J Bioecon

https://doi.org/10.1007/s10818-017-9266-7

Fair is foul, and foul is fair: experimental evolutionary

studies of mismatch

Terence C. Burnham1 · John P. Phelan2

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Abstract We describe two types of experimental evolution studies of “mismatch” that

are relevant to economics. “Evolutionary mismatch” is the concept that an organism
can be importantly “out of sync” with its environment. In such cases, an organism may
choose an option that is inferior to a feasible alternative. Mainstream and behavioral
economics do not address the notion of evolutionary mismatch. We argue for an
empirical program on mismatch utilizing the methodology of experimental evolution.

Keywords Evolution · Natural selection · Preferences · Mismatch · Evolutionary

economics

1 Introduction

Fair is foul, and foul is fair:

Hover through the fog and filthy air.
—Shakespeare, Macbeth

One of the striking features of modern industrial life is that we crave many items
that are harmful, while loathing others that are beneficial. It seems that the witches
in Macbeth are describing today’s world: items that are fair seem foul to us, and vice
versa.

B Terence C. Burnham
burnham@chapman.edu
John P. Phelan
jay@ucla.edu

1 Chapman University, Orange, CA, USA

2 Department of Life Sciences Core Education, UCLA, Los Angeles, CA 90095, USA

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Vaccines, for example, dramatically reduce human mortality and morbidity due
to infectious disease. And yet, even understanding the enormous positive impact
they have on human health does not change the fact that they can be unpleasant—
particularly when administered by injection. Conversely, imagine the foods that you
would love to consume. For most of us, the foods we crave would actually shorten our
lives if we consumed them regularly. This is a central puzzle in modern life: Why do
we love Big Macs and fear life-saving medical procedures?
Evolutionary mismatch is the answer to this puzzle. Over the course of hundreds
or even thousands of generations in a particular environment, a population typically
becomes well adapted to it (provided the environment doesn’t change too fast). Mis-
match is the phenomenon of a species living in an environment that differs from
the environment to which it is adapted (Bowlby 1969; Burnham and Phelan 2000;
Burnham 2016).
Mismatch can occur for numerous reasons: moving animals into a zoo or domes-
ticating them, for example, or developing through culture various methods of rapidly
altering the environment. When mismatch occurs, many of organisms’ instincts—
such as to consume large amounts of food when it is available—will no longer be
appropriate. As a consequence, many people, zoo animals, and pets are overweight.
Previously, we have advocated using experimental evolution to study economic
preferences (Burnham et al. 2015). This article has three sections. First, an abbrevi-
ated version of the economic mismatch framework from Burnham (2016). Second, a
taxonomy of economic mismatch experiments within that framework. Third, a discus-
sion of the potential impact of experimental evolution on economics.

1.1 A framework for mismatch and economic behavior

Becker (1976) wrote that preferences evolve to produce optimal behavior, “The pref-
erences taken as given by economists and vaguely attributed to ‘human nature’ or
something similar …may be largely explained by the selection over time of traits hav-
ing greater genetic fitness and survival value.” (p. 826). Subsequently, Hansson and
Stuart (1990) explored the implications of Becker’s insight concluding, “in very-long-
run equilibrium, utility mirrors fitness in the sense that marginal rates of substitution
equal analogously defined marginal rates of substitution in fitness.”
In this view, preferences evolve over evolutionary time so that the likes and dis-
likes are in sync with the biological payoffs. When in long-term equilibrium, humans
‘maximize utility’ by the process of choice as described in economics, and simul-
taneously these choices maximize reproductive success (a.k.a. biological ‘fitness’).
Table 1 (from Burnham 2016) summarizes an equilibrium view of preferences and the
reproductive payoff of associated behaviors.

Table 1 In equilibrium, preferences are aligned with reproductive consequences

Feels good (increases utility) Feels bad (decreases utility)

Increases fitness X
Decreases fitness X

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The physical, biochemical, and behavioral traits of many animals in the wild are
likely to be in equilibrium with their environment in a manner described in Table 1.
So much so that when some novel behavior is observed in a wild population, it can
stimulate a productive search for a reproductive benefit. Peahens, for example, tend
to choose peacocks with long and gaudy tails (Petrie et al. 1991). Why mate with a
male with a big, cumbersome tail? After all, predators are more likely to detect, and
out-maneuver, the big-tailed peacocks produced by such unions.
Zahavi (1975) speculated that, by surviving with a ‘handicap’, males with big
tails are sending an honest signal of their genetic quality. And in a set of ingenious
studies, this handicap hypothesis was confirmed. In the natural world, peahens choose
their mates (and favor those with long tails). In these experiments on the information
contained in a big tail, however, females did not get to choose their mates. Instead,
the experimenter randomized short-tailed mates for half the females, and long-tailed
mates for the other half.
The females that mated with long-tailed males had more offspring, and those off-
spring grew faster and were more likely to survive, than the offspring of short-tailed
males (Petrie and Williams 1993; Petrie 1994). Thus, the researchers conclude that a
big, gaudy tail is an honest signal of male genetic quality.
The relevance for this paper is that animals in equilibrium with their environment
are likely to be maximizing reproductive success, even if the route to maximization is
not obvious to human observers.
When animals are in evolutionarily novel environments, however, there is no reason
to assume that a behavior is maximizing anything. Indeed, we began our book Mean
Genes with a story about Chantek, an orangutan living in a zoo. In contrast to his lean
and healthy wild brethren, Chantek literally loved eating McDonald’s food. Like many
of us, Chantek suffered the consequences of living in a novel environment; he was
overweight and unhealthy. In another overlap with humans, Chantek became irritable
when the zookeepers placed him on a calorie-restricted diet.
Human genes have not had time to catch up with modern industrialized conditions.
Consequently, like zoo primates, we suffer from evolutionary mismatch. Table 2 (from
Burnham 2016) summarizes some speculation regarding modern inventions where
people derive pleasure from items that are bad for them and derive displeasure from
items that are good for them.

Table 2 In novel environments, being bad can feel good, and being good can feel bad

Feels good (increases utility) Feels bad (decreases utility)

Increases fitness Colonoscopy, dental visit,

Decreases fitness
saving money, college,
vaccines, bike
helmets,prudence
Crack cocaine, Big Mac, TV,
motorcycles, pizza, trans
fats, cigarettes

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The conclusion suggested from this perspective of evolutionary mismatch is almost

exactly the opposite of that embraced within standard economics. Standard economics
assumes that people will unconsciously and automatically make sophisticated choices
that simultaneously feel good in the short-term and are optimal in the long-term. In
sharp contrast, we have argued, and believe, that humans are out of sync with modern
environments in many significant ways. Humans are so out of sync with modern
industrialized settings, in fact, that a naive “do what feels good” approach to life often
leads to unhappiness and premature death.

2 Experimental evolution studies of mismatch

Experimental evolution is a powerful empirical method for investigating mismatch.

Two distinct approaches can illuminate aspects of mismatch: (1) create mismatch, and
(2) ameliorate mismatch.

1. Create mismatch
One set of possible experiments would create mismatch by altering the environment
in an engineered fashion. A central feature of such an experiment is to invert the
relationship between cues used by the organisms and the reproductive payoff.
One could add a toxin to a preferred food for a population, for example. In such a
case, it would be particularly interesting to use a toxin that could not be detected by
the organism. The initial populations would then face an extreme version of mismatch
where eating what was previously the “best” food, would lead to illness and/or death.
Enforcing this selection regime on multiple populations would make it possible
to document whether behavioral evolution away from the previously preferred food
occurs, and if so, numerous facts about that evolutionary change. Genotyping differ-
ent populations along their different evolutionary paths, for example, would make it
possible to quantify the variation in genotypic response to mismatch, to measure the
rate of evolution, and to characterize the different evolutionary paths taken by different
populations.

2. Ameliorate mismatch
In Mean Genes we identified three routes to reducing the negative impact of mismatch.
First, alter the organism in such a way that it comes to prefer the good item and not
prefer the bad item. “Fair becomes fair again.” Second, alter the environment, creating
a new option that is preferred to the bad item and is good for the organism. Third, alter
the environment, eliminating or reducing access to the bad item.
In humans, there are examples of successful mitigation of the negative effects of
mismatch via each of these routes. A nicotine vaccine, for example, aims to decrease
cigarette consumption by making smoking less enjoyable. This is a human example
of the first sort of intervention; the alternatives in the world remain constant, but the
organism is altered to make the negative item less enjoyable. With other organisms,
an even broader range of interventions is possible.
In the context of an experimental evolution program using non-human organisms,
more extreme interventions are possible including altering the genotype using the

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CRISPR gene-editing tool. In such a system, it would be possible to quantify the

impact on the intervention by measuring the associated behavioral changes.

3 Concluding thoughts

Humans living in modern industrial settings are out of equilibrium with respect to
numerous, important aspects of the environment. Moreover, the pace of technological
change is so rapid that there is no likelihood of returning to equilibrium. To the contrary,
our future is likely one of increasing mismatch. With the exception of a few fringe
papers, however, this concept of mismatch—with its many implications central to
human existence—is not considered by either mainstream or behavioral economics.
Experimental evolution allows the empirical study of economic mismatch. We
will be able to understand mismatch better if we can utilize controlled experimental
systems in which we create it and ameliorate it, while characterizing both phenotypic
and genotypic consequences of such interventions.

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