Towards multicellularity

Colonial organization

Information exchange ApoptosisExternal

secretion

Four elements to make a multicelluar organism

Paenibacillus dendritiformis

BacteriaPaenibacillus

•forms colonies•moves on hard surfaces through jointly secreted lubricants•communicates with other cells•no apoptosis•no real cell differentiation

Myxococcus xanthus

Myxobacteria•form colonies of millions of cells•Some have coordinated movements•form biofilms•largest bacterial genomes (9 - 12 kB)•some produce fruiting bodies for the release of spores•no apoptosis•rudimentary cell differentiation

Why did Bacteria not evolve true multicellularity?Maybe their limits in genome size do not allow for higher order differentiation.

Nanowires and electrical signalling

Geobacter sulfurreducens

Microbial electrical cell-cell communication via nanowires may

be widespread in nature.

Colonial organization

Information exchangeApoptosis External

secretion

Four elements to make a multicelluar organism

Vascular plants

Brown algae Slime moulds

Fungi

Metazoa

Cell differentiation

Specialized cells reproduceHigh degree of cell differentiationReal tissuesOrgansNo central coordination

Early differentiation of germ lineHigh degree of cell differentiationReal tissuesOrgansCentral coordinationSpecialized cells reproduce

Cell differentiationNo real tissuesNo organs

Specialized cells reproduceCell differentiationReal tissuesNo organs

Facultative multicellularityRudimentary cell differentiationNo real tissuesNo organsMultiple origin of multicellularity in each of these groups

Multicellularity probably monophyletic

Stigmergy:indirect signalling by secretion

ChlorophytesFacultative multicellularityLimited cell differentiationNo real tissuesNo organs

The multi-taxon genome initiative

Amoebozoa

Ichthyospora

Sphaeroforma arctica

Capsaspora

Nuclearia

Fungi

Metazoa

Choanoflagellata

Apusozoa

Ministeria

Pseudo-multicellular colonies

Nematostella

Single celled parasites of marine pulmonate snails

Some species form colonies

Chorallochytrium

Corallochytriumlimacisporum

Free living

Parasitic

Free living

True multicellularity

Single celled aquatic heterotroph

Single celled marine heterotroph

Parasitic

Single celled free living marine heterotroph Single celled terrestrial or

aquatic bacteriophages

Tonian1000-850

Mesoproterozoicum1600-1000

PlantaeOomycota

Mycetozoa s.str.

Choanoflagellata

Microsporidia

Metazoa

Chytridiomycota

Zygomycota

Ascomycota(Saccharomyces cerevisiae)Basidiomycota

Lecanoromycetes

Plant pathogen

Arthropod pathogen

phagotroph

Saprotroph / mutualists

lichenized

Dicaria

Opistho-konta

Fungi

terrestrial

Multiple loss of flagellum

Phytophora infestans

Amphiacantha

Chytridium

Glomeromycota

Phycomyces

terrestrialUnikonta

Bikonta

Nuclearia simplex

Nuclearia

(Chromista)

Arbuscular mycorrhiza

Ektomycorrhiza

First Glomeromycota fossils

Ordovician490-440

Silurian440-410

Devonian410-355

Carboniferous 355-290

First lichens

PDZ signal

PDZ signalwwguk

Generalized Metazoa

Ichthyospora

The MAGI genesGuanylate kinases regulate tight tissue junctions

Zebra fish

Single cell organismsParasites of marine fish, birds and mammalsSome species form pseudo- multicellular colonies

Ichthyospora

A major invention: Metameria

Christiane Nüsslein-Volhard (1942-)

Arche Hox

EHG box Proto Hox Proto NKL

EHG box Extended Hox NKL Para HoxEarly Vertebrates

Early arthropods

All animals share a common gene family, the homeobox family, that controls metameric and embryonal development.

Trichoplax adhaerens

Early Metameria

Cnidaria

Walter Jacob Gehring (1939-)

In sponges and Ctenophora Hox genes haven’t been detected yet.

Plants

Fungi

Metazoa

Homeotic genes: MADS-box

Homeotic genes

Homeotic genes: Hox-genes

Convergent evolution of genes that regulate ontogenetic development

Cnidaria

Metameria

Placozoa

From: http://users.rcn.com/jkimball.ma.ultranet/BiologyPages/H/HomeoboxGenes.html

Eleutheria dichotoma,Photo from Jacob and Schierwater

2007, Plos One 2: e694.

Inactivation of Cnox 3 in the hydrozoan Eleutheria

dichotoma produces multiple heads, for

instance head duplication and therefore a bilaterian

pattern

The evolution of Hox genes

Tonian1000Super-

continent Rodinia

Cryogenian850

Rodinia breaks up.Largest

glaciations (snowball

earth)

Ediacaran630

Warmer period

interrupted by local ice ages

?

Metazoa

Charniodiscus

Dickinsonia Tribrachidium

Spriggina floundersi

ParvancorinaCyclomedusa

?

From Tonian to modern times

HorodyksiaMaybe a colonial benthic two tissued

metazoan

Meso-protero-zoicum

1600-1000

Parmia

Maybe a homonomous segmented metazoan

Photos from Fedonkin 2003

Biotracers of Porifera

Early Ediacaran

630 Warmer period

Middle Ediacaran

600 Local ice ages

Avalon assemblages

580 Warmer period

Increase in atmospheric

O2 level

White sea and Nama

assemblages560

Warmer period

Cambrium540

Warmer period

Aspidella

Advanced Rangeomorpha and simpler ErniettomorphaProbably not related to any modern taxon

Charnia

Shallow water mobile animals related to

modern taxa

Immobile, deep-water filter feedersNo mouth or gut, no reproductive organs

Rangeomorpha were fractal organisms developing through simple branching patterns (like Fungi)

An early embryo

Kimberella, Mollusca: like

Chiton

Spriggina Arthropoda:Canadia,

Annelida

Tateana

Acri-tarch

Porifera

ChoanoflagellataPlacozoa

Ctenophora

Cnidaria

Plathelminthes s. str.

Cycloneuralia(Nematoda, Priapulida)

Lophotrochozoa

Chordata

Mul

ticel

lula

rity,

Hox

box

„Bilateria”

Protostomia

Blastoporus becomes anus

Cho

anoc

ytes

Upp

er a

nd lo

wer

sid

e

ParaphyleticMultiple bilaterality

Gas

trula

, Mus

cle

cells

Metameria, Coelom

Ect

o-, E

ntod

erm

Cnidocytes, Rhopalia

Ner

vous

cel

ls, S

tato

cyst

Acoela

Xenoturbellida

Cryogenian850-680

Ediacaran680-540

Tonian1000-850

Cambrian540-490

Mesoproterozoicum1600-1000

Ambulacraria (Hemichordata, Echinodermata)

Chaetognatha

OnychophoraArthropoda

Gnathifera

Annelida s. l.Mollusca

Deuterostomia

EcdysozoaMetameriaPseudocoelom

Metameria, Coelom

Mes

oder

m

Pseudocoelom

No anus

No anus

No anusNo coelom

Lophophorata

Pseudocoelom, Anus, Metameria

Paraphyletic

Ectoderm

Ciliate entoderm

Nervous cellsPorifera

Statocyst

PlacozoaInformation exchange via neurotransmitters

Trichoplax

A functional model of metazoan evolution

A hypothetical creeping animal of Gastrula organization

CtenophoraCnidaria

Acoela

Xeno-turbel-lida

Deuterostomia s. str. Lophotrochozoa Ecdysozoa

Mesogloa

Cryogenian850-630

Ediacaran630-540

Cambrian540-490

Mass extinction

Onychophora

Trilobites

The molecular evidence

ChelicerataXiphosura, Arachnida

Pycnogonida

Pancrustacea

„Myriapoda”Diplopoda

Chilopoda

MyodocopaPodocopa

Remipedia

Ordovician490-440

Silurian440-410

Hexapoda

Branchiopoda

Maxillopoda

Malacostraca

Aysheaia

Beckwithia

typa

Aglaspida

Cephalocarida

Isopoda

Ostra-coda

Tardigrada

Panarthropoda(Tetraconata)

MandibulataXenocarida

The Cambrian explosion

Cambrian 540-490

During the Cambrian atmospheric oxygen concentration increased to a level to allow for the development of hard skeletons. Probably all today’s phyla were already present.

First complicated food webs including higher predators appeared. This might have caused the disappearance of the Ediacaran fauna.

Waptia, Chelicerata? An early predator

Burgessochaeta, Polychaeta

An early predator

Ottoia, PriapulidaAn early predator

Chmatocrinus, CrinoideaThe earliest deuterostomes

Pikaia, ChordataOlenoides serratus,

Trilobites

Ordovician 490-440 Silurian 440-410

Ice ageMass extinction

First primitive terrestrial fungi, vascular plants and animals (millipedes,

arachnids)

Eurypterus remipes,

Chelicerata

First Cephalopoda (Nautiloids) and Bivalvia. Rise of Brachiopoda and Bryozoa.

Warm shallow seas Warm greenhouse phase (high CO2 level)

Trilobites Arthropoda Bryozoa

Cephalopoda

ConodontsBirkenia, Agnatha

Cooksonia grade land plants

Ordovician490-440

Silurian440-410

Devonian410-355

Charophytes

Em

bryo

phyt

es

Marchantiopsida

Bryophyta

Aglaophyton Rhynia

Trac

heop

hyte

s

Lycopodiaceae

Isoetales

Drepanophycales

Psilophyton

Sphenopsida

Pterydophyta

Seed plants

Cambrian540-490

?

First land plants

?

Molecular data put the divergence of Bryophytes and Tracheophytes to the end of the Proterozoic (540 to 700 mya).

Parafunaria sinensis

Chara Lunularia cruciata

Devonian 410-355

Stomata of Rhynia Pterychthyodes, Placoderna

Rather warm, zoned climate Rather warm, zoned climate Southern glaciation, mass extinction

Moresnetia zalesskyi

Kampecaris forfarensis , Myriapoda

Niedźwiedzki et al. 2010)

Carboniferous 355-300

Ice ageMass extinction

Warm and wet climateHigh oxygen concentration

Breyeria harlemensis Paleodictyoptera

Euproops rotundatus Xiphosura

Delitzshala bitterfeldensis

Homoptera

Equisetum

Lepidodendron source of today’s coal

Carboniferous 355-300

Ice ageMass extinction

Warm and wet climateHigh oxygen concentration

Synapsid reptiles Diapsid reptiles

Temporal fenestra

Heterodont HomodontAnapsid reptilesHomoodont

Archeothyrisfirst primitive Synapsid

Petrolacosaurusfirst primitive Diapsid

heterodont

Hylonomusa first primitive

Anapsid

Carboniferous 355-290

Permian290-250

Trias250-205

Jurassic205-140

Cretaceous140-65

Pelycosauria

Therapsida

Mammalia

Am

nion

Sarco-pterygia

Mesosauria

Testudines ??

Crocodylia

Pterosauria

Dinosauria

Aves

Euryapsida

Squamates

Rhyncho-cephalida

Synapsid cranion

Diapsid cranion

Lepidosauromorpha

Archosauromorpha

Anapsida Testudines ?

Anapsid cranion

Permian 300-250

Ice ageMass extinction Warmer and arid Arid Mass

extinction

Anapsid reptiles

Mesosaurus, Permian primitive anapsid aquatic reptile

Milleretta, Permian primitive anapsid terrestrial reptile

Aldabra tortoise

Dimetrodon, Permian primitive synapsid Pelycosaur

Pelycosaur → Therapsida → Theriodontia (mammal like)

Proburnetia, Permian primitive synapsid Therapsid

Annatherapsidus petri , Permian synapsid Theriodont

Permian 300-250

Ice ageMass extinction Warmer and arid Arid Mass

extinction

Synapsid reptiles

Mammal like teeth

Permian 300-250

Ice ageMass extinction Warmer and arid Arid Mass

extinction

Diapsid reptiles

Tuatara, Lepidosauria

Pterodactylus kochii, Archosauromorpha

Ichthyosaurus, Lepidosauria

LepidosauromorphaSquamata, Tuatara

ArchosauromorphaPterosauria, Dinosauria

Ichthyosauria

Thecodont dentition

Acrodont and pleurodont dentition

Terrestrisuchs, Crocodylomorpha

Endothermy?Scale derived thermoregulating body cover?

Thermoreg-ulating body cover

Crocodylomorpha

Today’s reading

Ediacara fauna and the origin of Metazoa: http://www.peripatus.gen.nz/paleontology/Ediacara.html

http://www.ucmp.berkeley.edu/vendian/critters.htmlThe Burgess shale: http://www.gpc.edu/~pgore/geology/geo102/burgess/burgess.htm

http://www.palaeos.com/Paleozoic/Cambrian/Cambrian.htmThe history of life: http://www.palaeos.com/The tree of life: http://www.tolweb.org/tree/The virtual fossil museum: http://www.fossilmuseum.net/

On the cambrian explosion: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1578734

Metazoan phylogeny: the state of art.:http://icb.oxfordjournals.org/cgi/content/full/46/2/93

Dunn C. W. et al. (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452: 745-750. Srivastava M. et a. 2008. The Trichoplax genome and the nature of placozoans. Nature 453: 855-960..