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