predisposes to metabolic, cardiovascular, and psychiatric disorders.
But which organisms are involved? At first, the medical profession hypothesised
that the older siblings were providing contact with the common infections of
childhood, and that these might be necessary for maturation of the immune system
(Strachan 1989). However, when we consider this proposition in relation to human
evolutionary history, it is clearly wrong. The common infections of childhood are
crowd infections that require large populations to become endemic, and rapidly
disappear from small ones such as hunter–gatherer groups, or small island
populations (Black 1966). Measles, for example probably did not affect human
populations until sometime between 300 BC and the end of the Roman empire so
we cannot be in a state of evolved dependence on measles. But as will be discussed
below, the unfortunately named hygiene hypothesis makes this mistake and also
confuses the public and the media by exaggerating the minor role of home hygiene
(Bloomfield et al. 2016). The old friends hypothesis, which forms the background to
this essay, suggests that to understand the precise nature of our dependence on
contact with microorganisms, and the identity of the microorganisms that matter, we
need to think about vertebrate and human evolution (Rook et al. 2004, 2017; Rook
2013), and to take seriously the observations of Blackley (1873).
18.1.1 Evolution of the Microbiota
The first cellular life forms evolved on earth approximately 3.8 billion years ago.
Eukaryotic life followed about 1.5 billion years ago when an organism resembling
an alpha-proteobacterium started to live inside another organism (an endosymbiotic
328
G. A. W. Rook
Hints that human health might depend on certain types of contact with the natural
environment can be traced back to the nineteenth century when it was noted that hay
fever was uncommon amongst farmers (Blackley 1873). This observation had been
forgotten more than a century later when it was observed that children with multiple
older siblings had a reduced risk of developing hay fever (Strachan 1989). It is now
widely accepted that lifestyle changes that have reduced our interactions with
microorganisms have contributed to faulty regulation of the immune system, and
several overlapping hypotheses (for example, hygiene hypothesis, old friends
hypothesis, and biodiversity hypothesis) have been developed to explain these
observations (Strachan 1989; Rook et al. 2004; von Hertzen et al. 2011). The defects
in immunoregulation have contributed to startling increases in two types of illness
(Rook et al. 2013). First, there are disorders where the immune system is attacking
targets that it should not attack, such as our own tissues (autoimmune disease), gut
contents (inflammatory bowel disease), or harmless allergens (allergic disorders).
Secondly, there are disorders associated with a failure to terminate redundant
inflammatory responses. This leads to persistently raised biomarkers of inflammation, and predisposes to metabolic, cardiovascular, and psychiatric disorders.
But which organisms are involved? At first, the medical profession hypothesised
that the older siblings were providing contact with the common infections of
childhood, and that these might be necessary for maturation of the immune system
(Strachan 1989). However, when we consider this proposition in relation to human
evolutionary history, it is clearly wrong. The common infections of childhood are
crowd infections that require large populations to become endemic, and rapidly
disappear from small ones such as hunter–gatherer groups, or small island
populations (Black 1966). Measles, for example probably did not affect human
populations until sometime between 300 BC and the end of the Roman empire so
we cannot be in a state of evolved dependence on measles. But as will be discussed
below, the unfortunately named hygiene hypothesis makes this mistake and also
confuses the public and the media by exaggerating the minor role of home hygiene
(Bloomfield et al. 2016). The old friends hypothesis, which forms the background to
this essay, suggests that to understand the precise nature of our dependence on
contact with microorganisms, and the identity of the microorganisms that matter, we
need to think about vertebrate and human evolution (Rook et al. 2004, 2017; Rook
2013), and to take seriously the observations of Blackley (1873).
18.1.1 Evolution of the Microbiota
The first cellular life forms evolved on earth approximately 3.8 billion years ago.
Eukaryotic life followed about 1.5 billion years ago when an organism resembling
an alpha-proteobacterium started to live inside another organism (an endosymbiotic
328
G. A. W. Rook