Miami Dade College Disgust as A Way of Avoiding Pathogens Article Review hi is just a 500 word response about an article that is attached, the other articl

Miami Dade College Disgust as A Way of Avoiding Pathogens Article Review hi is just a 500 word response about an article that is attached, the other article is examples/guideline on how to read it Downloaded from rstb.royalsocietypublishing.org on January 19, 2011
Phil. Trans. R. Soc. B (2011) 366, 389–401
doi:10.1098/rstb.2010.0117
Research
Disgust as an adaptive system for disease
avoidance behaviour
Valerie Curtis*, Mı́cheál de Barra and Robert Aunger
The Hygiene Centre, London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK
Disgust is an evolved psychological system for protecting organisms from infection through disease
avoidant behaviour. This ‘behavioural immune system’, present in a diverse array of species, exhibits
universal features that orchestrate hygienic behaviour in response to cues of risk of contact with
pathogens. However, disgust is also a dynamic adaptive system. Individuals show variation in pathogen avoidance associated with psychological traits like having a neurotic personality, as well as a
consequence of being in certain physiological states such as pregnancy or infancy. Three specialized
learning mechanisms modify the disgust response: the Garcia effect, evaluative conditioning and the
law of contagion. Hygiene behaviour is influenced at the group level through social learning heuristics such as ‘copy the frequent’. Finally, group hygiene is extended symbolically to cultural rules
about purity and pollution, which create social separations and are enforced as manners. Cooperative hygiene endeavours such as sanitation also reduce pathogen prevalence. Our model allows us to
integrate perspectives from psychology, ecology and cultural evolution with those of epidemiology
and anthropology. Understanding the nature of disease avoidance psychology at all levels of
human organization can inform the design of programmes to improve public health.
Keywords: infectious disease; disgust; evolutionary psychology; adaptive variation;
hygiene behaviour; manners
1. INTRODUCTION: THE PROBLEM
OF PARASITES
Parasites are ubiquitous; in some ecosystems their
biomass rivals that of predators [1]. Parasitic viruses,
bacteria, protozoa, nematodes, helminthes and arthropods live in durable relationships with their hosts,
from whom they draw energy, shelter, transport and
reproductive opportunity. They damage their host’s
inclusive fitness by producing toxins, manipulating
behaviour to their own ends, and spreading to kin
and community [2]. The costs of infection constitute
an important selection pressure, which all animals
face. As a result, natural selection has designed elegant
and interlocking solutions to protect animals from
parasite damage, including a range of physiological
barriers and a complex immune system [3]. Beyond
these physiological defences, animals also defend
themselves from infection through behaviour that
functions as a ‘behavioural immune system’ [4].
Pathogen avoidance behaviour has a long evolutionary history, and can be found in a broad range of taxa.
For example, eusocial insects manage faecal wastes
[5], crustaceans avoid diseased conspecifics [6], herbivores forage selectively to avoid faeces [7,8] and
grooming behaviour is found in a range of species
[9]. The disgust system is a psychological mechanism
for producing pathogen avoidant behaviour [10 – 12].
In previous work, we have stressed the universality
of disgust, showing that there is much that is similar
about disgust responses between animals and humans,
between humans and over historical time [11,13].
However, there is also much that differs between individuals and between social groups. In this paper, we
look at disgust and disease avoidance behaviour in
human individuals and in human social groups as an
adaptive system. Natural selection has produced a
solution to the problem of hard-to-detect parasites
by designing a system that is sensitive to local information about infection risk. This system responds to
parasite pressure not just over evolutionary time, but
over lifetimes, using what cues it can. This may be
information about an individual’s current state, its
history of sickness and exposure to disgusting experiences, or what it has learnt from the local culture
and from the hygiene practices of others.
In this paper, we begin by recapping evidence that
disgust is a universal driver of pathogen avoidance
behaviour in humans. We then turn to sources of
variation in the disgust system at the individual and
group level. We set out the links between the hygiene
behaviour of individuals and of groups and between
individual disgust and the content of cultures. This
allows us to integrate perspectives from psychology,
ecology and cultural evolution, as well as epidemiological perspectives on disease prevalence, anthropological
perspectives on manners and morality, and the symbolism of purity and pollution. Our conclusions stress
the importance of using an evolutionary perspective in
combination with interdisciplinary sources to provide
* Author for correspondence (val.curtis@lshtm.ac.uk).
One contribution of 14 to a Theme Issue ‘Evolution and human
behavioural diversity’.
389
This journal is q 2011 The Royal Society
Downloaded from rstb.royalsocietypublishing.org on January 19, 2011
390
V. Curtis et al.
Disgust as an adaptive system
an integrated understanding of the set of human behaviours that have a foundation in pathogen avoidance.
This, may, in turn, offer insights that are important to
the practice of public health.
2. THE UNIVERSALITY OF DISGUST
Disgust is a fundamental part of human nature.
Darwin was the first to propose that disgust is
expressed universally [14] and many studies since
then have supported this proposal [15,16]. Though
there has been no systematic cross-cultural survey of
the objects and events that elicit disgust in humans,
the available data suggest that there is a universal set
of disgust cues. These include bodily wastes, body
contents, sick, deformed, dead or unhygienic people,
some sexual behaviour, dirty environments, certain
foods—especially if spoiled or unfamiliar—and certain
animals [11,17,18]. Objects that have contacted any of
the above can also become disgusting. Further, certain
types of immoral acts are widely described as disgusting. Contact with disgust elicitors, real or imagined, is
associated with (i) a characteristic facial expression
that is recognizable across cultures [16,19], (ii) behaviour patterns that include withdrawal, distancing,
stopping or dropping the object of disgust and shuddering [20,21], (iii) physiological changes including
lowered blood pressure and galvanic skin response,
recruitment of serotonin pathways, increased immune
strength [22,23], and (iv) reports of negative affect
including nausea.
Pathogen avoidance behaviour is universal across
cultures, with all societies demonstrating individual
and group-level hygiene behaviours. These include
bodily, domestic and communal cleansing, avoidance
of close contact or exchange of bodily fluids with
others (with exceptions for mates and kin), and the
avoidance of foods that are spoilt, contaminated or
unfamiliar.
Explanations of disgust in the philosophical,
anthropological, humanities and psychological literatures have been varied and inconsistent, reflecting
this broad range of phenomena to be explained. The
phenomenological philosopher Aurel Kolnai thought
that disgust resulted from excess and surfeit:
‘A surplus of life, . . . an indifference to quality . . . a
desire towards death’ [24, pp. 72 – 73]. Freud considered disgust a learned reaction formation that
could be cultivated towards any activity through
development [25]. The social anthropologist Mary
Douglas argued that dirt and disgust are a product of
culture, such that anomalous objects and events that
do not fit the local cosmology have to be rejected, so
as not to threaten social order [26]. In psychology,
the dominant Rozin–Haidt school has disgust originating in the rejection of spoiled foods, but also serving to
cope with the existential terror of being an animal and
hence mortal [21,27]. A recent cultural study of disgust
labels it ‘the Hydra’ since it seems too complex to
explain [28].
An evolutionary perspective, however, provides a
parsimonious explanation for the multiple elicitors
and the behavioural tendencies of the disgust system.
According to Darwinian thinking, disgust should
Phil. Trans. R. Soc. B (2011)
be considered an adaptive system that drives the
behavioural avoidance of infectious disease [11] Constant selection pressure from the ubiquitous presence
of pathogenic parasites in animal and human ancestral
environments [29] would have selected for those individuals with alleles disposing towards a ‘behavioural
immune system’ preventing contact with, and incorporation of, pathogens [4]. Setting aside, for the
present, the issue of moral disgust, it can be seen
that all of disgust’s basic elicitors (listed above) are
implicated in the risk of transmission of infectious disease [11] and paired stimuli with, and without, disease
risk show significant differences in disgust response
[10,12]. This relationship between disgust elicitors
and disease sources appears consistently across cultures and through the historical record [14,20,30].
Rats and other mammals display the characteristic
gape expression after eating noxious food, and, as in
humans, this reaction is dependent on the insular
cortex [31] suggesting that disgust may be at least a
pan-mammalian adaptation. Because behavioural
immune systems are ubiquitous in animals and predate
the evolution of modern humans, all humans should
come equipped with a disgust system, rather than
learning disgust as a product of culture (as Douglas,
Freud and their followers have argued). It is also
unlikely that disgust in humans originated in food
distaste, because of the pan-vertebral need to avoid
pathogens of all types, not just those using food as a
vector of infection.
Brain imaging studies also show that there is a
specific network associated with disgust. Viewing
images of disgusting stimuli, or videos of people with
disgusted expressions results in robust and recurring
activation in specific brain areas—a neural network
including the anterior insular cortex, basal ganglia,
ventrolateral prefrontal cortex, anterior temporal
cortex, medial prefrontal cortex and visual cortex
[25,32,33]. Autobiographical recall of disgusting episodes activates the insular cortex and the basal ganglia
[34], as does exposure to disgusting smells [33]. Two
recent meta-analyses of functional neuroimaging studies
of emotion found that activation of the basal ganglia was
reliably associated with disgust [35].
3. THE VARIABILITY OF DISGUST
Although disgust has an ancient and universal function, the disgust system reacts with different levels of
activation to the same stimulus between individuals
and over the lifetime of the same individual [27,36].
Figure 1 shows global variation in disgust sensitivity
from a web survey with 38 845 participants. They were
asked to rate how disgusting they found a series of
disease-relevant images such as a sick person, a plate
of what looked like bodily fluids and a crowded underground train, on a Likert scale of 0– 5 (see [10] for
details of methods). The results showed a high
degree of variability between individuals (average
standard deviation ¼ 0.83). Differences in variability
between continents were not statistically significant,
varying only between 3.77 and 3.94 (s.d. ¼ 0.05).
Though a multivariate ANOVA model controlling for
age, gender and occupational differences found
Downloaded from rstb.royalsocietypublishing.org on January 19, 2011
Disgust as an adaptive system V. Curtis et al. 391
l
ta
to
Bl
o
Ea
s
te
rn
tin
on
bc
Su
In
di
an
ck
t
ic
er
m
A
th
or
N
M
id
dl
eE
as
en
a
a
er
m
A
in
t&
t ra
us
La
t
th
lia
A
/O
m
ce
er
an
ic
ic
ia
a
e
op
N
t
rE
as
Fa
Eu
r
or
A
Su
bs
ah
ar
an
A
fri
ca
5.0
4.5
4.0
3.5
3.0
2.5
2.0
1.5
1.0
0.5
0
Figure 1. Mean and standard deviation of disgust scores for a sample of 38 845 individuals by region.
cultural region to be a significant predictor of disgust
sensitivity, this result was largely explained by the
low average disgust sensitivity in the Australia/Oceania
sample.
How do differences in disgust sensitivity arise?
Evolutionary psychological approaches assume that
psychological systems—including emotions—represent
solutions to adaptive problems repeatedly encountered
during evolutionary history. Plasticity in these systems
should reflect the degree of variability in these problems: low levels of variability over the lifespan and
between generations will favour the evolution of
highly constrained systems. Such systems reliably
develop in a broad range of environments with little
phenotypic variation and have the benefit of efficiency
and rapid and reliable development [37]. Greater
environmental variation, on the other hand, should
favour more plastic systems that use environmental—
including social—information to adaptively shape
behaviour according to the challenges of the local
environment [38].
Pathogen pressure has led to the selection of a
disgust/hygiene behaviour system in individuals that
is both universal and plastic to local environmental
variation. Figure 2 schematizes the factors that
influence the human disease avoidance system. While
disgust motivates hygiene behaviour, disgust sensitivity
varies between individuals as a trait and within individuals by their state and also through individual learning.
Disgust and hygiene in ultrasocial humans facing
shared pressure from pathogens are not, however,
simply a matter for individuals. The lower half of the
diagram depicts group effects in the adaptive system.
Culture—the socially acquired information shared by
a particular group—affects the individual system
through social learning and group hygiene behaviour
through norms about manners. Group hygiene can be
symbolically extended into cultural ideas about
purity and pollution and can also affect public health
by influencing the prevalence and virulence of
pathogens in the environment. Group hygiene also
influences the hygiene behaviour of individuals via
imitation. The content of culture is, itself, a product
Phil. Trans. R. Soc. B (2011)
of the individual brains that support it and so reflects
the predispositions of those brains. Finally, pathogens
exert selective pressure on the whole system.
All of the components of the system, whether
in brains (shown on the left of the diagram) or in
behaviour (shown on the right) are affected by
environmental factors extraneous to the disease avoidance system, including seasonality, climate, ecosystem,
habitat and the particular structure of host populations
(not shown). In the following sections of this paper, we
describe the elements of this adaptive system and how
it works. (For ease of reference, numbers in the figure
refer to the relevant sections of the paper.)
4. DISGUST IN BRAINS: SOURCES OF DIVERSITY
Figure 2 shows pathogens exerting selection pressure
on individual disgust and the hygiene behaviour
it motivates. However, selection has not produced a
constant level of disgust sensitivity. Variation can
be accounted for by three kinds of phenomena:
(i) innate trait differences; (ii) by plasticity, which
allows for adaptation to current states; and (iii) the ability to learn from changes in the environment over the
lifespan. These types of influence will be treated in turn.
(a) Trait-based variation in disgust sensitivity
Individuals can consistently deviate from each other in
behaviour because of stable trait-based differences.
These arise from previous histories of adaptation
in differing selective environments or trade-offs with
other competing needs. A variety of traits are associated
with variation in disgust sensitivity, including personality, gender and maternally inherited sensitivity.
The dominant theory of personality is the ‘Big Five’
approach, which suggests that stable, long-term
patterns in behavioural proclivities can be summarized
along five dimensions: extraversion, neuroticism,
agreeableness, conscientiousness and openness
[39,40]. Neuroticism is associated with a variety of
deleterious traits such as an increased likelihood of
experiencing negative emotions such as fear, sadness,
anxiety and guilt [41]. High neuroticism is a strong
Downloaded from rstb.royalsocietypublishing.org on January 19, 2011
392
V. Curtis et al.
Disgust as an adaptive system
individual learning (4c)
disgust (4)
(trait (4a)/
state (4b))
individual
motivation (5a)
hygiene
behaviour
(5)
social learning (4d)
public
health
(6b)
natural
selection
manners (7b)
extension (6c)
brain
imitation (5b)
culture
(7)
pathogens
aggregation (6a)
predispositions (7a)
natural
selection
group
hygiene
(6)
group
behaviour
Figure 2. The disease avoidance adaptive system.
predictor of psychiatric disorder in general, particularly depression [42], and is also associated with
impaired physical health, presumably through chronic
activation of stress mechanisms [43]. However, the
reason for the persistence of such an apparently maladaptive personality trait may be that it helped to
reduce the risk of predation and accidents in dangerous ancestral environments [44]. Given that there is
covariance between neuroticism and disgust sensitivity
scores [45] and that parasites were one of the biggest
dangers in ancestral environments, it is probable that
disgust sensitivity is, in fact, a component of the
neuroticism trait. Indeed many animals display stable
‘personality’ traits [46,47]. For example, it has
been shown that shy sunfish (Lepomis gibbosus) carry
different types of parasite from bold sunfish, presumably because the differences in their behaviour mean
that they are exposed to different levels of parasite
risk [47].
Malfunctions of the disgust system can be seen as
extreme trait variation. For example, some forms of
obsessive compulsive disorder are thought to be related
to excessive disgust sensitivity [48], while those with a
genetic predisposition to Huntingdon’s disease have
been shown to have lower levels of disgust [49].
Men and women have recurrently experienced
different costs of pathogen exposure. Disgust sensitivity varies consistently between males and
females, with females consistently scoring substantially
higher on measures of disgust sensitivity than males
[10,27,50]. We hypothesized that this trait difference
reflects women’s differing history of responsibility
for childcare [11]. Women, in effect, need to be disgusted enough for two people if they are to keep
their dependent children free of disease.
Phil. Trans. R. Soc. B (2011)
(b) State variation in disgust sensitivity
While individuals are born with varying disgust sensitivity traits (which may or may not be adaptive in
current environments), there are also adaptive advantages to being able to modify one’s disgust sensitivity
according to one’s current physiological state. There
are times when one may be more vulnerable to pathogens; upregulating disgust sensitivity and hence
concern for hygiene may thus be adaptive. Equally,
there may be states in which it is advantageous to
lower one’s disgust sensitivity—when hungry or short
of suitable mates, for example.
When physiological immunity is compromised, the
probable costs of infection are greater and disgust sensitivity should increase. This interaction between
physiological immunity and the behavioural immune
system has been termed the ‘compensatory prophylaxis hypothesis’ by Fessler & Navarrete [51]. In one
recent study, participants who reported more frequent
infections had both higher disgust sensitivity and more
ruminations about contamination and disease [52].
Women undergo adaptive immunosuppression after
ovulation and during the first trimester of pregnancy
in order for the maternal immune system to be able
to tolerate the paternal genetic material in the blastocyst. Fessler et al. found s…
Purchase answer to see full
attachment