Evo-devo of novel traits: the genetic basis of butterfly ...
Micro-evo-devo: Genotype-phenotype relationships, convergences,...
Transcript of Micro-evo-devo: Genotype-phenotype relationships, convergences,...
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Virginie Courtier-OrgogozoInstitut Jacques Monod, Paris
Micro-evo-devo:Genotype-phenotype relationships,
convergences, environmental factors
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What is evo-devo?
● Development
● Evolution
● Evo-devo
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https://www.nature.com/articles/nrmicro3519/figures/1
Life cycle of Plasmodium falcifarum
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https://www.notesonzoology.com/phylum-chordata/ascidia-habit-locomotion-and-life-history-zoology/3974
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Pradeu, T., Laplane, L., Prévot, K., Hoquet, T., Reynaud, V., Fusco, G., ... & Vervoort, M. (2016). Defining “development”. In Current topics in developmental biology (Vol. 117, pp. 171-183). Academic Press.
process through which a single cell (often a fertilized egg) gives rise to a complex multicellular organism
Frontiers:RegenerationUnicellular organismsAsexual reproductionAgingCell death
Examples of subfields:MorphogenesisOrganogenesisCell differentiation
Development
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What is Evolution?
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https://en.wikipedia.org/wiki/Miller%E2%80%93Urey_experiment
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Plasticity: one genotype → several phenotypes
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Rapid evolution of great tits
Etonnant vivant : découvertes et promesses du XXIe siècle (2017)
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process through which the characteristics of populations or species change over successive generations
Frontiers:Origin of LifeEvolutionary roboticsPlasticity
Examples of subfields:PaleontologyExperimental evolutionModelling of Evolution
Evolution
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Classical Darwinian Evolution
Variation
Transmission
Differential reproduction
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Selection
Genetic Drift
Mutations in DNA
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Nature 2014
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Classical viewAdditions
extra-genetic inheritance
Extended evolutionary synthesis
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Developmental Bias
Natural evolution
D. quadrilineata
Standing variation
D. melanogaster
variationno variation
Marcellini et al 2006 PloS Biol
Garcia-Vázquez 1988 J. Heredity
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Niche construction
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Meyer & Beisson M/S 2005
Cortical heredity in Paramecium
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What is Evo-Devo?
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2001
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field of biological research that compares development between species to understand how they evolved
Frontiers:Same as development and evolutionEcologyPhysiology, Behavior
subfields:Macro-evo-devo (distantly related species)Micro-evo-devo (closely related species or populations)
Evo-devo
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The distinction between genotype and phenotype
is the basis of genetics
Johansen 1911
“The view of natural inheritance as realized by an act of transmission, viz., the transmission of the parent's (or ancestor's) personal qualities to the progeny, is the most naive and oldest conception of heredity.”
“All "types" of organisms, distinguishable by direct inspection or only by finer methods of measuring or description, may be characterized as ''phenotypes.”
“ A ''genotype'' is the sum of all the "genes" in a gamete or in a zygote.”
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Phenotype = observable attributes of an individual
Genotype = inheritable genetic material = DNA or RNA
How do genotypes map onto phenotypes ?
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A very brief history of genetics
- Mendel 1860s
- Classical genetics 1900-1950 distinction genotype-phenotypesegregation of characters & genesgenetic map, sex chromosomespenetrance - expressivity
"Rediscovery" of Mendel's lawExtension to animals
- Cytology from 1880-90s Flemming, Boveri, Suttonchromosomes as support of heredity, meiosis
Transmission + Phenotypic expression
Controlled breeding, use of probabilitiesDominant/recessive/intermediate expression of traits Random transmission of "factors"
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- Foundation of molecular biology 1940-1970in part using bacteria and phage genetics DNA as the material support of heredity
- Deciphering the role of the genes: 1970-Cellular, developmental, behavioral genetics: Screens"High-throughput" versions 2000- (e.g. deletion libraries)Reverse genetics
- Association mapping on natural populations: 2000-
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Mendelian genetics"Mendelians"
Statistical genetics"Biometricians"
Divergences and syntheses
Laboratorygenetics
Population geneticsevolution genotype
Functional genomics
Quantitativegeneticsphenotype
Evolutionarygenomics
Quantitativegeneticsmolecular basis
agriculture
Molecular evolution
Molecular geneticscell biology, developmentphysiology, etc.
1900
1975
1990
1930
Molecular markers
"Neodarwinian synthesis"
Evo-Devo
Molecular biology1950
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DEVELOPMENTAL BIOLOGY EVO-DEVO
Both are direct descendants of Morgan's school. Emphasis on genes.
One of the central problems of biology is that of differentiation - how does an egg develop into a complex many-celled organism? That is, of course, the traditional major problem of embryology; but it also appears in genetics in the form of the question, “How do genes produce their effects?
Sturtevant, 1932
How does an organism form from a single cell? What makes one organism different from another one?
How do genes produce observable traits?
Gene Observable character
How do genotypes map onto phenotypes ?
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Pax6 : an eye gene ?
Gene Observable character
Pax6 Eye development
Drosophila
WT
Ectopic expression of Pax6
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Pax6 Eye development
genescellular environment
mechanical forcessymbionts
external moleculestemperature
gravity...
Observable character
Too simplistic
Better, but difficult to disentangle the effects
environment
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Gene Observable character
GeneticLocus
Abstract Phenotypic
trait
Allele 1
Allele 2
Observed phenotypic state 1
Observed phenotypic state 2
Gene
Normal allele
Abnormal allele
Normal Phenotypic state
Aberrant Phenotypic state
Developmental Biology
Evolutionary Genetics
Abstract Phenotypic
trait
genescellular environment
mechanical forcessymbionts
external moleculestemperature
gravity...
Observable character
A Cause/Mechanism relates to a Difference
Differential Views
Evolutionary Genetics
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ColorSize and shapePresence/absencePosition
Aristote, Historia animalium, book I, 2, 300BC
Morphology
Physiology
Behavior
Different kinds of phenotypes
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Micro-evo-devo
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?
What makes us different?
between individuals between species
Where do we come from?
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?
GenomesCCTCCTCCATACCCAAATGGATGGTACGGCATTCTTGAATCATCAAAGCTTAGAGCGGGGGAATCGAAGCATATATCATGTCTAGGCGAGCAACTTATAGTGTTCCGTTCCCAAGCTGGTGAAGTTTATATCTTGGATGCGTATTGCCCGCACTTGGGCGCTAATTTGAGTAAGGGAGGTCGAGTTATAGGAGATAATATTGAATGTCCCTTTCACCACTGGAGCTTTAGAGGCAGTGATGGCATGTGTACCAATATTCCCTACAGCAGCAATATACACTCATCTACAAAAACTAAAAAATGGACCTCCACCGAAGTGAATGGATTCATATTTCTTTGGTACAATGTCGAAGAATCTGAAGTTCCGTGGAATATACCAAAATCAGTTGGTGTTGCAAAAA
CCTCCTCCATACCCAAATGGATGGTACGGCATTCTCGAATCATCAAAGCTTAGAGCGGGGGAATCGAAGCATATATCATGTCTAGGCGAGCAACTTATAGTGTTCCGTTCCCAAGCTCGTGAAGTTTATATCTTGGATTCGTATTGCCCGCACTTGGGCGCTAATTNGAGTAAGGGAGGTCGAGTTATAGGAGATAATATTGAATGTCCCTTTCACCACTGGAGCTTTAGAGGCAGTGATGGCATGTGTACCAATATTCCCTACAGCAGCAATATACACTCATCTACAAAAACTAAAAAATGGACTTCCACCTAAGTGAATGGATTCATATTTCTCTGGTACAATGTCGAAGAATCTGAAGTTCCGTGGAATATACCAAAATCAGTTGGTGTTGCAAAAA
Phenotypic differences
Genomic approach
identifies rapidly-evolving genomic regions, new genes, deleted genes
?
Phenotypic approach
identifies the gene(s) and the mutation(s)
responsible for a phenotypic change
What are the mutations responsible for phenotypic
differences?
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A case study
Evolutionary loss of bristles in D. santomea
Nagy et al Current Biology 2018
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D. santomeaD. erecta
D. orena
D. teissieri
D. yakuba
D. simulans
D. sechellia
D. mauritiana
D. melanogaster
0.5MYA
222222022
2 bristles
0 bristles
D. yakuba D. santomea
100 mm 100 mm
phallusphallus
D. santomea has lost sex bristles
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Gillespie and Walker 2001
Bristle development
futurethorax
futurewing
Marc
elli
ni 2
006
- P
loS
Bio
logy
scute
DC
SC
PA
Simpson 2007
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Lewis - Imaginal discs
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75kb 0kb
Gómez-Skarmeta 2003
Simpson 2007
scute cis-regulatory elements are “master switches”
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Marcelini and Simpson 2006 PloS Biology
Evolution of fly bristle pattern
Cis-regulatory element (CRE) in scute
scute
++
Xscute
+
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Genetic evolution is predictable
scute
Stern and Orgogozo 2009 ScienceMarcelini and Simpson 2006 PloS Biology
Cis-regulatory element (CRE) in scute
scute
++
Xscute
+
Evolution of fly bristle pattern
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Is the causing mutation X-linked?
D. yakuba D. santomea
xY
D. santomea D. yakuba
Y
xY
YF1 F1
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Is the causing mutation X-linked?
D. yakuba D. santomea
xY
D. santomea D. yakuba
Y
xY
Y
2 bristles 0 bristle
The causing mutation
is X-linked
n = 35 n = 8
F1 F1
1 bristle
0 bristle
2 bristles
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screen of D. melanogaster
GAL4 lines
GAL4
105 kb
Screening a 100-kb region
x UAS-RNAi-singed , UAS-Dicer2
drives expression in developing genital bristles
drives no expression
not tested yet
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drives expression in developing genital bristles
drives no expression
not tested yet
105 kb
18C05 drives expression independently of scute
18C05X X
GAL4x sc29 ; UAS-scute
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Mutation(s) in 18C05 cause loss of bristles
scuteyak scutesanscutemel
0 bristle
1 bristle
2 bristles
D. melanogaster transgenics
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27 SNPs and 3 indels between D. santomea and D. yakuba
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12 D. santomea-specificmutations
18C05alignment
7 affect sites that are conserved in the
melanogaster subgroup
30mutations
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3 mutations affect genital bristle number
yak scute0 bristle
1 bristle
2 bristles
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D. santomea lost genital bristles via 3 mutations in scute
XAncestral state Derived state
D. yakuba D. santomea
scute
-
Xscute
+
scute
XX
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QTL mapping
D. yakuba
x
D. santomea
x
D. yakuba
D. yakuba backcross
F1
Y
XX X XY
Genomic region associated with the phenotype
Y
Y
Y
Y
Y
Y
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QTL mapping
One major QTL at the tip of the X chromosomeTwo minor QTL on the 3rd chromosome
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D. yakuba2 bristlesn=30
2 bristlesn=30
no effect 18C05
Variablen = 30
Hybrid background at 25 °C
effect18C05
2 bristlesn=30
Introgression of 18C05 (scute)
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D. santomea Introgression of D. yakuba into D. santomea
0 bristlesn=30
no effect 3.37 MB
Hybrid background at 29 °CVariable
n = 482 bristles
n = 50
effect
0 bristlesn=30
Introgression of 3L
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D. santomea lost genital bristles via mutations in scute
XAncestral state Derived state
D. yakuba D. santomea
scute
-
Xscute
+
scute
.. and in at least 2 other genes on 3L.
The scute locus has no effect alone.
Sensitive genetic and environment backgrounds help to magnify the QTL effects.
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The genotype-phenotype relationship
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DNA(or RNA
originally)
protein
translation
catalysis
Genotype & Phenotype= what is apparent= what engenders
• Biochemical reactions
• Subcellular architecture
• Assembly of cells
• Organism morphology and behavior
etc.
• Regulation of gene expression
distinction appeared at the origin of life:
DNA/RNA
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Here a dot representsthe mean state of a
population
selection
repro-duction Population genetics:
stochastic processes and selection coefficient
Evolutionarybiology of phenotypes,evolutionary ecology
Quantitative genetics:heritability of phenotypes
Phenotype construction:
developmental and cellular
biologyphysiology
The first genotype-phenotype map
Lewontin 1974
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Salazar-Cuidad & Martin-Riera 2013
PhenotypeTooth
morphology
Fitness
Genotype
The genotype-phenotype-fitness map
Here a dot representsone individual
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Orgogozo et al 2015 Frontiers Genetics
The genotype-phenotype connection
Xu et al 2013 Current Biology
4
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Genotype = “the genetic makeup of an organism that determines a specific phenotype (trait), from one generation to the next, and potentially throughout the population”.
Report of the National Academy of Sciences on gene drive, 2016
NO!
The genotype-phenotype connectionis about differences
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The genes contributing to evolution
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www.Gephebase.org>2000 entries
@gephebase
Orgogozo et al Nucleic Acid Research 2019
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oca2 in cavefish
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anthocyanin-2 coding region(Quattrocchio 1999)
Wrinkled seed: TE insertion(Bhattacharyya 1990)
OVATE coding region(Liu 2002)
luciferase coding region(Stolz 2003)
Mc1r coding region(Eizirik 2003)
myostatin coding region(Grobet 1997)
FRI coding region(Johanson 2000)
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FORWARD GENETICSFrom traits to genes
Little Ascertainment Bias, but Micro-Evolution only
REVERSE GENETICSFrom genes to traits
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survey of ~300 articlesStern and Orgogozo 2008 Evolution
More cases of coding than cis-regulatory mutations
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More cases of coding than cis-regulatory mutations
2019
1259 mutations
356 mutations
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Evolution repeats itself
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Repeated evolution via the same amino acid change
garter snake
Tetrodotoxin
toxic newt pufferfish (fugu)
X
XNav1.4 sodium channelE945D
Nav1.4 E945D
toxic plancton
Saxitoxin
XNav1.4 E945D
clam
Bricelj 2005Geffeney 2005
Venkatesh 2005
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Repeats in..
.. the genes responsible for natural evolution
.. the genes responsible for experimental evolution
Ex : hemoglobin in dogs and humans in Tibet(Wang et al 2014 GBE)
Ex : sulfate transporter SUL1 in yeasts in low sulfate(Gresham et al 2008 PloS Genetics)
Orgogozo 2014 Interface Focus
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Repeated evolution
Orgogozo et al 2015 Frontiers Genetics
Also in:HumansHorsesQuailsChickensMicePigeons
4
4
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Specialized loci in the genome
Proteins that interact with external moleculesoxygen, photons, insecticide, cholesterol...
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Specialized loci in the genome
Proteins that interact with external moleculesoxygen, photons, insecticide, cholesterol...
Cis-regulatory elements of “developmental switch genes”
scute
Simpson 2007 Trends GeneticsStern and Orgogozo 2009 Science
scuteCRE CRE CRECRE
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From random processes can emerge predictability
Mutations in DNAChromosome segregation during meiosis
Assortative matingGamete competition during fecondation
Life history traitsGenetic linkage
Environmental changes (meteorite, etc.)...
Many unpredictable processes at a low level
Predictable Evolutionat the genetic level
coding mutation in VKORC1 gene
Orgogozo 2014 Interface Focus
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From random processes can emerge predictability
Position, mass, velocity of each particle
Microscopic world Macroscopic world
Pressure, Volume, Temperature, Number of moles
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After a few seconds
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A small number of genetic solutions for a given phenotypic change
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We sometimes seem to have forgotten that the original question in genetics was not what makes a protein but rather ‘what makes a dog a dog, a man a man’.(D. Noble – The Music of Life)
A small number of genetic solutions for a given phenotypic change
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Evolution:unconstrained and unpredictable?
1977
[past and present organisms are] a subset of workable, but basically fortuitous, survivals among a much larger set that could have functioned just as well, but either never arose, or lost their opportunities, by historical happenstance.
Stephen Jay Gould, 2002
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Would life evolve again,would it produce similar living beings?
How?
Why? (1) rather than nothing
Why? (2) rather than another change
evolution
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Main collaboratorsFly anatomy
Jean David (Gif-sur-Yvette)Morphometrics
Vincent Debat (Paris)François Graner (Paris)
Genotyping
David L. Stern (Janelia Farm, USA)Fly crosses
Daniel Matute (UNC, USA)Gephebase
Arnaud Martin (Berkeley, USA)
LabOlga Nagy (past member)Isabelle Nuez (IE)
Michael Lang (CR)Alexis Lalouette (MCU)
Bénédicte Lefèvre (PhD)Flora Borne (PhD)Manon Monier (PhD)
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https://www.youtube.com/watch?v=Ov30-7rXZCYUne brève histoire de l’évo-dévo (Denis Duboule)
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Evolution of Drosophila glue
Da Lage et al. 2019 BMC Evol Biol
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Evolution of left-right asymmetry in D. pachea