how to make protostomy - icim meeting 2014 in berlin (keynote)
TRANSCRIPT
How to make protostomy - A developmental perspective
Sars International Centre for Marine Molecular BiologyBergen, Norway
Andreas Hejnol
I see I am 3, Berlin 2014
Photos: AToL Team Protostome, Eric Röttinger, Steve Haddock, Michael Boyle, National Geographic, Wikipedia, G. von Dassow
Photos: AToL Team Protostome, Eric Röttinger, Steve Haddock, Michael Boyle, National Geographic, Wikipedia, G. von Dassow
The evolution of organ systems:The through gut
Fly HumanCnidarian
“Atlas of Drosophila development”, Volker Hartenstein
DeuterostomiaProtostomiaCnidaria
Bilateria
- bilateral symmetry- through gut- nervous system centralization- nephridia- mesoderm- HOX gene cluster
- radial symmetry- sac-like gut- nerve net
DeuterostomiaProtostomiaCnidaria
Bilateria
- bilateral symmetry- through gut- nervous system centralization- nephridia- mesoderm- HOX gene cluster
- radial symmetry- sac-like gut- nerve net
Masterman 1898
'Hypothetical ancestors'
Scenarios of bilaterian evolution
The Enterocoely-Hypothesis
polychaetecnidarian
Remane 1950
Scenarios of bilaterian evolution
polychaetecnidarian
Malakhov 2004; 2010
Scenarios of bilaterian evolution
The Amphistomy-Hypothesis
polychaete
Arendt & Nübler-Jung 1997
Scenarios of bilaterian protostome evolution
The Trochaea-HypothesisNielsen 1971
Scenarios of bilaterian evolution
The Acoeloid-Planuloid-Hypothesis
Hyman 1951(von Graff, Lankester, Beklemishev, Salvini-Plawen)
Its all about openings...
Simultaneous Evolution of mouth and anus
“Gastraea”“Trochaea”
Polyp
Egg
Planula
Blastopore Mouth Anus Mouth Anus
Single digestive opening
Mouth Mouth
Hejnol & Martindale 2008
Key-points:
The openings of the digestive tract (mouth and anus) are related to the blastopore.
The bilaterian mouth has been evolved either before ('acoeloid-planuloid') or simultaneously with the anus ('amphistomy').
We can reconstruct these ancient developmental processes at important bilaterian nodes.
Cnidaria Protostomia Deuterostomia
Conklin 1894
Grobben 1908
Conklin 1894
Grobben 1908
Cnidaria Protostomia Deuterostomia
Developmental types: BilateriaCampbell Biology (Ed. 2009)
Protostomy Deuterostomy
The blastopore is forming the mouth.
The mouth is formed separate from the
blastopore.
Blastopore: The site of endomesoderm formation.
Protostomy Deuterostomy
The blastopore is forming the mouth.
The mouth is formed separate from the
blastopore.
Blastopore: The site of endomesoderm formation.
Protostomy Deuterostomy
The blastopore is forming the mouth.
The mouth is formed separate from the
blastopore.
Blastopore: The site of endomesoderm formation.
An embryo is organized along the animal-vegetal axis
Martindale 2005
An embryo is organized along the animal-vegetal axis
Martindale 2005
BilateriaProtostomia Deuterostomia
Cnidaria Sea urchin Amphioxus VertebratesFly SnailRoundworm Earthworm
D?
?
Protostomyblastopore mouth
Deuterostomyblastopore anus
Amphistomyblastopore mouth
anus
Deuterostomyblastopore anus
A
Martín-Durán et al 2012
Deuterostomy: protostome variations
Nematomorpha
Inoue 1958
Nemertea
Eunice
Annelida
Åkesson 1967
Crustacea
Porcellio
Chaetognatha
Hertwig 1880
Priapulida
10 µm
mouth
a
anus
PriapulusMartin-Duran et al 2012
Lebedinsky 1897
BilateriaProtostomia Deuterostomia
Cnidaria Sea urchin Amphioxus VertebratesFly SnailRoundworm Earthworm
D?
?
Protostomyblastopore mouth
Deuterostomyblastopore anus
Amphistomyblastopore mouth
anus
Deuterostomyblastopore anus
A
Questions arising:
What are the morphological and molecular mechanisms that underly this variability?
What mode of gastrulation was present in the last common ancestor of Protostomia and whole Bilateria?
What does this mean for proposed scenarios of bilaterian evolution?
Priapulid Development
ArthropodaLoriciferaKinorhyncha Tardigrada OnychophoraNematodaPriapulida Nematomorpha
Panarthropoda
Cycloneuralia
Scalidophora
Ecdysozoan origins
Ancestral Ecdysozoancharacters
ArthropodaLoriciferaKinorhyncha Tardigrada OnychophoraNematodaPriapulida Nematomorpha
Panarthropoda
Cycloneuralia
Scalidophora
Ecdysozoan origins
Ancestral Ecdysozoancharacters
Gastrula Introvertula
blastopore
mouth
anus gut
HatchingFertilization
Introvert
retractionCleavage
Hatching
larva
1 2 3 4 5 6 7 8 90 days
Animal
Vegetal
Embryonic development
Wennberg et al., 2008Martín-Durán et al., 2012
Gastrulation
* *
* *
Day 3 Day 4
archenteron50 µm 50 µm
10 µm 10 µm
PhallacidinPropidiumIodide
C mo D
dgmc
A
* ac
B
*
Day 3 Day 4 Day 5 Day 6
&· '·$· %·
* * an
an
an
E
F
sc
mo
mc
sc
Gastrula Introvertula
bp
mo
an dg
sc
ActinNuclei
HatchingFertilization
IntrovertretractionCleavage Hatching
larvasc
in
tr
&·· '··$·· %··
1 2 3 4 5 6 7 8 90 days
Animal
Vegetal
Mouth development
Martín-Durán et al., 2012
Foregutbrachyury goosecoidfgf8/17/18
Midgutforkhead/FoxAnotch
Hindgutbrachyury caudal/cdxfgf8/17/18 wnt1
Molecular markers
Hindgut markers
cdx
* * anus
bra
* blastopore * anus
*
Gastrula Introvertula
Hindgut markers are expressed in the blastopore and anus
lateral view vegetal view lateral view posterior view
Foregut markers
Foregut markers are not expressed in the blastopore
foxA
gsc
** *
*
mouth
mouth
**
**
Gastrula Introvertula
lateral view vegetal view lateral view anterior view
Cnidaria(Nematostella vectensis)
Ecdysozoa(Priapulus caudatus)
Spiralia(Platynereis dumerilii)
Deuterostomia(Ptychodera flava)
Bilateria
Protostomia
gscfoxAcdxbra
*
* *
*
Hypothesis: Deuterostomy ancestral in Bilateria?
DD
D
P ?
D Deuterostomy
P Protostomy
Protostomia
Bilateria
Chaetognatha
Deuterostomia
Priapulida
Nematoda
Arthropoda
Annelida
Brachiopoda
Nemertea
Cnidaria
'Hybrid'taxa
Deuterostomy
Protostomy
Amphistomy
Protostomia
Bilateria
Chaetognatha
Deuterostomia
Priapulida
Nematoda
Arthropoda
Annelida
Brachiopoda
Nemertea
Cnidaria
'Hybrid'taxa
Deuterostomy
Protostomy
Amphistomy
The blastopore and mouth are different molecular entities.
Clythia Houliston et al 2010
Clythia , Momose et al 2010
Cnidariangastrulation
Summary:Protostomic and deuterostomic embryos develop from a blastula that seems to be the "default" stage of all bilaterian animals.
In comparison with deuterostomic embryos, protostomy needs additional changes such as differential growth, changes in axis determination and elongation of the embryo.
The phylogenetic framework identifies deuterostomy as part of the ground pattern for all Bilateria.
The bilaterian mouth is specified independently from the blastopore.
Conclusion The last common ancestor of Bilateria gstrulated by
deuterostomy
yes
Scenarios of bilaterian evolution that are
based on amphistomy are not parsimonious
Nemertean variationsFriedrich 1979
Conclusion The last common ancestor of Bilateria gstrulated by
deuterostomy
yes
Scenarios of bilaterian evolution that are
based on amphistomy are not parsimonious
Conclusion The last common ancestor of Bilateria gstrulated by
deuterostomy
yes no
The high variability and changes
between gastrulation modes indicates that
modes are not of major importance
Scenarios of bilaterian evolution that are
based on amphistomy are not parsimonious
Conclusion The last common ancestor of Bilateria gstrulated by
deuterostomy
yes no
The high variability and changes
between gastrulation modes indicates that
modes are not of major importance
yesScenarios of bilaterian evolution that are
based on amphistomy are not parsimonious
Conclusion The last common ancestor of Bilateria gstrulated by
deuterostomy
yes no
The high variability and changes
between gastrulation modes indicates that
modes are not of major importance
yesScenarios of bilaterian evolution that are
based on amphistomy are not parsimonious
no
well...
Aina BørveLab-
Technician
Sabrina Schiemann
PhD Student
Bruno VellutiniPhD Student
Kevin PangPostdoc
Chema Martín-DuránPostdoc
Sars Centre
Annie BoddingtonAnimal Facility
Technician
Carmen AndrikouPostdoc
Daniel ThielPhD Student
Henrike Semmler LêPostdoc
.org
DeuterostomiaProtostomiaCnidaria
Bilateria
- bilateral symmetry- through gut- nervous system centralization- nephridia- mesoderm- HOX gene cluster
- radial symmetry- sac-like gut- nerve net
AcoelaCnidaria
Bilateria
Nephrozoa
DeuterostomiaNemertodermatida Protostomia
Acoelomorpha
- nephridia- through gut?- centralized nervous system?
- “brain”, nerve cords- bilateral symmetry- mesoderm- HOX cluster (anterior, central, posterior)
- radial symmetry- nerve net- sack like gut