Towards an Extended Evolutionary Synthesis The... · Towards an Extended Evolutionary Synthesis...

Towards an Extended Evolutionary

Synthesis

Gerd B. Müller

Department of Theoretical Biology, University of Vienna

and

KLI Klosterneuburg

Modern Synthesis

Neo-Darwinism

Mendel: rules of heredity

Darwin: variation and natural selection

Lyell: uniformitarianism

Lamarck: continuous evolution

Hunter: recapitulation

Hutton: gradualism

Linnaeus: systematics

1800

1900

?

evolution of evolutionary theory

Scala Naturae

Contemporary Debates in Philosophy of Biology

recent challenges

evolution as species diversification

evolution as variation in populations

htt

ps://c

oo

pla

b.g

ith

ub.io/

Selection against an extreme

Population

after selection

Original

population

evolution as generation of organismal complexity

evolution as origin of language, mind, culture

“descent with modification”

–

“the heritable change of properties over successive

generations in populations of organisms”

–

“the change of gene frequencies in populations”

changing definitions of evolution

-1-

key tenets of the

Modern Synthesis theory

Julian HuxleyErnst Mayr

Th. DobzhanskyG.G. Simpson

"Modern Synthesis" of the 1930s -1940s

population genetics

neo-Darwinian theory

experimental genetics

systematics

paleontology

botany

Modern Synthesis

population genetic core of the MS theory

ADAPTATION

VARIATION

populations contain genetic variation that arises randomly

from mutation and recombination

populations evolve by changes in gene frequency brought

about by natural selection, gene flow, and drift

genetic variants have slight phenotypic effects, the resulting

phenotypic variation is gradual and continuous

genetic inheritance alone accounts for the transmission of

selectable traits

natural selection acting on these incremental differences

provides the only directional factor in evolution

key tenets of the MS theory

after Futuyma 2003

populations contain genetic variation that arises randomly

from mutation and recombination

populations evolve by changes in gene frequency brought

about by natural selection, gene flow, and drift

genetic variants have slight phenotypic effects, the resulting

phenotypic variation is gradual and continuous

genetic inheritance alone accounts for the transmission of

selectable traits

natural selection acting on these incremental differences

provides the only directional factor in evolution

key tenets of the MS theory

after Futuyma 2003

• gene frequencies in evolving populations

• gradual variation of phenotypic traits

• adaptation of traits

• genetic features of speciation

the MS theory concentrates on

explantory deficits of the MS theory

• phenotypic complexity

• biases in the generation of selectable variation

• origins of phenotypic novelty

• non-gradual forms of transition

• non-genetic factors of change

-2-

challenges that arise from

integrating “evo” with “devo”

two components of EvoDevo

DEVELOPMENT EVOLUTION

evolution of development

role of development in evolution

evolution of development

Swalla 2006

PHYLOGENY HOX GENES FOUND KNOWN EXPRESSIONS

evolution of development

Davidson et al., 2005

two components of EvoDevo

DEVELOPMENT EVOLUTION

evolution of development

role of development in evolution

EvoDevo concepts

epigenetic innovation

internal selectionheterochrony

“not all variants arise with equal probabilities”

developmental bias

Brakefield 2003

“anisotropic accessibility in morphospace”

emergent cell patterning

“not all developmental structures are deterministic”

Alan Turing

Goldbeter at al. 2007

developmental bistabilities

somite formation

“not all developmental variation is continuous”

Dequéant and Pourquié 2008

variation of digit number in vertebrates

(–) (+)

vertebrate limb development

cellular limb bud regulatory interactions

cell autonomous skeletogenesis

cartlage matrix

production

(type II collagen,

aggrecan, etc.)

condensation cell number

I - V - II - III - IV

Greer, 1990

digit loss associated with limb size reduction in skinks

I

II

III

IV

V

II

III

IV

V II

III

IV

III

IV

IV

developmental sequence of digit formation

d19 d19.5 d20 d22

Müller and Alberch, 1990

IV - III - II & V - I

size reduction by mitotic inhibition

control ara-c treated

experimental sequence of digit loss

control ara-c treated

I

II

III

IV

V

II

III

IV

V

0 5 10 20 30 40

0

1

2

3

4

5embryoweight

(g)

µg ara-c (mitotic inhibitor)

digit

loss

I

II

V

buffered response

all

transgenic forelimb polydactylies in mice

control ShhN+

Li et al. 2006

Etv5/–; Twist1Ska10/+

Zhang et al. 2010

Shh–/–;Gli3–/–

Litingtung et al. 2002

**

*

*

*

**

*

spontaneous polydactyly in Maine Coon cats

Preaxial PolyDactyly (PPD)

polydactyly associated point mutations

cats

human

+ mouse

Lettice et al. 2008

CNE = a conserved non-coding element in a cis-regulatory region of sonic hedgehog (Shh)

ectopic expression of Shh in transgenic Hw mice

Lettice et al. 2008

PolyTrack database for Maine Coon cats

http://www.polytrak.net

975 individual cats

485 Hw mutants with PPD

range of polydactyly patterns in Hw mutant cats

Lange et al. 2014

forelimb

hindlimb

dist

post

prox

ant a b c

wild type 5-5-4-4

a threshold model for polydactly

cellular automaton simulation of skeletal formation

Lange et al. in preparation

activated

non-activated

activation stripe formation

Lange et al. in preparation

thresholds of activation stripe formation

Lange et al. in preparation

individual simulation runs

average

Variation of reaction rate

model predicition and empirical polydactyly in cats

Lange et al. in preparation

prediction

observedthresholds for polydactylous digits in cats

EvoDevo challenge

Developmental systems can react to selectional or

environmental perturbations in biased, emergent, and

discontinuous ways, thus introducing non-linearities

into the evolutionary process

Understanding the rules of developmental systems

permits to be predictive about evolutionary variation

-3-

challenges from other fields

genome evolution

gene duplication -

horizontal transfer -

epigenetic modification -

small RNA -

etc. -

Old view of gene evolution New view of gene evolution

Rose and Oakley 2007

challenges the notion of individual allelic substitution

multilevel selection

species ?

group

kin

individual

cells

genes

nat

ura

l

sele

ctio

n

Wilson & Wilson 2008

challenges the exclusiveness of selection at the level of the individuum

replicator theory

Eörs

Szathmary

topological or dynamical

neuronal replicators

chemical

replicators

replicators can enhance natural selection

inclusive inheritance

- Genetic

- Epigenetic

- Behavioral

- Cultural

INCLUSIVE

INHERITANCE

challenges the exclusiveness of genetic inheritance

low vs. high folic acid diet of mother

environmental induction

DEVELOPMENTALREACTION NORM

distribution of phenotypes

ENVIRONMENTAL INDUCTION

challenges the exclusiveness of natural selection

(Ulijaszek & Strickland, 1993)

"the process by which organisms alter

their own (or other species's) environment,

often (but not always) is in a manner that

increases its chances of survival"

niche construction

challenges unidirectional causation

systems biology

challenges the program dogma

the paradigms of

- random variation

- individual allelic substitution

- single level selection

- uniquely genetic inheritance

- unidirectional causation

have stopped to serve as privileged explanations

of evolutionary change

consequences

-4-

towards a theoretical integration

Mendelianinheritance

population genetics

Modern Synthesis

inheritance

variationreproduction

naturalselection

gene variation

DARWINISM

MODERN SYNTHESIS

quantitativegenetics

evo-devo concepts

Extended Synthesis

environmental induction

epigeneticinheritance

niche construction

replicator theory

multilevel selection

genome evolution

Mendelianinheritance

population genetics

inheritance

variationreproduction

naturalselection

gene variation

DARWINISM

MODERN SYNTHESIS

quantitativegenetics

EXTEDED SYNTHESIS

natural selection

next genera

tion

populations of phenotypes

natural selection

gene pool a

gene pool b

Et

Et+1

environm

ent

populations of phenotypes

t+1

t

genetic inherita

nce

Modern Synthesis

after Odling-Smee et al., 2008

Extended Synthesis

natural selection

next genera

tion

populations of phenotypes

natural selection

Et

Et+1

environm

ent

populations of phenotypes

t+1

t developmentalpool a

developmentalpool b

genetic inherita

nce

Extended Synthesis

next genera

tion

populations of phenotypes

Et

Et+1populations of

phenotypest+1

t developmentalpool a

developmentalpool b

multilevel selection

multilevel selection

genetic inherita

nce

Extended Synthesis

next genera

tion

populations of phenotypes

Et

Et+1populations of

phenotypest+1

t developmentalpool a

developmentalpool b

multilevel selection

multilevel selection

genetic inherita

nce

niche construction

niche construction

Extended Synthesis

next genera

tion

populations of phenotypes

Et

Et+1populations of

phenotypest+1

t developmentalpool a

developmentalpool b

multilevel selection

multilevel selection

genetic inherita

nce

epig

enetic

inh

erita

nce

niche construction

niche construction

Extended Synthesis

next genera

tion

populations of phenotypes

Et

Et+1populations of

phenotypest+1

t developmentalpool a

developmentalpool b

multilevel selection

multilevel selection

genetic inherita

nce

epig

enetic

inh

erita

nce

niche construction

niche construction

behavio

ral

inherita

nce

cultura

l in

herita

nce

Extended Synthesis

next genera

tion

populations of phenotypes

Et

Et+1populations of

phenotypest+1

t developmentalpool a

developmentalpool b

multilevel selection

multilevel selection

genetic inherita

nce

epig

enetic

inhe

rita

nce

niche construction

niche construction

behavio

ral

inherita

nce

cultura

l in

herita

nce

environmental induction

environmental induction

natural selection

next genera

tion

populations of phenotypes

natural selection

gene pool a

gene pool b

Et

Et+1

environm

ent

populations of phenotypes

t+1

t

genetic inherita

nce

Modern Synthesis

after Odling-Smee et al., 2008

Extended Synthesis

next genera

tion

populations of phenotypes

Et

Et+1populations of

phenotypest+1

t developmentalpool a

developmentalpool b

multilevel selection

multilevel selection

genetic inherita

nce

epig

enetic

inhe

rita

nce

niche construction

niche construction

behavio

ral

inherita

nce

cultura

l in

herita

nce

environmental induction

environmental induction

-5-

consequences

Modern

Synthesis

Extended

Synthesis

Basis of variation genetic,unbiased

developmental,biased

Genetic evolution drives phenotypic change

stabilizesemergent variation

Inheritance genetic inclusive

Rate of change gradual, continuous + discontinuous

Natural selection maintenance of traits

+ release of develop. potential

Environment independent of organismal activity

generated by organismal activity

major predictions

evolution of genotype-phenotype relation

origin of complex traits

major transitions

rapid and punctuated events

behavior, language, cognition

gene-culture coevolution

expanded explanatory reach of the EES

the EES results from new data and concepts that

have arisen in multiple areas of research

the EES integrates these concepts into a coherent

theoretical framework

the EES proposes a logic and predictions that differ

from the MS theory

the EES inspires novel research in evolutionary

biology and adjacent fields

summary EES

-6-

future directions

formal integration

VP=VT+VNT+VT*VNT

VT=VG+VTNG+VG*VTNG

VTNG=VTEpi*VPNGE*VTEcol*VTSoc

PHENOTYPIC

COMPLEXITY

genes

development

cells

Organization Theory

ADAPTATION

VARIATION

genetic

variation

reproductive success

inheritance

Population Theory

integrating developmental variation

quantitative EvoDevo with microCT

Metscher & Müller 2011

microCT developmental imaging

microCT with molecular probes

Metscher & Müller 2011

quantitative gene expression

Streicher et al. 2000

Costa et al. 2005

http://extendedevolutionarysynthesis.com

Department of Theoretical Biology

exploratory behavior

Plo

tkin

1988 a

fter

Waddin

gto

n

“A shift into a new niche

or adaptive zone is, almost

without exception, initiated

by a change in behavior. The

other adaptations to the new

niche, particularly the struc-

tural ones, are acquired secondarily.”

Mayr 1963

e.g., Waddington,

Piaget, Lorenz, Popper,

Bateson, Plotkin, etc.

challenges passive exposure to natural selection

key tenets of the MS theory

"Modern Synthesis" of the 1930s -1940s

Modern Synthesis

Extended Synthesis

Laland et al. 2015

major distinctions

predictability

Modern Synthesis

predicts what will be maintained and varied in organismal

evolution

Extended Synthesis

permits predictions about what can arise

in organismal evolution

explanatory role of natural selection

specificphenotypicsolution

boundary

condition

Modern

Synthesis

natural

selection

variation

Extended

Synthesis

developmental

dynamics

variation

+ natural selection

Source Initiation Specificity Phenotype

individualized

character

gradual

variationnatural

selectionadaptation

develomental

property

selection,

induction,

etc.

threshold

responsenovelty

Müller & Wagner 1991

Müller & Newman 2005

Peterson & Müller 2016

distinction: variation vs. emergent novelty

Modern Synthesis position on the origin of novelty

"the problem of the emergence of

evolutionary novelties consists in

having to explain how a sufficient

number of small gene mutations can

be accumulated until the new

structure becomes sufficiently large

to have selective value"

Mayr, 1960

developmental Finite Element Analysis (devFEA)

Petersen & Müller, in press

homoplasy

the (re-)occurrence of similar forms in independent lineages

Hemingway Model

summary threshold model

limb bud cells act as binary switches

perturbations generate single additive changes

summation of small effects into continuous distribution

threshold transformation in cell patterning and differentiation

discontinuous phenotypic outcome, i.e. gain or loss of digits

recognition of internal factors

constraint

emergence

autonomy

INHERENCY

Newman & Müller 2006

Callebaut, Müller & Newman 2007

CONTINGENCY

Modern Synthesis emphasizes

Extended Synthesis includes

Modern Synthesis

speciation

Mendelianinheritance

population genetics

contingency

inheritance

naturalselection

gene mutation

variation

evo-devo concepts

speciation

Mendelianinheritance

population genetics

contingency

Extended Synthesis

inheritance

naturalselection

gene mutation

environmental induction

inclusiveinheritance

niche construction

multilevel selection

genomic evolution

variationexploratory

behavior

on the authority of scientific theories

Concepts that have proven useful in

ordering things easily achieve such

an authority over us that we forget

their earthly origins and accept

them as unalterable givens

[.....]

The path of scientific advance is

often made impassible for a long

time through such errors.

A.E. 1916

explantory deficits of the MS theory

• behavioral complexity

• biases in the generation of behavioral variation

• behavioral novelty

• non-gradual forms of behavioral transition

• non-genetic factors of behavioral change

microevolution = genetic evolution

macroevolution = evolution “above the species level”

& major changes of form and function

the micro-macro distinction

The micro-macro distinction obscures the issues that

emerge from the current challenges to the standard theory

exploitive behavior

behavior

behavior preceedes morphological change

further reading

Alberch et al. 1979

“not all variants arise with equal probabilities”

biased variation

Brakefield 2003

limitations of developmental trajectories

anisotropic accessibility in morphospace

genotype space phenotype space

genotype space developmental space phenotype space

genotype-phenotype relation

Population Genetics

EvoDevo

cell beaviorsfunction

biophysics topologyfunctionbiophysics

DNA self-assembly, cis-regulation, etc.

E

E

E

developmental system

developmental sequence of digit formation

d19 d19.5 d20 d22

Müller and Alberch, 1990

IV - III - II & V - I

limb size reduction in skinks

Lerista praepedita

Lerista punctata

Lerista jacksoni

Lerista microtis

non-realized digit variation in skinks

I

II

III

IV

V

I

II

III

IV

V

I

II

V

control loss of distal phalanges loss of central digits

formal integration of developmental variation

PHENOTYPIC

COMPLEXITY

genes

development

cells

EvoDevo Theory

ADAPTATION

& FITNESS

variation

heredity

multiplication

Synthetic Theory

?