Journal of the History of Biology

https://doi.org/10.1007/s10739-019-9555-1

REVIEW ESSAY

The Domestication of Animals and the Roots

of the Anthropocene
Lee Ann Dugatkin and Lyudmila Trut, How To Tame a Fox (and Build
a Dog): Visionary Scientists and a Siberian Tale of Jump-Started
Evolution (Chicago: University of Chicago Press, 2017), viii + 216 pp.,
16 color illus., $26.00 Cloth, ISBN: 9780226444185

Richard C. Francis, Domesticated: Evolution in a Man-Made World

(New York: W. W. Norton, 2015), xii + 484 pp., 74 b&w illus., $17.95
Paperback, ISBN: 9780393353037

Pat Shipman, The Invaders: How Humans and Their Dogs Drove

Neanderthals to Extinction (Cambridge: Belknap Press of Harvard
University Press, 2015), xvi + 266 pp., 23 b&w illus., $29.95 Cloth, ISBN:
9780674736764, $18.95 Paperback, ISBN: 9780674975415

William T. Lynch1

© Springer Nature B.V. 2019

Books on animal domestication might seem to be naturally targeted to dog or cat fan-
ciers, or at best to specialists on the origins of agriculture. The books under review
suggest a broader interest in the topic. Themes that would interest historians of biol-
ogy include animal domestication’s relevance for engaging debates in evolutionary
biology over rapid evolutionary change and the possibilities of an extended evolu-
tionary synthesis, as well as understanding the “Big History” behind the human rise
to dominance over other species and the transformation of the environment begun
during the Upper Paleolithic and early Neolithic. On this view, the first stage of the
now trendy topic of the Anthropocene might have involved the domestication of the
dog, initiating the transformation of the niches of other animals as the result of the
rapid cultural evolution of a new kind of primate. At the center of these discussions
is the history of a remarkable, half-century long experiment breeding tame foxes.
With the power of Lysenko at its apex in Stalin’s Soviet Union in the 1950s,
geneticist Dmitri Belyaev first conceived the experiment, which he carried out

* William T. Lynch
william.lynch@wayne.edu
1
Department of History, Wayne State University, 3094 FAB, 656 W. Kirby, Detroit, MI 48202,
USA

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 W. T. Lynch

following Stalin’s death and the retreat of Lysenko’s power. The experiment contin-
ues to this day and produced a domesticated form of fox by selective breeding for a
single behavioral trait. He sought to test his hypothesis that selection for tameness
drove domestication. Other characteristics of the domesticated phenotype such as
shortened muzzles, mottled fur, curly tails, and floppy ears emerged as the byprod-
uct of selection for tameness. He worked with silver foxes from the fur trade, a
choice based on their taxonomic closeness to wolves. Belyaev bred the most tame
foxes together over generations and found that the animals not only became increas-
ingly friendly, but their appearance and behavior changed to resemble a dog.
While the experiment involved selective breeding, its significance is the sugges-
tion that the human role in early domestication was merely to accept tame animals
near human settlements and drive away or kill aggressive animals. All the rest of
the characteristics emerging as domesticated animals differentiated themselves from
their wild ancestors resulted from this premium on getting along with humans. As
such, the experiment challenged the idea that domesticated animals emerged as the
result of conscious intervention by humans in the process of animal breeding, at
least before later development of specialized breeds. This “unconscious selection,”
following Darwin (1859/2003, pp. 116–18), might be seen as initiated by would-
be domesticates themselves and reflecting ordinary natural selection in new niches
opened up by human camps and settlements.
While Belyaev directed the experiment from the Institute of Cytology and Genet-
ics in Novosibirsk, Siberia, the hands-on management of the fox breeding and the
testing for tameness was carried out by Lyudmila Trut, then a graduate student,
beginning in 1959 initially at a fox farm at Lesnoi, a 225-mile train ride away from
Novosibirsk. A closer location just outside Novosibirsk was established in 1967,
which allowed Belyaev to visit the foxes more frequently, often with visiting scien-
tists curious about the project.
Trut took over as director of the project following Belyaev’s death in 1985 and
continues to oversee the project today as it reaches fifty-seven generations and
counting. Trut has now written a fascinating and moving book on the experiment in
collaboration with evolutionary biologist and historian of science Lee Alan Dugat-
kin. Tracing the conceptualization, execution, and reception of the experiment, they
describe the emergence after only a few generations of a bond between human work-
ers at the farm and the foxes despite the fact that the foxes remained confined to their
cages.
Belyaev insisted that the foxes be treated the same as foxes raised for fur since he
was at pains to show that behavioral changes resulted from genetic breeding rather
than Pavlovian conditioning resulting from training or familiarity with human care-
takers. New behavioral traits emerged nonetheless. By the fourth generation, a fox
pup wagged its tail at Trut’s approach, while the sixth generation’s pups engaged in
solicitous behavior at the approach of humans, including whining, nuzzling, roll-
ing on their backs, and licking. In addition to their receptivity to humans, the foxes
retained a more playful orientation longer, suggesting that neoteny was playing a
role in slowing development. At the same time, many vixens began to breed sooner
and more frequently than wild foxes, which also echoed the enhanced fertility of
many domesticated animals.

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The Domestication of Animals and the Roots of the Anthropocene

Belyaev theorized that hormonal production, which was tightly regulated in the
wild, was being disrupted by selection for tameness and year-round availability of
food, bringing about what he called destabilizing selection (p. 61). In this, Dugat-
kin and Trut see Belyaev as anticipating recent emphasis on epigenetic regulation
of gene expression. Belyaev and Trut set up a control population of wild foxes, as
well as an aggressive breed, and began to document differences in stress hormones
between controls, aggressives, and the domesticated “elite” that displayed the full
range of domesticated behaviors.
With the tenth generation in 1969, foxes with floppy ears and piebald fur emerged,
further underscoring Belyaev’s contention that there were common genetic causes of
behavioral and physiological changes. Only by 1969 had Belyaev started publishing
his results in English in international journals. Dugatkin and Trut trace effectively
the growing international reputation of Belyaev and the fox experiment. In 1971,
Belyaev presented at the International Ethological Conference at Edinburgh, extend-
ing his impact beyond genetics.
Linking behavior to genetic causes remained a goal of the experiment, something
Trut delivered by the first decade of the new century after severe financial problems
nearly shut down the program. In collaboration with Anna Kukekova, a Russian
born geneticist then at Cornell University, she mapped 335 genes with dramatically
different protein expression between aggressive and tame foxes. Belyaev’s hypoth-
esis that all the characteristic traits common to most domesticated animals reflect
byproducts of selection for tameness seem to be borne out by recent work connect-
ing the “domestication syndrome” to alteration of neural crest cells distributed to
different parts of the body during development (Wilkins et al. 2014).
In Richard C. Francis’ comprehensive new book on domesticated animals, Bely-
aev’s work on foxes and theoretical ideas about destabilizing selection provide the
theoretical context for the book. The first chapter on Belyaev’s “house foxes”—some
of which were indeed eventually let out of the cage and into the house as pets—lays
out an up-to-date framework for understanding domestication, followed by chap-
ters on dogs, cats, pigs, and assorted grazing herbivores domesticated following the
development of agriculture, as humans looked to manage wild prey populations. To
understand how such a similar domesticated phenotype could emerge in a variety
of mammal species, Francis draws attention to homologies due to common descent
and to “phylogenetic inertia” (p. 98) for such convergent evolution, rather than a pre-
dominant emphasis on the forces of similar environmental pressures by themselves.
In doing so, Francis explicitly brings the extended evolutionary synthesis to bear
on domestication studies, drawing on Evo-Devo’s emphasis on regulatory constraint
and genomics’ demonstration that the basic forms of biological classes are con-
served, with new adaptations tinkering on the edges. He explicitly challenges Rich-
ard Dawkins’ emphasis on the power of adaptation driven by new environmental
pressures, substituting an emphasis on the constraints imposed by long-lasting line-
ages in reconsidering Dawkins’ tale of the leafy sea dragon. The moral of the tale
for Dawkins was that “animal shapes are malleable like plasticine” as “required for
its way of life” (Dawkins 2004, p. 331).
The remarkable camouflage of the leafy sea dragon is not driven all at once by
the need for this largely immobile creature to blend in with kelp to avoid predation,

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 W. T. Lynch

but by the constraints of the Syngnathidae family of sea horses, sea dragons, and
pipefishes set up 50 million years ago (see also Smith et al. 1985; Goodwin 1994;
Kirschner and Gerhart 2005). All members of the family lack the scales that facili-
tate fluid movement through the water, in keeping with a shared sedentary lifestyle.
The developmental pathways that lead to scales in other fish have been altered in
Syngnathidae to produce ring-like segments made of dermal bone that are better
suited for producing structures from collagen that can, and often do, serve as camou-
flage in other members of the family.
What does this have to do with domesticated animals? The common features of
domesticated mammals can come about only because they exploit features common
to the mammal class as a whole.
The domesticated phenotype is a form of convergent evolution that occurs in
human–environments and only human–environments. While the human envi-
ronment is necessary for the evolution of the domesticated phenotype, the
domestic phenotype would not emerge in such diverse species were it not for
certain key homologies shared by all mammals through descent from a com-
mon ancestor (p. 101).
Some of the key differences between mammals and other animals provide the basic
tune from which domestication riffs, as evidenced by shared mammalian hair, milk,
endocrine system, and limbic system. Hair facilitates higher body temperatures and
activity levels, while milk allows greater maternal investment in offspring, potentiat-
ing social learning depending upon the length of the juvenile stage. The hypotha-
lamic–pituitary–adrenal (HPA) axis provides the basic stress response, and the lim-
bic system the emotions, each of which are further tweaked to mesh with the human
environment during domestication.
It is the preexisting variability of the mammalian heritage that is exploited in
domesticated animals to facilitate this peculiar, if not completely unprecedented,
form of interspecies cooperation (Diamond 1998). Francis also makes the argument
that humans may well have domesticated themselves in the process of developing
high levels of social cooperation and “tameness” over time. Indeed, since gener-
ally speaking the early stages of domestication are driven by natural selection in
human environments, much the same kind of process seems to be at work in human
self-domestication.
This helps counter the paradoxical, or merely metaphorical, quality of the human
self-domestication argument and puts the emphasis on human alterations to the envi-
ronment that ultimately drove us away from being niche foragers to the keystone
species par excellence (contrast Shephard 1996). It is our unprecedented levels of
group cooperation that have in turn created the possibility for our significant altera-
tion of worldwide ecosystems, through technology and by facilitating the emergence
of domestic animals and the displacement of many wild species. In effect, human
self-domestication made animal and plant domestication possible, which in turn set
the stage for the emergence of the new human-dominated geological epoch known
as the Anthropocene.
It is on the question of the Anthropocene that Pat Shipman weighs in with an
intriguing speculation on the connection that the domestication of dogs may have

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The Domestication of Animals and the Roots of the Anthropocene

had in facilitating the extinction of megafauna with the spread of modern humans.
Scientists have recently considered various dates for a proposed Anthropocene, the
geological epoch beginning when humans decisively impacted the earth’s geol-
ogy, climate, and ecosystems. Working backwards, some attribute the period to
mid-twentieth century impacts, as humans began to equal nature in moving sedi-
ment around, mining minerals, altering climate, and introducing new archaeologi-
cal strata, whether of chicken bones or nuclear isotopes (McNeill 2000). Alterna-
tively, the invention of the steam engine and the rise of the industrial revolution can
be seen as the crucial transition, bringing about climate change, pollution, and the
intensified exploitation of resources (Crutzen 2002). Finally, it is possible to view
the Anthropocene as a replacement for the Holocene as a whole, with the invention
of agriculture radically transforming biodiversity and perhaps already forestalling
a return to ice age conditions via carbon emissions from deforestation and artificial
rice paddies (Ruddiman 2005).
Shipman favors an early date for the Anthropocene by dint of the fact that the
period saw the existence of only one remaining hominin, with the distinctive abil-
ity to transform the environment through rapid technological innovation. The roots
of the Anthropocene, in other words, lie in the displacement of Neanderthals and
other top predators in Eurasia. Indeed, roughly two-thirds of her book charts the
impact that immigrant Homo sapiens had in displacing the existing predator guild
that included cave bears, cave lions, saber-toothed cats, leopards, cave hyenas, and
Neanderthals. Situating her work within the context of invasion biology, as well as
recent methodological criticisms of the carbon-dating of Neanderthal archaeological
sites, she argues that the Neanderthals were largely extinct by 40,000 BP, not 26,000
BP as generally alleged.
While climate change may have played a role in the Neanderthal retreat, it did so
largely through the creation of open grasslands unsuitable for the ambush hunting
of Neanderthals with their thrusting spears. By contrast, modern humans were able
to use long-distance weapons that served as “niche-broadening technology” (p. 57,
quoting John Shea) in pursuing herbivores over open steppe. Modern humans were
able to hunt larger animals, including adult mammoths generally beyond the ability
of Neanderthals to kill. At the same time, modern humans employed “cultural buff-
ering” (p. 124) to keep their metabolic needs lower via fitted, sewed clothing and
superior hearths and shelters compared to Neanderthals.
Crucially, Shipman points to evidence that Homo sapiens not only outcompeted
other predators in killing more large prey, but they were able to retain control of the
carcass, keeping away other predators who would otherwise fight over the scraps. At
mammoth “megasites” (p. 158) dating to almost 40,000 BP, settlements show evi-
dence of many adult mammoth remains, with little evidence of scavenging by other
predators, but with extensive processing areas for butchering, storing, and tool-mak-
ing. Perhaps this was the first sign that other creatures might survive only by the
indulgence of humans, who found they could exploit every bit of a carcass for food,
fur, hides, and shelters.
This protection of human settlements and property was facilitated by the
transformation of the wolf, the other surviving large predator of the period, into
the domesticated watch dog and hunting companion. Just as Shipman argues

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 W. T. Lynch

that recent evidence pushes back the Neanderthal extinction dates by as much
as 15,000  years, her argument also depends upon pushing back the date of dog
domestication. She relies on recent statistical techniques for distinguishing wolf
and dog skulls developed by Mietje Germonpré. The methodology suggests a
skull from 32,000 BP was that of a dog, pushing back the date of domestication
by 18,000  years or so. With the new dating decreasing the gap between fossil
finds and molecular clock studies, which had initially suggested divergence as old
as 100,000  years ago (Morey 2010, pp. 50–53), Shipman is able to build a cir-
cumstantial case that dogs aided modern humans in their rise to dominance well
before sedentary and agricultural society emerged.
In her view, the newly emerging dog lineage, or “wolf-dogs” (pp. 171–172),
helped secure camps at mammoth kill sites, warning and protecting against out-
side predators and aiding human hunters in tracking and killing prey. In this
sense, they were “living tools” (p. 197) every bit as important to human success
as atlatls and bows and arrows. She also points to evidence that wolves were the
last members of the predator guild to be displaced by humans, perhaps as the
result of the tendency of wolves to fight other canids over territory, which forced
the hand of the wolf-dogs’ new human companions. The origins of what Shahid
Naeem calls the “domesticated kingdom,” where species survive preferentially
only if allied with humans, traces to dog domestication at the height of behavioral
modernity and sets the stage for the Anthropocene (Naeem 2009; Naeem et  al.
2012). The resulting transformation of planetary biodiversity to favor domesti-
cated plants and animals, human commensals, and simplified ecological systems
might better be designated the Homogenocene (Mann 2011, pp. 25–26).
What remains to elucidate is why certain animals were capable of being
domesticated in the first place. Francis argues that suitability for domestica-
tion reflected the prior existence of genetic variability in the ancestor species.
However, this variability was often “cryptic genetic variation,” since epigenetic
mechanisms suppressed the phenotypic effects of mutations in the normal course
of development, which could reemerge during moments of extreme environmen-
tal change to “be exposed for subsequent selection” (p. 16). Drawing on Ivan
Schmalhausen’s concept of stabilizing selection, Belyaev had seen domestication
as an extreme form of destabilizing selection. In periods of environmental stress,
destabilizing selection could explain how rapid development of tameness and
byproduct effects could take place.
Most domesticated animals that emerged with agriculture were herbivores with
strong dominance hierarchies that could be exploited by the new human alpha, who
began to herd and ultimately corral their wild prey. Even here, such human man-
agement probably depended upon a period of tameness brought on by commensal-
ism. Among domesticates, dogs and cats were exceptional in being predators. With
the case now made by Shipman that dogs were much older than agriculture, and
with cats seen by Francis as largely self-domesticated, as the result of inhabiting
human settlements (see also Driscoll et al. 2009), the common denominator for all
domesticated animals is significant human ecological disruption. This disruption
was brought about by new, rapidly changing cultural practices, whether extractive
mammoth hunting, sedentary foraging, or agricultural civilization. The thriving of a

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The Domestication of Animals and the Roots of the Anthropocene

few species suitable for domestication is the flip side of the disruption of ecologies
brought about by our species for the last 40,000 years or so.
What is it about our species that brought about such momentous changes, unique
even for the hominin lineage? Francis, again on a path paved by Belyaev, suggests
that humans were the first domesticated animals, having domesticated themselves
not only by facilitating “tameness” or “ultrasociality” among human groups (Camp-
bell 1983; Tomasello 2014; Turchin 2016), but by so altering the environment they
lived in as to bring niche construction to a new level (Odling-Smee et  al. 2003).
Francis considers and dismisses distinctly biological changes for the emergence of
behavioral modernity within our species, since candidate mutations in language
genes like FOXP2 do not differ from allegedly non-behaviorally modern Neander-
thals and Denisovians.
Francis considers cultural evolution the true driver of behavioral modernity and
human self-domestication as evidenced by practices like herding dairy animals,
which shaped biological evolution in the form of lactose tolerance, or cooking,
which shaped the increased size of the human brain. On his view, gene-culture coev-
olution would be better termed “culturally driven biological evolution” (p. 310). In
this emphasis on cultural evolution as a driving force, Francis differs from Shipman,
who had already staked her ground with defense of the biological reality of human
racial differences (Shipman 1994).
Just as domestication does not begin from artificial selection, but from natural
selection for tameness among human commensals, so too human self-domestica-
tion is understood as an “adaptation to the human cultural environment” (p. 312).
In direct opposition to evolutionary psychology’s modular and mutational view of
human language evolution, Francis, drawing on Dor and Jablonka (2001) and the
Baldwin effect, argues that language emerged as biological adaptations to human
cultural practices (see also Dor 2015). Cultural practices provided the environments
that in turn selected for biological traits that facilitated success in them (compare
Henrich 2016).
A corollary is that the emergence of cultural evolution as a new evolutionary
transition in nature is what ultimately drives the emergence of the Anthropocene
itself (Smith and Szathmáry 1995). Francis argues that until the past few centuries,
domestication was driven less by explicit artificial breeding than “garden-variety
natural selection” (p. 319) adapting to the human niche. Students of plant domestica-
tion are finding something similar, arguing that “[t]he domestication process appears
driven largely by unconscious selection pressures and is in principle simply natural
selection in the novel environments established by human agriculture” (Purugganan
and Fuller 2011, p. 181).
In this sense, human commensals are the first stage of animal domestication, lead-
ing to behavioral changes for animals like raccoons who have come to tolerate (or
ignore) humans and cooperate with each other when food sources are concentrated.
In this case, raccoons may be exploiting greater levels of phenotypic plasticity and
may never transition to genetic assimilation of tameness associated with domestica-
tion, as for instance ferrets seem to have done. However, Francis sees this capacity
for behavioral flexibility as a necessary first step for domestication that favors the
(potentially) fearless.

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 W. T. Lynch

What has changed dramatically during the “long Anthropocene” is the expansion
of the human niche itself, which evolves and aggregates through cultural evolution
at a faster pace than biological evolution and increasingly transforms the biosphere
as a whole. The open question is whether the long-term result will be a stabilized,
human-controlled biosphere or societal and ecosystem collapse. When that first wolf
abandoned the call of the wild, was that the harbinger of the sixth mass extinction or
the new face of nature itself?

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