11/04/17

From Nerve Net to Brain: The Rise of the Urbilaterian in Evoluon

Detlev Arendt 10-04-17

COS, Heidelberg University European Molecular Biology Laboratory Heidelberg, Germany Bringing the ocean to Heidelberg

amphioxus

sea anemone

Man is but a worm Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa the Urbilaterian the cnidarian-bilaterian ancestor ? Porifera the Urneuralian the last metazoan common ancestor Choanoflagellata the first animal some images courtesy C. Nielsen choanoflagellates

Latest phylogenomic animal tree

(Simion et al 2017) emerged in the

(Budd and Jensen 2015) Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa

Ctenophora

? Porifera

Choanoflagellata the first animal choanoflagellates resemble sponge choanocytes

Dayel.com Salpingoeca rosea Dayel.com ARTICLE IN PRESS

190 The first cell type: the 4 choanocyte 191 (a)(b) rstb.royalsocietypublishing.org 192 Plesiomorphies: 193 • guanylyl cyclase signaling via cGMP 194 • TRP channels 195 • various GPCRs including the metabotropic glutamate receptor 196 • prominent endocytoc machinery mediang phagocytosis 197 • well-developed Golgi produces lysosomes for intracellular digeson 198 199 200

201 Synapomorphies B Soc. R. Trans. HolozoaPhil. : 202 • flagellum surrounded by a collar of contracle microvilli 203 • 5 TRP channels , TRPV involved in mechanosensaon 204 • ‘synapc’ adhesion molecules 205 • a primordial neurosecretory apparatus acve on the apical cell 206 surface (but no presynapc acve zone proteins) 207 • postsynapc density proteins such as Homer or Shank 20150286 208 • actomyosin with NM- MHCII for slow contracon, integrin-mediated 209 basal adhesion, intercellular adhesion 210 • ST-MHCII for fast contracon (of what?) 211 212 213 Figure 2. The origin of metazoans. (a) The choanoblastaea. This animal represented the simplest possible(Ruiz- epitheliumTrillo in the, Burkhardt form of a sphere., King) The first and only cell 214 type are choanoflagellate-like cells. (b) A hypothetical ancestral metazoan cell-type resembling choanoflagellates. These cells had an apical, undulating cilium or Arendt et al., Phil. Trans. Roy. Soc. Lond. 2015 215 flagellum, propelling water away from the cell, surrounded by a circle of long, contractile, actin-containing microvilli. A well-developed Golgi complex produces 216 lysosomes for intracellular digestion, and a prominent endocytotic machinery mediates phagocytosis (Pc). Mm, mucoid mesh; Fp, filopodia. 217 218 Chemosensation involved guanylyl cyclases signalling via basal adhesion, cell–cell adhesion dynamics via adherens 219 cGMP (Johnson, 2010 #5539). Five subfamilies of transient junctions or apical constriction [37]—processes that were 220 receptor potential (TRP) channels were present [24], among key for the evolution of metazoan epithelia. The slow 221 which TRPV channels likely played an ancient role in mechan- myosin is also involved in amoeboid movement [38] that 222 osensation, as they mediate mechanosensation in Paramecium probably belonged to the behavioural repertoire of early 223 and Chlamydomonas [25], human airway epithelia [26] and metazoan cells. In addition, we can infer that early metazoan 224 Caenorhabditis elegans sensory cells [27]. In Chlamydomonas, cells formed lamellipodia and filopodia, using proteins that 225 these channels localize to the proximal region of the cilia, reorganize cortical actin filaments such as the Arp2/3 com- 226 where active bending is restricted (and self-activation avoided) plex, the actin cross-linking protein fascin and myosin X, a 227 [25]. Proteins required for action potential generation and myosin with pleckstrin homology domains that associates 228 propagation were likewise present in early meatzoans, such with regions of dynamic actin [39,40]. Filopodia are highly 229 as voltage-gated sodium [28,29], potassium and calcium dynamic structures that probably played a role in anchoring 230 channels [30]. Mechanical and chemical stimuli triggered and stabilizing cells in the blastaea (figure 2a,b). 231 depolarization of the ciliary membrane potential and calcium 232 influx into the cilium that had a direct effect on ciliary beat- 233 ing such as reversal or inhibition, as reported for unicellular 234 eukaryotes, cnidarians, ctenophores and bilaterians [31]. 3. The microphageous gastraea 235 Adding to this, choanoflagellates and metazoans share It is a long-standing notion that the second step in the evolution 236 synaptic adhesion/signalling molecules, a primordial neuro- of the metazoan body was the transformation of the spherical 237 secretory apparatus active on the apical cell surface (but no blastaea into the gastraea [9,10], which may have been close to 238 presynaptic active zone proteins) [32], postsynaptic density the last metazoan common ancestor (figure 1b). The term ‘gas- 239 proteins such as Homer or Shank [33,34] and a variety of recep- traea’ means ‘animal with a primitive gut’ and was coined by 240 tors including the metabotropic glutamate receptor [35] (but Ernst Haeckel [10]. Its most characteristic feature is the infolding 241 not ionotropic glutamate receptors, which only appeared in of the lower body surface, resulting in an outer ectoderm, 242 the metazoan stem). Many of these molecules and associated an inner gastroderm and a gastric opening (figure 3a). From 243 functions were key to the evolution of the first neural cell Haeckel’s times until today, strong support for the gastraea 244 types, as will be detailed below. hypothesis comes from the prevalence of gastrula-like stages 245 On the effector side, early metazoans cells already pos- during animal development that are interpreted as recapitula- 246 sessed a complex machinery for cellular contractions and tion of the gastraea-like ancestral body plan. Even in , 247 shape changes based on a dynamic actomyosin cytoskeleton. a transitory cup-like stage forms during metamorphosis, as 248 Actin-based movement involved a slow and a fast version of recently confirmed [41]; and in cnidarians and ctenophores, 249 myosin II that responded in a different manner and with the overall body form resembles that of a gastrula during the 250 different velocities to Ca2 signalling [36]. The slow non- entire life cycle—at larval, polyp and medusa stages. The þ 251 muscle myosin probably played a role in various cellular ancient gastraea is originally assumed as creeping on the sea 252 processes involving contraction, such as integrin-mediated floor, with the gastric opening facing downwards (while other

RSTB20150286—6/10/15—21:35–Copy Edited by: Not Mentioned The first animals possessed large part of the pre- and postsynapc cellular modules

(Liebeskind et al 2017) Kolmer-Agduhr cells ‘protoneuron’

chemosensory cell

enterocyte

choanocyte- like precursor

mechanosensory hair cell rhabdomeric photoreceptor flame cell Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa

Ctenophora

? Porifera

Choanoflagellata the first animal Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa

Ctenophora

? Porifera

the last metazoan

Choanoflagellata common ancestor The evoluon of development

Arendt et al., Phil. Trans. Roy. Soc. Lond. 2015 Sponges Sponge development: GATA expression demarcates micromeres / inner cells

GATA

Sycon ciliatum (Calcarea)

GATA Leininger et al 2014

Leininger et al 2014 Arendt et al., Phil. Trans. Roy. Soc. Lond. 2015 GATA is a marker for the inner layer in Nematostella!

Mesodermal gene expression in a diploblast 2467

sea anemone Nematostella

Fig. 4. Nv-GATA. Phylogenetic analysis and expression. (A) Alignment of 80 amino acids from various(Marndale et al 2004) GATA transcription factors spanning a central C2C2 zinc finger motif. (B) Phylogeny of GATA sequences. The tree was constructed and labeled as in Fig. 3. Sequences included in the analysis are: CG10278-PA (hypothetical protein), Drosophila, residues 514-595; GATA, Nematostella, residues 248-321; GATA-1 (GATA binding protein 1), Homo, residues 235-316; GATA-2, Homo, residues 326-406; GATA-3, Homo, residues 294-373; GATA-4, Homo, residues 193-273; GATA-5, Homo, residues 221-300; GATA-6, Homo, residues 274-356; grain, Drosophila, residues 292-378; MGC2306 (hypothetical protein), Homo, residues 326-407; pannier, Drosophila, residues 148-224; serpent, Drosophila, residues 451-535; TRPS1, Homo, residues 873- 959. (C-H) Expression of Nv-GATA. (C,D) Scattered cells express Nv-GATA at the blastula stage. Nv-GATA-expressing cells appear to move into the blastocoel (arrows). (E,F) At gastrulae stages expression is confined to endodermal cells. In the late planula (G) and early polyp (F) stages, ectodermal cells at the base of the developing tentacles also express Nv-GATA. Asterisks indicate the site of the mouth. end, endoderm; ect, ectoderm; tn, tentacles.

285 amino acids long. Within the forkhead , the 3I,J). This expression in a terminal gut structure is reminiscent Nematostella sequence is roughly 90% identical to Drosophila of the hindgut and foregut expression of forkhead in Drosophila forkhead and the FOXA2 sequence of humans (Fig. 3A). (Weigel et al., 1989) and the hypostomal expression of budhead Phylogenetic analysis places Nv-forkhead squarely within the in Hydra (Martinez et al., 1997). However, budhead is larger forkhead , most closely related to Drosophila expressed in the endoderm while Nv-forkhead is expressed forkhead, FOXA2, and the Hydra budhead genes (Fig. 3B). primarily in the ectodermal lining of the pharynx. The Similar to budhead (Martinez et al., 1997), Nematostella expression of orthologous forkhead genes in the sea anemone forkhead exhibits several phylogenetically conserved residues pharynx and the Hydra hypostome suggests that these structures within transcriptional activation domain II, and a handful of may be important for the development of the oral/anal opening. conserved residues within transcriptional activation domain III (Fig. 3A) (Pani et al., 1992). Nv-GATA Nv-forkhead expression is first detected in the late gastrula at The GATA genes constitute a family of zinc-finger transcription the site of the blastopore (Fig. 3C). Throughout , factors that bind the GATA motif, a widespread cis-regulatory Nv-forkhead continues to be expressed at very high levels element found in many promoters (Evans et al., 1988). GATA- exclusively in cells that are moving into the coelenteron (Fig. binding proteins can be recognized by the presence of one or 3D-H). This expression associated with the blastopore and two distinctive zinc-finger motifs of the form CXNCX17CNXC gastrulation is similar to that reported for sea urchins (Harada (Fig. 4A). In , GATA transcription factors are et al., 1996) and ascidians (Olsen and Jeffery, 1997). In the late implicated in the development of many mesodermal cell types planula and juvenile polyp, Nv-forkhead is expressed including red and white blood cells, smooth muscle, cardiac exclusively in the cells of the mesenteries and pharynx (Fig. muscle, adipocytes and gonadal cells (Arceci et al., 1993; The evolution of form: Ontogeny recapitulates phylogeny

(Ernst Haeckel) SFI working group on The origin and Cell types and Cell Type Originaon evoluon of cell types Organizers: Detlev Arendt, Manfred Laubichler, and Günter P. Wagner with Jacob Musser, Clare Baker, Mihaela Pavlicev, Doug Erwin, Stefanie Widder, Aviv Bergman, Gerhard Schlosser, Connie Cepko

NEWS | IN DEPTH

Studies of the marine worm Platynereis have confirmed that the has two origins.

very early in animal history and only later joined forces in the brain. Similar surprises are waiting in other brains, Arendt says. “It cannot be taken for granted that all cell types categorized as ‘neurons’ today in a given animal are more related to each other than to other cell types,” he concludes. “It is impossible to really understand a nervous system in the absence of knowledge about the distinct evolutionary histories of its constituting cell types.” Günter Wagner, a development evolu- tionary biologist at Yale University, saw something similar when he studied gene expression patterns in the cells that make up the uterus. He found that one type, the DEVELOPMENTAL BIOLOGY decidual cells that form part of the inter- face between fetus and mother and are sloughed off after birth with the placenta, Using evolution to better are a relatively recent innovation compared with other uterine cells. Many of the cell types making up the uterus appear to have identify cell types evolved very early in the history of mam- on November 12, 2015 mals, he said at the meeting. But based on on November 12, 2015 Gene expression patterns show that apparently related differences in gene expression profiles in cells can have very different evolutionary histories decidual cells from across the mammalian family tree, Wagner concluded that they arose about 200 million years ago, with the By Elizabeth Pennisi, in Santa Fe ferences themselves can’t be used to trace evolution of placental mammals. their origins. But each cell type has a dis- Gene expression is also telling un expected n biology, appearances can be deceiv- tinctive pattern of gene activity, which de- stories about cell types that look similar in ing. Evolutionary biologists know that pends not just on a cell’s current function different species. For example, both verte- www.sciencemag.org similarities in form and function are no but, bio logists believe, on its evolutionary brates and cnidarians such as have www.sciencemag.org guarantee that distinct species are ac- history. The sequencing revolution has led striated muscle cells, but researchers have Jake Musser I tually related: Think bats and birds, or to efficient ways of assessing this reper- shown that these cells arose independently wombats and groundhogs. To classify a toire of active genes, and through compari- in the two groups and built the striation us- creature, scientists now look to its DNA. But sons of such “transcriptomes,” biologists ing different sets of genes. These studies, many still rely on appearance and function are finding that many cell types are in need as well as other work in mammals, sea ur- for parsing the cell types that make up these of revision. chins, and over the past decade, . A small group of biologists is About 18 months ago, for example, indicate that it’s just a subset of the gene Downloaded from now pushing their colleagues to look instead Detlev Arendt, an evolutionary biologist at regulatory network that defines a cell type. Downloaded from for evolutionary clues to cells’ true nature. the European Molecular Biology Labora- This subset is in play in the same cell type The push grows out of recent evidence tory (EMBL) in Heidelberg, Germany, drew across organisms, providing strong evi- that similar-looking cells in the brain and re- on studies of brain evolution in vertebrates, dence of evolutionary connectedness. productive tract can have entirely different annelid worms, and insects to suggest that “We find that at [any] given time, each cell origins. “We need a different, more reliable all brains originate from two separate places expresses only 40% of the genes that are ex- concept” for classifying cells, says Stefanie in the embryo. One part arises from the tip pressed in all cells of the same type together,” Widder, a systems biologist at the Univer- of the embryo, he said, and the other from Mihaela Pavlicev, an evolutionary quantita- sity of Vienna. Widder was one of about what becomes the animal’s trunk. Working tive geneticist at the University of Cincinnati 20 scientists who gathered this month at the with John Marioni, a mathematician at the in Ohio, reported at the Santa Fe meeting Santa Fe Institute to hammer out an alter- EMBL-European Bioinformatics Institute from her studies of placental cells. The other native way of defining the identities of cells, in Hinxton, U.K., Arendt tested that idea active genes likely represent “modules” that based not on their looks but on the pattern by looking at gene expression in individual turn on to impart a particular structure or of genes they express. Not only do the gene- nerve cells in the marine worm Platynereis function to the cell, Arendt has proposed. expression signatures yield a truer picture of dumerilii. Even though the cells from the Defining these functional modules and the range of cell types in an , ad- two embryo sites look similar, their ex- distinguishing them from the so-called vocates argue, they also offer clues to how pression patterns are distinct, he reported character-identifying networks is a chal- particular cell types have adopted new roles at the meeting. For example, the trunk- lenge for researchers who want to use tran- over the course of evolution. derived neurons also express genes active scriptomics and other genomics data to Because almost all cells in a body have in striated muscle cells. The two kinds of define cell types. As the meeting in Santa Fe

the same basic genome, DNA sequence dif- neurons must have evolved independently drew to a close, participants outlined a pa- FISCHER ANTJE PHOTO:

618 6 NOVEMBER 2015 • VOL 350 ISSUE 6261 sciencemag.org SCIENCE

Published by AAAS

DA_1106NewsInDepth.indd 618 11/4/15 10:04 AM Nature Reviews | Genetics Manuscript number NRG-15-205V2 Arendt 05|09|16

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Fig 1 Phenotypic similarity

A B C D E F G H

Dispatch R759 functions that are characteristic and, in the ideal case, specific for neurons. A ? Recent comparative genomic and Concerted transcriptomic studies in basal Homology Convergence evolution metazoans, including ctenophores, have thus focused on the presence The cell type as an evoluonary unit or absence of pre- and postsynaptic Nature Reviews | Genetics genes [1,6,7]. Within the synapse, the postsynapse receives the transmitter Protostomia signal sent by the presynapse. Deuterostomia Postsynaptic genes are present in Cnidaria ctenophores [1], but the sequencing Ctenophora of a sponge genome [6] had also Placozoa identified an almost complete gene Porifera complement of the ‘postsynaptic ? Assembly of presynaptic scaffold density’, indicating that the emergence Synapse: Fig 2 chemosensory → postynaptic density of this cellular module predated Choano- ELKS the evolution of neurons with flagellates RIM Plants A Ba morphological synapses [5] and is thus Metabotropic glutamate and GABA receptors 2:NLI uninformative with regard to nervous Chemosensory receptive fields system homology. One hypothesis Ligand Ionotropic glutamate receptor Gain of gene/cellular module explaining this counterintuitive finding is that the ‘postsynapse’ is a modified TS1 TS2 TS3 V2a interneuron sensory receptive field that acquired Lhx3 Lhx3 Positive specifcation Ctenophora the capacity to detect intercellular B feedback signals [5,11]. This would also account TF1 TF2 TF3 m for the recruitment of glutamate as D Synaptic a transmitter (extensively used in vesicle BbCore Regulatory 2:NLI ctenophores [1]): glutamate might v ApomereCoRC x have initially been detected as an Rab3/27 Complex (CoRC) TF2 Munc13 Synaptotagmin sER ELKS environmental signal, later facilitating TF1 TF3 x Synaptobrevin/ GTP Isl1 Isl1 its recruitment as intercellular x RIM VAMP Motor neuron α-Liprins C Vertebrata transmitter following the advent of x Lhx3 Lhx3 specifcation the synapse [5,11]. In sponges, RIM-BP SNAP-25 and axon guidance postsynaptic density proteins are sER Syntaxin indeed localized to flask-shaped E1 E2 E3 E4 E5 sensory cells [12]; furthermore, as Ca2+-channel Synaptic cleft glutamate has been reported to trigger m Nature Reviews | Genetics contractions as an intercellular v paracrine signal in sponges [13], m ‘postsynaptic’ receptor assemblies E s b k may already be involved in the propagation of contraction waves. If the postsynapse is not specific Placozoa v for neurons, what can be said about the presynapse? The emergence of Current Biology the presynapse allowed direct and targeted information transfer to the postsynapse of other cells and may Figure 2. The phylogenetic position of ctenophores and the evolution of neurons. indeed represent the key novelty in (A) The step-wise assembly of synapses in metazoan evolution. Dashed lines demarcate possible positions of the ctenophore branch in a simplified animal evolutionary tree. Boxes neuron evolution. Ultrastructurally, indicate the gain of a cellular module or its constituting proteins. Coloured bars demarcate the ctenophore presynapse exhibits animal groups that possess the proteins labelled with the same colour code in panel D. Animal a unique morphology, referred to drawings from [4]. (B) Diagram of the ctenophore presynaptic triad. sER: smooth endoplasmic as the presynaptic triad (Figure 2B), reticulum; v: vesicle; m: mitochondrium. From [14] with kind permission from Springer Science stereotypically composed of a and Business Media. (C) Diagram of the presynapse. sER, smooth endoplasmic mitochondrion, an extension of the reticulum; v, vesicle; m, mitochondrium. From [15]. (D) The presynaptic active zone protein complex. Colored proteins form the evolutionarily conserved core of active zones [16]. Colour endoplasmic reticulum and synaptic code refers to the phylogenetic occurrence of individual proteins as indicated by bars in panel vesicles facing the membrane [14]. A. Adapted from [16]. (E) Fiber cells in adherens after https://sites.google.com/a/ This peculiar morphology, however, poriferaproject.com/www/moretrichoplaxadhaerens; s: synpase-like intercellular connection does not preclude presynapse with vesicles (v); b: intracellular bacterium; k: concrement ‘vacuole’; m: mitochondria. homology, given that the same cellular components are also involved in occurs from the presynaptic active zone proteins (Figure 2D) some presynaptic morphology in bilaterians ‘active zone’, which aligns with the have more general functions outside (Figure 2C) [15]. Transmitter release postsynaptic density [16]. Among the the synaptic context and are thus Research agenda

• invesgate the complement of cell types in representave species • molecular characterizaon of ! CoRCs ! synapomeres/apomeres • all cell types needed for comparison -> whole-organism comparison • all genes should be included -> no candidate gene bias • determine homologous and sister cell type relaonships Comparave single cell Kaia transcriptomics of Achim sponge cell types Jaime Huerta Cepas, Bork lab Jacob • Tethya wilhelma Musser • • Leuconoid body type Klaske • minimum of 10 cell types Schippers

Michael • Spongilla lacustris Nickel • Demosponge • Leuconoid body type Gert Wörheide

Warren Francis Cell capture and single cell sequencing

Fluidigm Single cell Auto Prep system®

Spongilla: dissociang whole sponges, oscula 335 Single Cell Transcriptomes Expression values for ~40,000 transcripts Choanocyte prep 223 Synapc gene homologs

Spongilla morphology

Oscule Oscular tube Subdermal lacunae (incurrent) Osa (incurrent)

(

Incurrent Excurrent Choanocyte channel channel chambers

Image courtesy of Michael Nickel GABA and glutamate trigger contracon waves

(Ellwanger and Nickel 2006) Nature Reviews | Genetics Manuscript number NRG-15-205V2 Arendt 01|08|16

Fig 4 Evoluon of the synapse: module integraon and divergence

Adherens and exocytosis

Divergence Integration

Adherens and reception

Adherens junctions Intercellular Reception • Cadherins exocytosis • Metabotropic • β-catenin • Syntactin glutamate receptor • P120-catenin • Synaptobrevin • GABA Receptors • Nectin • Synaptotagmin • Homer • Afadin • Dlg • MAGI1

Nature Reviews | Genetics Arendt et al. Nat. Rev. Genet. 2016 Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa

Ctenophora

? Porifera

the last metazoan

Choanoflagellata common ancestor Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa

Ctenophora

? Porifera the Urneuralian

Choanoflagellata Ctenophores: comb jellies Development and body plan

Arendt et al. Nat. Rev. Neurosci. 2015 The ctenophore nervous system

(Moroz et al 2014) A nerve net in cnidarians and ctenophores

Arendt et al. Nat. Rev. Neurosci. 2015 Cnidaria Ctenophora The Urneuralian: homology of neurons? Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa

Ctenophora

? Porifera the Urneuralian

Choanoflagellata Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa

Ctenophora the cnidarian-bilaterian ancestor ? Porifera

Choanoflagellata Cnidarian animal models: Nematostella and Hydra

Nematostella Hydra 172

Fig. 1 a, b. Whole-mount staining of Hydra attenuata by RFamide antiserum 146II. a Low power(from Richter et al 2010 micrograph showing a strong agglomera- tion of sensory cells around the mouth openingHydra and a weakerRfamide innervation of tentacles and upper gastric region, x 160. b Side view showing numerous sensory cells and a dense plexus of radially orientated processes in the apical half of the hypostome. • 160 Cellular composion and wiring of the cnidarian nerve net

Cerianthus (Petaya 1973)

Arendt et al. Phil. Trans Roy. Soc. Lond. 2015 Hydra neurons smulate muscle contracon via chemical synapses using large dense-cored vesicles Differences between Hydra and vertebrate synapses: ( Gründer and Assmann 2015) - few vesicles - large size (120–200 nm in diameter) - en passant along neurites - dense cores (Alzugaray 2013) - dense-cored vesicles arise from Golgi apparatus, suggesng they contain neuropepdes - RFamide, Allatotropin - neuromuscular juncon lacks postsynapc folds - HyNaCs: pepdergic ionotropic channels in Hydra - prevalence of electrical synapses between myoepithelial cells

(Liebeskind 2017) Gastrula-like larval stages Gastrula-like larval stages Regionalizaon #1: Apical – non-apical

Arendt et al. Nat. Rev. Neurosci. 2015 Specialized sensory structures at the apical pole

Arendt et al. Nat. Rev. Neurosci. 2015 Regionalizaon #2: nerve net

Mediolateral paerning

annelid

frog

anthozoan The cnidarian nerve net: the muscle connecon

mouth

sphincter muscle

mesentery

gastric pouch mechanosensory nerve net neuron

mulpolar myoepithelial ganglion cell cell

(Brusca and Brusca 2003) contracle process

(Mackie and Passano 1968) Gastric pouches in Cnidaria and

(Siewing) Animal evoluon * *

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa

Ctenophora the cnidarian-bilaterian ancestor ? Porifera

Choanoflagellata Gastric pouches in amphioxus

(Stach 2002) Gbx demarcates pouches in mid-body region

Castro et al., 2006

Branchiostoma The Hox genes paern gastric pouches/somites in Neuralia The cnidarian-bilaterian ancestor: close to ?

Arendt et al. 2015 Branching diverculae in Ediacaran

(Budd and Jensen 2015) The cnidarian-bilaterian ancestor: close to Dickinsonia?

(Budd and Jensen 2015) Life in the Precambrium: Dickinsonia with feeding traces

Sperling and Vinther 2010: Body of Dickinsonia costata associated with a series of feeding traces (South Australia Museum specimen 40845a). Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa

Ctenophora the cnidarian-bilaterian ancestor ? Porifera

Choanoflagellata Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa

Ctenophora the cnidarian-bilaterian ancestor ? Porifera

Choanoflagellata Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa the Urbilaterian Ctenophora

? Porifera

Choanoflagellata Regionalizaon #2: nerve net

The chimeric brain hypothesis Arendt et al Nat. Rev. Neurosci. 2015

Albrecht Fischer

Dorresteijn, Balavoine Jekely et al, Nature 2008 What are the Platynereis cell types and how are they evoluonarily related?

pictures : Harald Hausen, Nicolas Dray, Patrick Steinmetz Rope ladder-like nervous system: brain and ventral nerve cord

pictures : Harald Hausen, Nicolas Dray, Patrick Steinmetz single cell sequencing

Molecular signatures of cell type

with John Marioni Kaia Achim Nils Eling Marker genes of the apical nervous system

neurosecreon: - Allatostan - NPY - Vasopressin/Oxytocin

ciliary photoreceptor circadian clock

Tosches et al., Cell, 2014 The vertebrate ANS: a chimeric brain?

(Swanson, 2000) A digital cellular atlas for Platynereis

Hernando Marnez Vergara Platynereis serial block-face SEM

SBFSEM 6dpf

collaboraon Y. Schwab and C. Genoud, R. Friedrich, FMI Basel

• 300µm x 150µm x 150µm GATAN 3view, Zeiss Merlin • Resoluon 4-6nm xy • conducve embedding

Animal evoluon

Acrania

Ambulacraria

Cnidaria Protostomia

Placozoa the Urbilaterian Ctenophora the cnidarian-bilaterian ancestor ? Porifera the Urneuralian the last metazoan common ancestor Choanoflagellata the first animal Arendt lab 2017

Joaquim David Hernando Contradancas Jacob Puga Marnez

Musser

Mairi Marzia Paola Clarke Kaia Sidri Emily Bertucci Achim Savage 7