Postneodarwinistic Theories of

Evolution - From the Selfish Gene to Frozen Evolution

Jaroslav Flegr

Department of philosophy and history of science

Prague 2008

Outline

• Darwinisms, neodarwinisms and evolution of adaptive traits by means of natural selection

• Model of selfish gene – a theory of evolution of adaptive traits in sexual organisms

• Shortcomings of the theory of selfish gene– Context-dependent phenotypic expression of gene

(epistasis)– Context-dependent impact of biological trait on

biological fitness– Frequency dependent selection (ESS)

• Theory of frozen plasticity

Charles Darwin

Darwinistic explanation of the origin of adaptive traits

• An average number of offspring/parent > 1• Populations are stable in a long term• Therefore, only a fraction of the young survive and

reproduce• Organisms in populations differ • Probability of survival and reproduction (fitness)

depends on properties of an individual• Offspring inherit properties and fitness of their parents• Therefore, useful (adaptive) traits (structures and

behavioral patterns accumulate in populations

What is wrong with darwinistic theory of origin of adaptations?

• An average number of offspring/parent > 1• Populations are stable in a long term• Therefore, only a fraction of the young survive and

reproduce• Organisms in populations differ • Probability of survival and reproduction (fitness)

depends on properties of an individual• Offspring inherit properties and fitness of their parents• Therefore, useful (adaptive) traits (structures and

behavioral patterns accumulate in populations

What is wrong with darwinistic theory of origin of adaptations?

• An average number of offspring/parent > 1• Populations are stable in a long term• Therefore, only a fraction of the young survive and

reproduce• Organisms in populations differ • Probability of survival and reproduction (fitness)

depends on properties of an individual• Offspring inherit properties and fitness of their parents• Therefore, useful (adaptive) traits (structures and

behavioral patterns accumulate in populations

Vanishing nature of heritability.

genotype

phenotype

fitness

Richard Dawkins

Theory of selfish gene

• Individual genes are (usually) transmitted from parents to offspring unchanged

• Variants of the same gene (alleles) differ in their influence on phenotype and fitness of an organism

• Successful variants of a gene are transmitted to next generation in more copies than unsuccessful variants

• Therefore, variants of the same gene compete for ability to program their “vehicle” to help them to be transferred in as many copies as possible

• Mostly, but not always, the variants try to increase biological fitness of their “vehicle”

Necker’s cube

Blue beard model

♀ XX ♂ XY ♀ XX ♂ XY

W : WM

8 : 5 or 4 : 5

?????????????

Theory of selfish gene

• Explains origin of adaptations in sexual organisms• Explains evolutionary origin and success of “blue

beard” genes • Explains evolutionary origin and success of an

important category of altruistic traits – Under certain conditions, an organism could transmit more

copies of its genes by helping in reproduction to its relatives than by its own reproduction (helpers, bees, ants)

Theory of selfish gene is now the mainstream evolutionary theory

• Darwin: How this trait increases fitness of an individual?• Dawkins: How this trait increases a number of copies of

variant of gene that is responsible for its formation?

What is wrong with the selfish gene theory?

• It disregards a phenomenon of frequency dependent selection

• It disregards context-dependency of an impact of biological trait on biological fitness

• It disregards context-dependency of phenotypic expression of gene (epistasis)

b/2 b/2

0 b

(b-c)/2(b-c)/2

What is a final frequency of hawks in a population (p)?

Profit of hawks: ZH = p(b – c)/2 + (1 – p)bProfits of doves: ZD = 0 + (1 – p)b/2in equilibrium: ZH = ZD

p(b – c)/2 + (1 – p) b = 0 + (1 – p)b/2p = b/c = benefit/cost

A selective value of many traits depends on frequency of particular traits in population.

Therefore, not the highest fitness but an evolutionarily stable strategy (ESS) wins

Evolutionary stable strategy: to behave with probability b/c as a hawk and with probability 1-b/c as a dove.

Frequency dependent selection

Frequency dependent selection

What is a final frequency of yellow chromosomes in a population (p)?

Profit of red chromosomes : ZR = p(b – c)/2 + (1 – p)bProfits of yellow chromosomes: ZY = 0 + (1 – p)b/2in equilibrium: ZY = ZR

p(b – c)/2 + (1 – p) b = 0 + (1 – p)b/2p = b/c = benefit/cost

A selective value of many traits depends on frequency of particular traits in population.

Therefore, not the highest fitness but an evolutionarily stable strategy (ESS) wins

Evolutionary stable strategy: to behave with probability b/c as a yellow chromosome and with probability 1-b/c as a red chromosome.

b/2 b/2

0 b

(b-c)/2(b-c)/2

time (generations)

end of selection

Effect of selection on morphological trait (body size)

body

siz

e

Mayr E. 1964: Animal species and evolution. Cambridge Press, Cambridge.

Context-dependency of an impact of a trait on biological fitness

Then, tell me, what am I to do with my colts hanging pretty damn low, with my pretty damn short arms!

Gene 1

Gene 2

Gene 3

Gene 4

Trait 1

Trait 2

Trait 3

Trait 4

epistasis

Gene-phenotype trait relationships

pleiotropy

Gene 1

Gene 2

Gene 3

Gene 4

Trait 1

Trait 2

Trait 3

Trait 4

Gene 1

Gene 2

Gene 3

Gene 4

Trait 1

Trait 2

Trait 3

Trait 4

epistasis

Gene-phenotype trait relationships

pleiotropy

Gene 1

Gene 2

Gene 3

Gene 4

Trait 1

Trait 2

Trait 3

Trait 4

Gene 1

Gene 2

Gene 3

Gene 4

Trait 1

Trait 2

Trait 3

Trait 4

epistasis

Gene-phenotype trait relationships

pleiotropy

Gene 1

Gene 2

Gene 3

Gene 4

Trait 1

Trait 2

Trait 3

Trait 4

Problem with heritabilaty of fitness

Then, tell me, how can help me that an allele is transmitted from generation to generation unchanged when it has in each subject different impact on phenotype and different impact on biological fitness!

What is wrong with the selfish gene theory?

• It disregards context-dependency of an impact of biological trait on biological fitness

• It disregards context-dependency of phenotypic expression of gene (epistasis)

• It disregards a phenomenon of frequency dependent selection

Selfish gene theory is better than previous evolutionary theories (it explains broader spectrum of biological phenomena), however, it fails in its major purpose, i.e. in explaining origin of adaptations in sexual organisms.

Neither Darwin nor Dawkins, mama mia, what to do next?

creationist

sympatric

dichopatric

peripatric

Origin of new species - Speciation

colonization

Role of peripatric speciation in evolution

population growth

homogenization by genetic drift

adaptation by natural selection

freezing by accumalation of genetic variability

Theory of frozen plasticity • An average number of offspring/parent > 1• Populations are stable in a long term• Therefore, only a fraction of the young survive and reproduce• Organisms in populations differ • Probability of survival and reproduction (fitness) depends on properties of

an individual• Offspring inherit properties and fitness of their parents• Therefore, useful (adaptive) traits (structures and behavioral patterns

accumulate in populations• All these holds only in asexual species or in large genetically uniform

(plastic) population, ie. just after birth of species by peripatric speciation• For most of time (98-99% of life of a species), the sexual species are

evolutionary frozen.

time (generations)

end of selection

What genetic experiments say

body

siz

e

Mayr E. 1964: Animal species and evolution. Cambridge Press, Cambridge.

time (5 milions years)

What a paleontology says

Eldredge,N. 1971: Allopatric model and phylogeny in paleozoic invertebrates. Evolution, 26, 156-167.

What a biogeography says

Ricklefs,R.E. Cladogenesis and morphological diversification in passerine birds. Nature 430, 338-341, 2004.

What molecular phylogeny says

Mark Pagel,* Chris Venditti, Andrew Meade: Large Punctuational Contribution of Speciation to Evolutionary Divergence at the Molecular Level Science 314, 119-121, 2006

Differences between classical and frozen plasticity theory

clasical theory frozen plasticity theory anagenesis and cladogenesis ** are independent are coupled genetic polymorphism accelerates evolution decelerates evolution species respond to selection ** plastically (as plasticine) elastically (as ruber) species are adapted to its current environment its original environment abundance of species * is independent on its age decreases with age of species species on islands are derived ** as much on continents more than species on continents asexual species* less adapted to their environment more adapted to their environment cross-polinating species * as stable as self-pollinating more stable than self-pollinating divergence of species does not correlate with taxon richness correlates with taxon richness invasive species express average heritabilaty express higher heritabilaty domesticated species express average heritabilaty express higher heritabilaty domesticated species express average age are evolutionary younger successful selection has no influence on fitness decreases fitness local and global abundance ** correlate for any species does not correlate for old species group selection is rare is frequent rate of anagenesis with a clade * is (in average) constant always decreases two species in the same niche usually cannot coexist frequently could coexist slow long-term trends are hardly possible are quite possible

Flegr J.: Frozen evolution. Charles University, Prague 2008.Amazon, or http://natur.cuni.cz/flegr/frozen/index.php

Conclusions

• Neither darwinism, nor neodarwinism can explain adaptive evolution in sexual species

• Selfish gene model could operate only in systems without context-dependent gene expression and context dependent fitness

• Theory of evolutionarily stable strategies shows that sexual species respond to selection elastically

• After peripatric speciation, a new species turns plastic• After restoration of genetic polymorphism, the specie freezes and

rest of its existence just passively waits for its extinction• Frozen plasticity theory could explain broader spectrum of

biological phenomena than classical evolutionary theory