towards an extended evolutionary synthesis the... · towards an extended evolutionary synthesis...
TRANSCRIPT
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
?