Domestication as a Model of Speciation
50 years long experiment, run in the Institute of Cytology and Genetics
Biology. Summer School 2007 Novosibirsk
Marina VoloshinaPhys-Math School, Novosibirsk State University, 2007
http://www.slideshare.net/outdoors
This is an educational lecture for
students –
an overview of an experiment
conducted by scientists of Novosibirsk
Institute of Cytology and Genetics
and its evolutionary implications
Evolution – changes in genetic programs
What kind of changes leads to speciation?
Our subject today:
The genetic background of evolution
Domestication of animals is a long-scale
process, which began in prehistoric times
Pet or tool? Man walks a dog many thousands years ago
http://www.kamat.com/kalranga/rockpain/betaka.htm
Rock Painting, Madhya Pradesh, India ~ 12 000 years old
Our assistants
And pets
Domestication is a result of
artificial selection, which, opposite to
natural selection, is carried out by man.
Actually, there is no real opposition between
these two kinds of selection – even Charles
Darwin began his classical work with
amazing examples of variation in domestic
animals, caused by man.
Darwin’s example of artificial selection – pigeons breeds
Darwin considered the man’s job on
changing animal’s phenotype and behavior
as a model of what nature can do.
And as any model it can help us to
understand the mechanisms of evolutionmechanisms of evolution –
the basic process of life history.
The problem is that prehistoric people had
not bothered of making detailed scientific
records for us.
In 1959 a group of Siberian scientists, headed
by academician Dmitry K. Belyaev, the
Director of the Institute of Cytology and
Genetics in Novosibirsk, started a large-scale
experiment on fox domestication.
It lasts ~ 50 years It lasts ~ 50 years
by nowby now
Institute of Cytology and Genetics, Novosibirsk, Academgorodok
Academician Dmitry Belyaev1917 - 1985
Belyaev’s collaborator.
Guides this experiment
now
Dr. Ludmila Trut
It means:
The individuals differ by fitness – the most
adopted have more chances to survive and
to produce offspring
hence – to pass their genes to future
generations
The basic mechanism of evolution is
natural selection
Charles Darwin
Depending on particularDepending on particular phenotypes it favors, theit favors, the natural selection has has severalseveral types.
The universality of these three patterns is based on some assumptions:
1. The object for selection is some phenotypic trait
2. All traits are equal for selection – any of them can fall under selection pressure and change in similar way
3. The phenotype variation, which is a raw material for selection, is just a manifestation of pre-existing genetic variation, produced by mutation process
The real evolution is more complicated. Selection never affect one character only. Because an organism is by no way a mechanical combination of traits, but a highly integrative system
The proteins and cells interact in the ontogenesis (individual development)
This process has hierarchy – some genes and gene complexes (the master genes) rule and control other genes activity.
The highest integrative levels in animals are nerve and hormonal regulation
From this point of view traits become not
equal
Even slight changes in the regulatory
genes can give rise to a wide network of
changes in the developmental processes
they govern.
In highly integrative systems even small
changes of one element can lead to an
avalanche-like events
Regulatory systems The systems make an organism develop
and function as a whole
1. Genes, controlling development
2. Hormones
3. Nerve system
The hormonal and nerve systems are also defined by genes!
Regulatory genes
Thus, selecting animals for behavior – the
top regulatory character, involving many
genes - may lead to other, far-reaching
changes in the animals’ development
It can cause destabilization of ontogenesis,
and by that means changing of many other
characters, which had not undergone direct
selection
The mystery of parallelism
These was in line with one of well-known and mysterious facts about domestication: a striking parallelism in the morphological changes
In a wide range of mammals – herbivores and predators, large and small – domestication seems to lead to strictly coincident forms
Character Domesticated species
appearance of dwarf and giant forms
all
piebald coat color all
wavy or curly hair sheep, poodles, donkeys, horses, pigs, goats, mice,
guinea pigs
rolled tails dogs, pigs
shortened tails, fewer vertebrae dogs, cats, sheep
floppy ears dogs, cats, pigs, sheep, goats, cattle
changes in reproductive cycle all except sheep
Can all these modifications be a consequence
of a change in one character – behavior ?
That was the idea of academician Belyaev,
when he started the domestication experiment
in 1959.
The fox domestication experiment
As experimental model was chosen a species taxonomically close to the dog, but never before domesticated: Vulpes vulpesVulpes vulpes, the silver fox, the silver fox
Belyaev began with 30 male and 100 female foxes, most of them from a commercial farm in Estonia
Foxes had been farmed since the beginning of XX-th century. The founding foxes were already tamer than their wild relatives
The only criterion for selection was tameness – friendly behavior towards human beings
Selection was strict: not more than 4 or 5 percent of male offspring and about 20 percent of female offspring have been allowed to breed
To ensure that their behavior is determined rather by genes, than by the environment, any training was excluded: the foxes spent their lives in cages and were allowed only brief contacts with humans
By behavior tests foxes were divided to 3 classes:
Class I – tame. Friendly toward experimenters,
wagging their tails and whining
Let themselves be petted and handled but show no emotionally friendly response
Class II – neutral
Class III – wild. Aggressive behavior
wild
To the 10th generation of selection 18 % of foxes became elite (best of the Class I).
Now days the elite foxes make about 80 %.
What distinguishes the domesticated foxes of the wild ones?
1. The first is the behavior
2. Behavior is strictly determined by hormones – and hormone level changed significantly too
3. The reproductive cycle regulated by hormones is very conservative in wild animals. Domestication shifted time of the normal breeding season and even made some animals capable for twice a year reproduction. (normally once)
4. More surprising were the morphological changes
The new morphological characters that are absent in wild animals but are quite common in dogs:
a loss of pigment in the coat color – “Star” mark on the forehead and piebald coat
floppy ears
rolled tails
shortened tails and legs
‘Star’ heterozygous
‘Star’ homozygous
Domesticated American mink
Floppy ears
Floppy ears in cats – Scottish-fold
Tails curled upwards
Shortened tail and legs
Questions and answers
Why the changes involved so many traits
whereas animals were selected for
behavior only?
Why the changes are so similar in animals
of various systematic groups, domesticated
by different people at different times in
different parts of the world?
Nikolay Vavilov in 1930-th explained the
phenomenon of homologous variability (parallelism) by gene homology in species of one lineage
Similar genes produce
similar mutations
Similar mutant phenotype
But the frequency of aberrant phenotypes in the population selected for behavior is 10-2 - 10-3. which is 2 or 3 orders higher than the average frequency of spontaneous mutations
This contradicts to mutational explanation of all observed aberrations
In some foxes several different aberrations appeared simultaneously – which is statistically impossible if mutations at structural loci are the cause of these changes
The answer of Belyaev was that the key is the selection for behavior.
He considered the genetic transformations of behavior to be the main factor entraining other genetic events.
Many of the genes determining behavior may be regulatory, engaged in stabilizing an organism’s early development, or ontogenesis.
Ontogenesis is an extremely delicate process. In principle, even slight shifts in the sequence of events could throw it into chaos. Thus the genes that orchestrate those events and keep them on track have a powerful role to play.
The leading role among genes stabilizing an organism’s development belongs to the genes that control the neural and endocrine systems
The same genes govern the systems that control an animal’s behavior, including its friendliness or hostility toward human beings.
So, selecting animals for behavior can fundamentally alter the development of an organism.
Gene networks rule the development of all traits in ontogeneses
Master genes in inductor cells
Membrane receprors’ genes
Regulatory genes
Srtucrural proteins’ genes
Most of the novel traits and other changes
in the foxes seem to result from shifts in the
rates of ontogenetic processes
in other words, from changes in the
timepoint of genes action
Floppy ears, for example, are characteristic
of newborn fox pups but become get carried
over to adulthood
The disintegration of regulatory mechanisms
can give chance to manifest to the
“sleeping” mutations, which are normally
blocked by these mechanisms
Recessive mutations can express like
dominant in the new hormonal state
It leads to the growth of variability of all
characters – psychic and morphological.
Belyaev’s Idea of Destabilizing Selection
1. Destabilizing Selection is a strong
directional selection by an integrative
character, that controls ontogenesis.
2. This type of selection provides wide genetic
variation by destroying the masking
regulatory mechanisms.
3. The idea explains the parallelism in
evolutionary changes of domesticated
animals of different taxonomic groups.
Indeed, if the regulatory mechanisms –
nerve and hormonal – are similar in all
Mammals, then destabilizing of them
would lead to similar phenotypic changes.
Belyaev’s Idea of Destabilizing Selection
Destabilizing Selection as a Model of Speciation
A puzzle of speciation is that species seem
to be stable for a long periods of time
And then suddenly (in geological time scale)
disappear (in case of extinction) or transform
to a new species.
Thus, speciation is relatively fast process
(hundreds - thousands generations) in
comparison with species continuance.
Stasis, Extinction and Speciation
Species stability is maintained by stabilizing selection
Ivan Shmalgauzen 1884 - 1963
It provides It provides genetic
homeostasis. .
All genes act in All genes act in
coordinatecoordinate way, resulting way, resulting
in in normal development
But stabilizing selection is effective in
stable environment only
If environment abruptly changes – the
average fitness of population falls
dramatically and directional selection
for previously rare phenotypes began
These extreme phenotypes may be
not balanced with other genes –
because synchronizing gene orchestra
takes time.
The population enters the period of
instability.
new equilibrium.new equilibrium. extinction.extinction.
This model of speciation was put forward by Stephen Jay Gould in 1970-th
Punctuated Equilibrium Theory of Speciation
This theory strongly resembles
processes observed in domestication
Of course, natural selection, leading to
speciation should not always affect
behavior
Selection may act on any regulatory
chain
For example, strict change of environment can provoke stress – intensive emotional pressure.
Stress leads to long-time hormonal
changes and selection for stress-
resistance genes – regulatory kind
of genes, like genes of behavior
The recent results from molecular study
of genomes come in line with this view on
speciation
They revealed that most of general
changes in organism’s structure are result
of changes in gene regulation, their
spatial and temporal pattern of
expression, rather than direct changes in
their DNA sequence
Regulatory evolution at the yellow gene underlies
the wing pigmenation of Drosophilidae
Staining for yellow protein
D.melanogaster
D. biarmipes
D. guttifera
Wings
Domestic Animals: Parallelism in Color
Humans and dogs – convergent evolution?
http://email.eva.mpg.de/~tomas/pdf/Hare_Tomasello05.pdf
Implications of Domestication Mechanisms for Human Cognitive Evolution
This recent comparative work suggests that human-like social intelligence could initially have evolved, not as an adaptation,
but rather as a by-product of selection on social-emotional systems –
perhaps supported primarily by limbic and endocrine systems rather than the neocortex
Wikipedia article http://en.wikipedia.org/wiki/Tame_Silver_Fox
Links
Lyudmila Trut. Early Canid Domestication: The Farm-Fox Experiment http://www.americanscientist.org/my_amsci/restricted.aspx?act=pdf&id=3038739723681
Website of the Cornell University on the collaboration work with the Institute of Cytology and Genetics, Novosibirsk http://cbsu.tc.cornell.edu/ccgr/behaviour/Index.htm
What Can Dogs And Silver Foxes Tell Us About Each Other? http://cbsu.tc.cornell.edu/ccgr/behaviour/04_Recent_Publications/FoxChapter.pdf
B.Hare and Michael Tomasello. Human-like social scills in dogs? http://email.eva.mpg.de/~tomas/pdf/Hare_Tomasello05.pdf
Copyright notice
This is an educational presentation, based on works of D.K. Belyaev and L.N.Trut of the Institute of Cytology and Genetics.
You can use it in education with the links to original works.
Any commercial use is prohibited.
You have no right to place it on any website or portal for download.
Marina Voloshina
http://www.slideshare.net/outdoors
http://biologii.net