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