J Bioecon

https://doi.org/10.1007/s10818-017-9264-9

Domestication experiments reveal developmental link

between friendliness and cognition

Brian Hare1

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

Abstract The goal of economics is to understand human preferences. Most research

focuses on adult humans and does not take an evolutionary approach. In biology
experimental evolution has been able to shift the preferences of animals. As an exam-
ple, artificial selection for friendly behavior toward humans results in a syndrome
of changes that strongly resembles differences between wild and domestic animals.
These domestication experiments have revealed precise genetic and neurobiological
systems that are altered by the selection and linked through expanded windows of
development. Similar evolutionary experiments selecting for a range of social, risk
or discounting preferences could push economics toward consilience with biology.
Prospects for a unified theory of economic behavior would be drastically improved.

Keywords Domestication · Artificial selection · Prosociality · Social preferences ·

Decision making · Self domestication

Artificial selection played a central role in Darwin’s proposal of evolution through

natural selection. The opening chapter of the Origin of Species uses human led selection
to demonstrate how natural selection shapes wild populations (Darwin 1859). Darwin
went on to write two monographs chronicling the range of phenotypic variation that
exists in domestic animals (Darwin 1868). He used these books to bolster his claim
that sufficient variation exists as the raw material on which nonrandom selection acts.
Observing artificial selection and the variation humans base their breeding decisions
upon gave Darwin one of his most powerful tools in developing and testing his ideas
about natural selection (Browne 2011). Economics, as a science focused on human

B Brian Hare
apeminds@gmail.com

1 Duke University, Durham, NC, USA

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 B. Hare

preferences, could also explore the origins of our social preferences through artificial
selection experiments (Burnham 2017).
Today selection experiments are uncovering how proximate mechanisms evolve.
Instead of inferring a causal relationship between behavior and biology solely based
on natural observations, selection experiments allow you to cause heritable behav-
ioral change and study resulting phenotypic and genotypic consequences. This will
lead to far more predictive models of behavior. Experiments exploring the process of
domestication provide an example. Dimitry Belyaev hypothesized that animal domes-
tication is the result of selection for friendliness (Belyaev et al. 1985). For decades
he and his colleagues bred foxes based on whether they approached and interacted
with a human experimenter. They also maintained a control population that was bred
randomly in regards to how they interacted with people. After the first twenty genera-
tions, the experimental foxes had already become more prosocial toward humans than
the control foxes. This less aggressive temperament was accompanied by increases in
brain serotonin levels and reduced HPA responsiveness. A host of other features also
appeared at higher frequencies that were never under direct selection. As adults, the
experimental foxes maintain behaviors such as tail wagging, barking and whimpering
primarily observed in fox kits of the control population (Gogoleva et al. 2008). The
window during which the experimental foxes can be socialized to humans is wider
and their breeding season is months compared to weeks seen in the control population
(Plyusnina et al. 1991). The experimental population also shows a higher prevalence
of floppy ears, piebald coat coloration, shorter tails, curly tails, shortened muzzles,
more crowded teeth and white patches on their foreheads (Trut 1999; Trut et al. 2009).
Perhaps most surprisingly the experimental foxes are more skilled at reading human
gestures than the control line—a communicative skill that is crucial in human devel-
opment, but again was never directly selected for in the foxes (Hare et al. 2005).
Wilkins and colleagues proposed the neural crest hypothesis to explain the link
between behavior and other phenotypic traits discovered by Belyaev (Wilkins et al.
2014). They propose that individuals whose neural crest stem cells have less develop-
mental input show less aggression as well as a range of seemingly unrelated changes
because all the affected tissues are neural crest derivatives or influenced in their devel-
opment by the neural crest. Pluripotent stem cells originating from the neural crest
migrate from the neural tube and are involved in the formation of brain, skull, teeth,
cartilaginous structures, pigment-related melanoblasts in the head and trunk, and the
adrenal cortex (Wilkins et al. 2014). This provides a unified explanation for traits com-
monly observed in domestic animals that previously had been proposed to originate
due to a symphony of different selection pressures. Geneticists are now testing this and
other hypotheses by comparing the genetics and development of these experimentally
domestication animals (Albert et al. 2008, 2012; Theofanopoulou et al. 2017).
Beyleav’s selection experiments have provided a powerful model for thinking about
how selection for prosociality in nature may act similarly. Following the fox model,
Hare and colleagues have proposed the self-domestication hypothesis that predicts that
species shaped by selection for prosociality will show features of the domestication
syndrome observed in experimental populations (Hare et al. 2012). Comparing dogs to
wolves and bonobos to chimpanzees reveals behavioral, physiological and cognitive
differences predicted a priori by the self-domestication hypothesis (Hare 2017). These

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findings led to the inference that this phenotypic pattern or syndrome can act as a
signature of selection for prosociality (and against aggression) in natural populations.
Self-domestication is now being tested as a factor in explaining the island syndrome,
the recent invasion of urban areas by megafauna (i.e. coyotes, deer, etc.), and the
success of our own species over other humans in the Upper Paleolithic (Cieri et al.
2014; Hare 2017).
The foxes also provide a novel model for cognitive evolution. Most cognitive
hypotheses focus on the benefit of cognitive flexibility and assume variation in these
skills would be directly targeted by selection as a result of the fitness advantage they
confer (Maclean et al. 2012). This has led to the assumption, for instance, that domes-
ticated animals are dull or unintelligent since they rely so heavily on humans (Hare and
Woods 2013). In contrast, the self-domestication hypothesis suggests that cognitive
variation can be produced as another by-product of selection for prosocial prefer-
ences. This hypothesis was first suggested by the dog-like communicative ability of
the experimental foxes in reading human gestures—even though the foxes were not
selected for this skill (Hare and Tomasello 2005b). Further support has come from
comparisons revealing cognitive flexibility in domesticates not present in their wild
progenitors. Populations of domestic dogs (i.e. dingos and New Guinea singing dogs)
and domestic ferrets are also skilled at reading human gestures while wolves and wild
ferrets are not (Wobber et al. 2009; Smith and Litchfield 2010; Hernádi et al. 2012).
Domestic Bengalese finches are open-ended learners with far more complex songs
than the Munia from which it evolved (Kagawa et al. 2014). However, none of these
domestic populations was selected for their communicative abilities. These examples
suggest cognition can evolve as a by-product, but that the revealed variance in these
correlated traits can then become the target of selection (Hare and Tomasello 2005a;
Hare 2017). For example, the unusual communicative skills of working and herding
breeds of dogs have been hypothesized to be a product of artificial selection. Human
breeders intentionally targeted the variance in communicative abilities revealed by
self-domestication (Kaminski et al. 2004; Wobber and Hare 2009).
Belyaev’s work represents a starting point. Future experimental selection experi-
ments can be designed to explore a variety of complex phenotypic traits. Belyaev and
his colleagues selected foxes for breeding based on their response to a human, but
animal aggression can be classified in a variety of ways including offensive, defen-
sive, maternal, predatory, ingroup, outgroup, intraspecific, interspecific and more.
Populations of rodents can be selected based on variation in their responses in each
of these social contexts. It will then be possible to disentangle the interactions of
neurotransmitters, receptors and gene expression and their role in modulating each
form of aggression (Carre et al. 2011; Montoya et al. 2012). One hypothesis sug-
gests that selection for or against aggression of any form will affect neurobiology
similarly. In support of this hypothesis are experiments selecting against male-male
aggression in mice. After only a few generations of selection, adults in the exper-
imental line retain juvenile responses to social threat not seen in the control lines
but similar to mice selected to be less aggressive toward humans (Gariépy et al.
2001). This suggests selection against any form of aggression targets developmental
pathways to increase tolerance. The alternative suggests that different mechanisms
will be shaped differently depending on the form of aggression being selected.

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The domestication syndrome is not expressed uniformly across domestic species

(Sánchez-Villagra et al. 2016). This has been proposed to be a result of selection
affecting neurobiological systems differentially depending on the type of behaviors
being selected for or against (Hare 2017). A carefully orchestrated set of selection
experiments could provide a powerful way to test between these two hypotheses and
finally give neurobiologists a shortcut in their tasks of sorting out the relationships
between the alphabet soup of neurotransmitters, peptides and hormones (e.g. serotonin,
testosterone, oxytocin, vasopressin, dopamine, cortisol, etc.) that modulate different
forms of aggressive behavior. Genomic comparisons between selected and unselected
lines with known pedigrees also will provide a unique opportunity to identify with
improved resolution the network of developmental and genetic mechanisms shaped by
selection.

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