Breeding Belyaev’s Pets
Domestication, Evolution, and the Farm-Fox Experiment
by
J. Phil Gibson, University of Oklahoma
Learning Objectives
• Understand how artificial selection supports Darwin’s
Theory of Evolution by Natural Selection.
• Understand how artificial selection can change
characteristics of a breeding population.
• Investigate changes that occur in a lineage as a result
of domestication.
2
Clicker Question 1
Which of these forms of data did Darwin not
use in developing his Theory of Natural
Selection?
A. fossils
B. domesticated species
C. Mendelian genetics
D. structural homology
E. Darwin used all of these forms of data
3
Clicker Question 2
Domestication involves selectively breeding
for:
A. many separate, genetically-based traits specifically
chosen by the breeder.
B. genetically-based traits that arise at random due to the
species’ need for those traits.
C. some genetically-based traits and unpredictable changes
in other traits that were not specifically chosen.
D. genetically-based and environmentally caused traits.
4
Darwin’s Data
In addition to examples of
adaptation, structural homology,
the fossil record, and
biogeography, Darwin used
domesticated species as support
for his theory evolution.
Why do you think domesticated
species would be an important
part of his theory?
5
Darwin & Inheritance
Because Mendel’s work was not
yet known and discovery of DNA
and its function was over a century
in the future, domesticated species
provided Darwin’s only information
on heritable traits. Although he had
no direct knowledge of genetics,
Darwin understood that some
favorable traits could be passed
from parents to offspring.
6
Artificial Selection
Darwin knew changes could occur from observing
selective breeding of domesticated species. He
called this process Artificial Selection.
• What is domestication?
• How does domestication relate to artificial
selection?
• How could knowledge of domestication and
experience with plant and animal breeding be of
use as Darwin considered how evolution by
natural selection could work?
7
Artificial Selection
An avid pigeon breeder, Darwin knew that breeders
could change a species by choosing individuals with
interesting traits that occurred at random and by
allowing those individuals to breed. Over
generations, those traits become more common and
the population changes over time.
8
Darwin’s Observations
In addition to traits intentionally chosen by
breeders, Darwin noted this observation in The
Origin of Species
“. . . not a single domestic animal can be
named which has not in some country developed
drooping ears.”
9
Traits Common In Domesticated Species
Not only drooping ears, but also:
• piebald coloration, forehead star
• wavy hair
• rolled, shorter tails
• changes in reproductive cycles
What could this mean?
10
Wolves, Dogs, & Domestication
Dogs, the first domesticated animal species, were
domesticated from gray wolves in Southwest Asia
over 15,000 years ago.
Canis lupus
Canis lupus familiaris
11
Wolves, Dogs, & Domestication
• Morphologically, dogs and
wolves share a number of
traits because they are
canids.
• Genetically, they are 99.8%
similar in their mtDNA,
which strongly indicated
dogs were domesticated
from wolves. Wolves and
coyotes are only 96%
similar.
12
How Were Dogs Domesticated?
Different studies have investigated how dogs were
domesticated by early humans.
Current thinking suggests:
• Ancestral wolves that tended to tolerate humans would
have had the best access to high-quality food in human
trash piles. Those wolves would have protected their
scrap piles from other animals and may have provided
other benefits to humans.
• Humans may have then started to keep wolves and begin
breeding them. Maybe they artificially selected for
different traits. Over time this resulted in the animals we
now know as dogs.
13
Lingering Questions
Questions still remain about dogs in
particular and domestication in general
that have interested biologists for
many years.
1. What changes occur during
domestication?
2. How quickly could domestication
occur?
Dogs of King Antef from Egyptian
relief (2323 BC. to 2134 BC).
How would you investigate these
questions scientifically?
14
The Fox-Farm Experiment
In 1959, Dr. Dimitry K.
Belyaev, Director of the
Institute of Cytology and
Genetics in the U.S.S.R.,
began investigating the
genetics of dog
domestication by selectively
breeding another canine,
silver foxes, from local fur
production farms.
Vulpes vulpes
15
Clicker Question 3
Dr. Belyaev hypothesized that variation in tameness is linked
to genes. If so, artificial selection during domestication
should, therefore, change the frequency of tameness genes
in a fox population over time. How long do you think it will
take for a population to become “tame” or considered
domesticated?
A. Very quickly, just a few generations
B. Moderate time, a slow start but quickly after the first
generations of breeding.
C. Fairly slow, a gradual change over many generations.
16
A Farm-FoxExperiment
Suppose you had a fox farm with a large diverse
population of animals available for you to study.
• Design an experiment you would conduct to see if
you could “re-create” dog domestication and
investigate the genetics of tameness using foxes.
• What is your hypothesis and what would you
expect to observe? Explain.
• How would your experiment further our understanding of dog domestication? Domestication in
general?
17
The Farm-Fox Experiment
Belyaev’s Procedure
• Fox pups (called kits) from the population were
scored for tameness and assigned to classes:
– Class 3: flee or aggressive response to experimenter
– Class 2: allow petting but no emotional response to
experimenter
– Class 1: friendly to experimenter (wag tail, whine, etc.)
• Next, they bred the most friendly Class 1 foxes
(Elite Class 1 = E1) over many generations.
What specific changes would you expect to observe over
time as the experiment proceeded?
18
Farm-Fox Experiment Results
The number of E1 foxes increased in frequency
and showed significant increases in “dog-like”
behavior (docile, eager to please, lick hands,
compete for attention) in relatively few
generations.
(Trut, 1999)
Generation
% 1E Kits
10
18
20
35
35
70-80
19
Farm-Fox Experiment Results
But, there were other changes as well.
Generation
(Trut, 1999)
Observations
2
decreased aggressive response
4
tail wagging, petting allowed
6
friendly kits follow and lick humans
9
floppy ears, piebald fur, forehead star
appear
13
tail curls
15
shorter tail, fewer vertebrae
20
The Farm-Fox Experiment
Over relatively few generations, the foxes
displayed tremendous changes in behavior
and appearance. They were starting to look
and act like dogs! The researchers’ data was
showing how selection for a single characteristic was also related to a number of other
unselected traits. They could see clear
evidence of changes that could occur over
the course of domestication.
http://scienceblogs.com/thoughtfulanimal/2010/06/14/monday-pets-the-russian-fox-st/
http://www.gmilburn.ca/2009/03/20/clever-as-a-fox/
http://edauer.wordpress.com/tag/dmitry-belyaev/
http://www.nytimes.com/1999/03/30/science/new-breed-of-fox-as-tame-as-a-pussycat.html
http://doctorbarkman.blogspot.com/2013/04/belyaev-fox-farm-experiment.html
http://155.97.32.9/~bbenham/2510%20Spring%2009/Behavior%20Genetics/Farm-Fox%20Experiment.pdf
21
Farm-Fox Experiment Results
Characteristic
Undomesticated
Animals With
Trait
(per 100,000)
Star On Forehead
710
Mottled Fur
Coloration
86
Floppy Ears
170
Shortened Tail
Curled Tail
(Trut, 1999)
Domesticated
Animals With
Trait (Per
100,000)
Frequency
Increase
2
830
22
Farm-Fox Experiment Results
Characteristic
Undomesticated
Animals With
Trait
(per 100,000)
Domesticated
Animals With
Trait (Per
100,000)
Frequency
Increase
(%)
Star On Forehead
710
12,400
1,646
Mottled Fur
Coloration
86
450
423
Floppy Ears
170
230
35
2
140
6,900
830
9,400
1,033
Shortened Tail
Curled Tail
(Trut, 1999)
23
Clicker Question 4
The results so far indicate. . .
A.domestication is a slow process.
B.selecting on one trait can lead to changes in
another, unselected trait.
C.fox domestication has little to do with dog
domestication.
D.domestication proceeds by changing one trait at a
time.
E.None of the above.
24
Farm-Fox Experiment Data
In addition to appearance, other changes occurred. The time when different
maturation events occur in dogs and foxes are show below. Complete the figure for
when you think these events should occur in domesticated foxes.
DAYS
WEEKS
7 8 9 10 11 12 13 14 15 16 17 18 19
4 6 8 10 12
DOGS
WILD
FOXES
DOMESTICATED
FOXES
eyes fully open
(Trut, 1999)
response
to sound
window of
socialization
25
Farm-Fox Experiment Data
In addition to appearance, other changes occurred. The time when different
maturation events occur in dogs and foxes are show below. Complete the
figure for when you think these events should occur in domesticated foxes.
DAYS
WEEKS
7 8 9 10 11 12 13 14 15 16 17 18 19
4 6 8 10 12
DOGS
WILD
FOXES
DOMESTICATED
FOXES
eyes fully open
(Trut, 1999)
response
to sound
window of
socialization
26
Nature vs. Nurture
Although the researchers observed specific changes,
treating some kits differently could have changed their
behaviors. That would mean tameness is learned, or at
least influenced by environment, and not a heritable trait.
What experiment could the researchers do next to support
their conclusion that artificial selection for tameness has
produced an evolutionary change in the fox population?
27
Nature vs. Nurture
To determine whether tameness is a genetic or environmental
trait, researchers conducted two additional experiments.
• In one experiment, they bred for aggressive behavior in the
same way that they bred for tameness.
• In another experiment, they switched kits among mothers.
Kits from tame, E1 mothers were nursed by more
aggressive mothers. Likewise, kits from aggressive mothers
were nursed by tame, E1 mothers.
If tameness is genetically based, what do you expect will
happen in these two experiments?
How do these experiments provide a necessary follow-up to
the first experiment?
(Ratliff, 2011)
28
Clicker Question 5
If tameness is genetically based, what would you predict
would happen in a kit swapping experiment where an
aggressive kit was given to a tame mother?
A.The kit would become docile due to hormones in her
milk.
B.The kit would cause the docile mother to become
aggressive.
C.The kit would be more easily trained than if the
aggressive mother raised it.
D.The kit would mature to become an aggressive adult.
E.No predictions can be made because breeding is
unpredictable.
29
Clicker Question 6
As predicted, fox lineages bred for aggression
became more so. Comparisons of the docile and
aggressive foxes’ DNA identified genetic
differences at a number of different loci. This
indicates that . . .
A.domestication involves relatively few genes.
B.domestication affects genes for traits being
selected as well as other traits.
C.domestication changes only those traits selected.
D.domestication is basically the same as training an
animal to behave.
30
Farm-Fox Epilogue
Further genetic analysis of the aggressive and
domesticated silver fox lineages have identified
two regions that are distinct between them.
Studies of these regions and the genome of other
domesticated species will not only provide deeper
insights into the genetic changes caused by
domestication that can be applied to other
species, but may also provide insights into
changes that occurred in human evolution as well.
31
Other Studies
In addition to the work being done on foxes, other
researchers sequenced the full genomes of 12 wolves from
around the world, as well as 60 dogs representing 14 diverse
breeds. They searched for signatures of domestication by
looking for sequences that showed the greatest differences
between dogs and wolves, or for sequences that were
consistent across dog breeds but varied in wolves.
Why are these researchers taking this approach? What are
they expecting to find?
(Yong 2013)
32
Genetic Differences: Behavior
They identified 36 regions of the genome (122 genes) that
were completely different between dogs and wolves.
Eighteen of the regions contained genes affecting the
brain. Researchers think these may relate to less
aggressive behavior, improved social interactions, and less
fear of humans in dogs. Differences may also relate to
dogs’ ability to read human behavioral cues.
(Yong 2013)
33
Genetic Differences: Digestion
Differences in 6 other regions, containing 10 genes, are
involved in digesting fat and starch.
Dogs have extra copies of the gene for amylase, an intestinal
enzyme that cuts starch into maltose, and produce 28 times
more amylase than wolves.
Dogs also produce 12 times more maltase-glucoamylase, which
converts maltose into sugar, due to mutations in the gene for
this enzyme.
Mutations in a third gene, SGLT1, improved the function of a
protein that absorbs the sugar through the gut.
(Yong 2013)
34
Summarizing It All
The research described in this case study identified
genetic, behavioral, physiological, and anatomical
features of wild and domesticated canine lineages.
What are the most important conclusions that can be
drawn from this research?
What is the significance of these findings?
Summarize the results and their significance in either
one or two paragraphs or a clearly labeled diagram.
35
Deeper Thinking
You have rescued a puppy from a local animal shelter. As it
grows, you and your friends make different guesses
about what breeds its parents were.
One day you notice a web site that
announces it can tell you the
breeds of dog produced your
lovable mutt simply by sending
them a swab of the cells from the
inside of your puppy’s mouth.
Using accurate terminology, describe or diagram how this
company’s offer could possibly work.
36
Deeper Thinking
One of the great stories in biology is that Charles Darwin
had an unopened copy of Gregor Mendel’s manuscript
on his office. Apparently, Darwin never read it, and,
consequently, developed his theory of evolution with no
working knowledge of the mechanisms of Mendelian
inheritance.
Suppose he had read this manuscript, how would this have
affected his description of artificial selection? Natural
selection? Evolution?
37
Deeper Thinking
Darwin’s Theory of Evolution by
Natural Selection can be
summarized with the simple
acronym VISTA.
(Variation, Inheritance,
Selection, Time, Adaptation)
How does VISTA apply to the
Farm-Fox case study?
38
Acknowledgements
Development of this case study was supported by NSF
Grant No. DUE #0940835. Any opinions, findings,
conclusions, or recommendations expressed in this
material are those of the author and do not
necessarily reflect the views of NSF.
39
Image Credits
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Permission is granted to copy, distribute and/or modify this document under the terms of the GNU Free Documentation License,
Version 1.2 or any later version published by the Free Software Foundation; with no Invariant Sections, no Front-Cover Texts, and no
Back-Cover Texts.
Slide 5. http://commons.wikimedia.org/wiki/File:Charles_Darwin_aged_51.jpg This work is in the public domain in the United States
because it was published (or registered with the U.S. Copyright Office) before January 1, 1923.
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because it was published (or registered with the U.S. Copyright Office) before January 1, 1923.
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with no Invariant Sections, no Front-Cover Texts, and no Back-Cover Texts.
Droopy eared mutt Copyright © 2013 J. Phil Gibson.
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This file is licensed under the Creative Commons Attribution 2.0 Generic license. Attribution: Santiago Atienza
Border collie with balls Copyright © 2002 J. Phil Gibson
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Slide 36. Let the sleeping puppy lie. Copyright © 2013 J. Phil Gibson
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41