Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution

In the paper

“Animals of this organizational state would have resembled Ediacarian fossils such as Dickinsonia and may have been close to the cnidarian–bilaterian”

In the paper

“The concomitant acquisition of bilateral symmetry may have allowed more directed locomotion and, with more demanding coordinative tasks, triggered the evolution of specialized nervous subsystems.”

In the paper

“Second, the inner surface of the animals folded into metameric series of gastric pouches, which optimized nutrient resorption and allowed larger body sizes.”

In the paper

“In the bilaterian lineage, the mucociliary sole was used mostly for creeping, or frequently lost.”

In the paper

“Prerequisite for tracing nervous system evolution is understanding of the body plan, feeding behaviour and locomotion of the first animals in which neurons evolved.”

In the paper

“First, the invention of a mucociliary sole entailed a switch from intra- to extracellular digestion and increased the concentration of nutrients flowing into the gastric cavity.”

In the paper

“One possible remnant is the enigmatic Reissner's fibre in the ventral neural tube of cephalochordates and vertebrates.”

In the paper

“Starting from cup-shaped, gastraea-like animals with outer and inner choanoflagellate-like cells, two major innovations are discussed that set the stage for nervous system evolution.”

In the paper

“The slow myosin is also involved in amoeboid movement [38], which probably belonged to the behavioural repertoire of early metazoan cells.”

What the sources say

• Not checked yetcites [38] Liu YJ, Le Berre M, Lautenschlaeger F, Maiuri P, Callan-Jones A, Heuze M, Takaki T, Voituriez R, Piel M 2015 Confinement and low adhesion induce fast amoeboid migration of slow mesenchymal cells. Cell 160, 659– 672. (10.1016/j.cell.2015.01.007) 25679760

In the paper

“The flagellar cilia were both motile and sensory (as reported for unicellular eukaryotes and human airway cilia), and thus contained a very short and direct sensory-effector arc [22].”

What the sources say

• Not checked yetcites [22] Salathe M 2007 Regulation of mammalian ciliary beating. Annu. Rev. Physiol. 69, 401– 422. (10.1146/annurev.physiol.69.040705.141253) 16945069

In the paper

“These ancestors represented an epithelium [14] that took the shape of a sphere, called choanoblastaea [8], which later gave rise to the cup-shaped gastraea”

What the sources say

• Not checked yetcites [8] Nielsen C 2008 Six major steps in animal evolution: are we derived sponge larvae? Evol. Dev. 10, 241– 257. (10.1111/j.1525-142X.2008.00231.x) 18315817 source
• Not checked yetcites [14] Leys SP, Riesgo A 2012 Epithelia, an evolutionary novelty of metazoans. J. Exp. Zool. B Mol. Dev. Evol. 318, 438– 447. (10.1002/jez.b.21442) 22057924

In the paper

“the extensive folding of the inner surface into metameric pouches, which optimized nutrient distribution and resorption”

In the paper

“the endochoanocytes into cell types specializing in internal nutrient distribution and resorption”

In the paper

“and the ectochoanocytes into cell types specializing in mechanosensation, information integration and body contractions in response to environmental stimuli”

In the paper

“One prominent example is the division of labour that accompanied the birth of the first neurons and muscle cells (see §2).”

In the paper

“Various lines of evidence indicate that a new feeding mode evolved in the Precambrian ocean, referred to as mucoid-ciliary particle feeding [3] (figure 4a,b).”

• Also stated in: § Grazing algal mats with mucus and digestive gland cells · hedged

  “A rich body of fossil and comparative evidence indicates that mucoid-ciliary particle feeding evolved in early metazoans.”

What the sources say

• Not checked yetcites [3] Sperling EA, Vinther J 2010 A placozoan affinity for Dickinsonia and the evolution of Late Proterozoic metazoan feeding modes. Evol. Dev. 12, 201– 209. (10.1111/j.1525-142X.2010.00404.x) 20433459 source

In the paper

“We will hypothesize that the simple, bilayered, cup-shaped anatomy of this ancestor was reflected by a first diversification at the cellular level, including: (i) the external ‘ectochoanocytes’, mediating interactions with the environment; (ii) the internal ‘endochoanocytes’ that specialized towards particle capture and nutrient resorption; and (iii) the ‘kopeocytes’, regulating water currents”

In the paper

“choanoflagellates and metazoans share synaptic adhesion/signalling molecules, a primordial neurosecretory apparatus active on the apical cell surface (but no presynaptic active zone proteins) [32], postsynaptic density proteins such as Homer or Shank [33,34] and a variety of receptors including the metabotropic glutamate receptor [35] (but not ionotropic glutamate receptors, which only appeared in”

What the sources say

• Not checked yetcites [32] Burkhardt P 2015 The origin and evolution of synaptic proteins—choanoflagellates lead the way. J. Exp. Biol. 218, 506– 514. (10.1242/jeb.110247) 25696814 source
• Not checked yetcites [33] Alie A, Manuel M 2010 The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans. BMC Evol. Biol. 10, 34 (10.1186/1471-2148-10-34) 20128896 PMC2824662
• Not checked yetcites [34] Ryan TJ, Grant SG 2009 The origin and evolution of synapses. Nat. Rev. Neurosci. 10, 701– 712. (10.1038/nrn2717) 19738623
• Not checked yetcites [35] Krishnan A, Schioth HB 2015 The role of G protein-coupled receptors in the early evolution of neurotransmission and the nervous system. J. Exp. Biol. 218, 562– 571. (10.1242/jeb.110312) 25696819 source

In the paper

“We propose that, with these changes, basal metazoans had reached the organizational grade of the Ediacaran fossil Dickinsonia, which may have been close to the last common ancestor of cnidarians and bilaterians (that we collectively refer to as ‘Metameria’, figure 1a).”

In the paper

“Cell-type diversification involves the segregation and divergence of existing cellular modules or functions [5].”

What the sources say

• Not checked yetcites [5] Arendt D 2008 The evolution of cell types in animals: emerging principles from molecular studies. Nature reviews. Genetics 9, 868– 882. (10.1038/nrg2416) 18927580

In the paper

“Sponges might be regarded as representatives of a gastraea-type organization (which then would have undergone surface extension independent of other metazoan lineages”

In the paper

“Food was predigested externally in a layer of mucus and the predigested nutrients transported into the body cavity with water currents.”

In the paper

“Its most characteristic feature is the infolding of the lower body surface, resulting in an outer ectoderm, an inner gastroderm and a gastric opening (figure 3a).”

What the sources say

• Not checked yetcites [9] Haeckel E 1874 Die Gastraea-Theorie, die phylogenetische Classification des Thierreiches und die Homologie der Keimblätter. Jena Z. Naturwiss. 8, 1– 55.

In the paper

“classical authors agreed that the first metazoan cells had an apical collar with an undulating flagellum [16,17]”

What the sources say

• Not checked yetcites [16] Hibberd DJ 1975 Observations on the ultrastructure of the choanoflagellate Codosiga botrytis (Ehr.) Saville-Kent with special reference to the flagellar apparatus. J. Cell Sci. 17, 191– 219. 1089676
• Not checked yetcites [17] Leadbeater BSC 1983 Distribution and chemistry of microfilaments in choanoflagellates, with special reference to the collar and other tentacle systems. Protistologia 10, 157– 166.

In the paper

“Digestive enzymes were secreted into this mucus layer for external digestion. The coordinated and directional beating of effective stroke cilia distributed and transported the mucus over the digestive epithelium and washed the nutrients into the gastric cavity.”

In the paper

“It is a long-standing notion that the second step in the evolution of the metazoan body was the transformation of the spherical blastaea into the gastraea [8,9], which may have been close to the last metazoan common ancestor (figure 1b).”

What the sources say

• Not checked yetcites [8] Nielsen C 2008 Six major steps in animal evolution: are we derived sponge larvae? Evol. Dev. 10, 241– 257. (10.1111/j.1525-142X.2008.00231.x) 18315817 source
• Not checked yetcites [9] Haeckel E 1874 Die Gastraea-Theorie, die phylogenetische Classification des Thierreiches und die Homologie der Keimblätter. Jena Z. Naturwiss. 8, 1– 55.

In the paper

“Even in sponges, a transitory cup-like stage forms during metamorphosis, as recently confirmed [41]; and in cnidarians and ctenophores, the overall body form resembles that of a gastrula during the entire life cycle—at larval, polyp and medusa stages.”

What the sources say

• Not checked yetcites [41] Leys SP, Eerkes-Medrano D 2005 Gastrulation in calcareous sponges: in search of Haeckel's gastraea. Integr. Comp. Biol. 45, 342– 351. (10.1093/icb/45.2.342) 21676779

In the paper

“the transition to bilateral symmetry, which enabled directed movement, facilitated food search and avoided grazing the same area twice”

In the paper

“These latter cells would have constituted the first nerve net, which possibly controlled some form of amoeboid locomotion.”

In the paper

“They were swimming or lived partially benthic in shallow waters, filtering and concentrating dissolved organic carbon and bacteria as microphageous suspension feeders [3,15].”

What the sources say

• Not checked yetcites [3] Sperling EA, Vinther J 2010 A placozoan affinity for Dickinsonia and the evolution of Late Proterozoic metazoan feeding modes. Evol. Dev. 12, 201– 209. (10.1111/j.1525-142X.2010.00404.x) 20433459 source
• Not checked yetcites [15] Leys SP 2015 Elements of a ‘nervous system’ in sponges. J. Exp. Biol. 218, 581– 591. (10.1242/jeb.110817) 25696821 source

In the paper

“Subsequently, the kopeocytes may have further diversified into cell types specializing in ciliary movement and control, mucus production and secretion of digestive enzymes, thus enabling external digestion and forming a ‘mucociliary sole’ around the gastric opening”

In the paper

“However, digestion was intracellular at first and took place in the same multifunctional cells that also trapped the food—just as in unicellular eukaryotes.”

In the paper

“The sister cell-type concept [5] posits that cell-type evolution can be resolved into a scheme of stepwise diversifications, giving rise to sister cell types [5]”

What the sources say

• Not checked yetcites [5] Arendt D 2008 The evolution of cell types in animals: emerging principles from molecular studies. Nature reviews. Genetics 9, 868– 882. (10.1038/nrg2416) 18927580

In the paper

“Five subfamilies of transient receptor potential (TRP) channels were present [24], among which TRPV (vanilloid TRP) channels likely played an ancient role in mechanosensation”

What the sources say

• Not checked yetcites [24] Cai X, Clapham DE 2012 Ancestral Ca2+ signaling machinery in early animal and fungal evolution. Mol. Biol. Evol. 29, 91– 100. (10.1093/molbev/msr149) 21680871 PMC4037924
• Not checked yetcites [25] Fujiu K, Nakayama Y, Iida H, Sokabe M, Yoshimura K 2011 Mechanoreception in motile flagella of Chlamydomonas. Nat. Cell Biol. 13, 630– 632. (10.1038/ncb2214) 21478860

In the paper

“From Haeckel's times until today, strong support for the gastraea hypothesis comes from the prevalence of gastrula-like stages during animal development that are interpreted as recapitulation of the gastraea-like ancestral body plan.”

In the paper

“The initial function of this nerve net might have been the control of amoeboid locomotion of the gastraea, grazing on algal mats (resembling the movement of an amoeba, but at multicellular scale).”

In the paper

“the thyroid-related transcription factors TTF-2/foxE4, foxq1 and foxA are jointly expressed in the amphioxus and ascidian endostyle, a presumed homolog of the thyroidea that harbours mucus-secreting and motile ciliated cells; and this function of the Fox genes is considered ancestral for the chordates [119].”

What the sources say

• Not checked yetcites [119] Hiruta J, Mazet F, Yasui K, Zhang P, Ogasawara M 2005 Comparative expression analysis of transcription factor genes in the endostyle of invertebrate chordates. Dev. Dyn. 233, 1031– 1037. (10.1002/dvdy.20401) 15861404

In the paper

“Feeding traces indicate that one of the most characteristic fossils of the Ediacaran fauna, Dickinsonia, was grazing on the sea floor, which was covered by ubiquitous microbial mats [3] (figure 4a).”

What the sources say

• Not checked yetcites [3] Sperling EA, Vinther J 2010 A placozoan affinity for Dickinsonia and the evolution of Late Proterozoic metazoan feeding modes. Evol. Dev. 12, 201– 209. (10.1111/j.1525-142X.2010.00404.x) 20433459 source

In the paper

“Importantly, neuromuscular orthogon and mucociliary sole appear to have overlapped, because longitudinal muscles reach the gastric opening (at least in cnidarians).”

In the paper

“As a rule, the ectodermal muscle fibres associated with the nerve are oriented longitudinally, that is in parallel to the primary body axis (while the inner layer forms circular fibres [61,62]).”

What the sources say

• Not checked yetcites [61] Hertwig O, Hertwig R 1879 Die Actinien. In Studien zur Blättertheorie. Jena, Germany: Gustav Fischer.
• Not checked yetcites [62] Hyman LH 1940 The invertebrates: protozoa through Ctenophora. New York, NY: McGraw-Hill Book Company.

In the paper

“Most prominently, foxj has been identified as an ancient key regulator of motile cilia biogenesis [72,112,113], conserved in cnidarians [72] and even sponges [114].”

What the sources say

• Not checked yetcites [72] Vij S et al. 2012 Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program. PLoS Genet. 8, e1003019 (10.1371/journal.pgen.1003019) 23144623 PMC3493443
• Not checked yetcites [112] Stubbs JL, Oishi I, Izpisua Belmonte JC, Kintner C 2008 The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafish embryos. Nat. Genet. 40, 1454– 1460. (10.1038/ng.267) 19011629 PMC4648715
• Not checked yetcites [113] Yu X, Ng CP, Habacher H, Roy S 2008 Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nat. Genet. 40, 1445– 1453. (10.1038/ng.263) 19011630

In the paper

“A choanocyte-origin has been previously postulated for enterocytes [45] and for flame cells [46], based on morphological, functional and molecular resemblance.”

What the sources say

• Not checked yetcites [45] Takashima S, Gold D, Hartenstein V 2012 Stem cells and lineages of the intestine: a developmental and evolutionary perspective. Dev. Genes Evol. 223, 85– 102. (10.1007/s00427-012-0422-8) 23179635 PMC3873164
• Not checked yetcites [46] Jacobs DK, Nakanishi N, Yuan D, Camara A, Nichols SA, Hartenstein V 2007 Evolution of sensory structures in basal metazoa. Integr. Comp. Biol. 47, 712– 723. (10.1093/icb/icm094) 21669752

In the paper

“Interestingly, the metazoan foxA, B, C, D and E subfamilies are evolutionarily related [120–122] and resulted from duplications of an ancient precursor gene;”

What the sources say

• Not checked yetcites [120] Adell T, Muller WE 2004 Isolation and characterization of five Fox (Forkhead) genes from the sponge Suberites domuncula. Gene 334, 35– 46. (10.1016/j.gene.2004.02.036) 15256253
• Not checked yetcites [121] Mazet F, Yu JK, Liberles DA, Holland LZ, Shimeld SM 2003 Phylogenetic relationships of the Fox (Forkhead) gene family in the Bilateria. Gene 316, 79– 89. (10.1016/S0378-1119(03)00741-8) 14563554
• Not checked yetcites [122] Magie CR, Pang K, Martindale MQ 2005 Genomic inventory and expression of Sox and Fox genes in the cnidarian Nematostella vectensis. Dev. Genes Evol. 215, 618– 630. (10.1007/s00427-005-0022-y) 16193320

In the paper

“Placozoans move by ciliary gliding with the thick mucociliary sole facing the sea floor, and by concomitant contraction of the syncytial fibre cells (figure 4b).”

What the sources say

• Not checked yetcites [104] Ruthmann A, Behrendt G, Wahl R 1986 The ventral epithelium of Trichoplax adhaerens (Placozoa): cytoskeletal structures, cell contacts and endocytosis. Zoomorphology 106, 115– 122. (10.1007/BF00312113)

In the paper

“Such an ectodermal nerve net essentially controlled body wall contractions, possibly mediating local to more widespread ‘avoidance’ responses to mechanical stimuli [141].”

What the sources say

• Not checked yetcites [141] Pantin CFA 1956 The origin of the nervous system. Pubbl. Staz. Zool. Napoli 28, 171– 181.

In the paper

“Necessarily, in the absence of comparative molecular data for most of the cell types discussed here, the postulated sequence of cell-type diversification events underlying these transitions remains tentative.”

In the paper

“In essence, we hypothesize that such locomotion required more sensory integration and coordination with increasing body size (and that the increase in body size in turn resulted from the invention of the mucociliary sole with external digestion).”

In the paper

“These diverticulae have been compared with cnidarian pouches repeatedly [169,170] (figure 6e), which would imply that modern cnidarians resemble ‘a grade of Late Precambrian organization from which bilaterians evolved’ [171].”

What the sources say

• Not checked yetcites [169] Valentine JW 1992 Dickinsonia as a polypoid organism. Palaeobiology 18, 178– 182. source
• Not checked yetcites [170] Malakhov VV 2004 New ideas on the origin of bilateral animals. Russ. J. Mar. Biol. 30, S22– S33. (10.1007/s11179-005-0019-4)
• Not checked yetcites [171] Budd GE, Jensen S 2000 A critical reappraisal of the fossil record of the bilaterian phyla. Biol. Rev. 75, 253– 295. (10.1017/S000632310000548X) 10881389 source

In the paper

“Our scenario explains the evolutionary origin of this fibre, yet cannot explain why it is so persistent in extant vertebrates.”

In the paper

“The obvious advantage of this innovation was the extension of the internal surface, i.e. the surface of the resorptive epithelium, and would have intensified body physiology and probably allowed the maintenance and movement of larger body forms [163]”

What the sources say

• Not checked yetcites [163] Laflamme M, Xiao S, Kowalewski M 2009 From the cover: osmotrophy in modular Ediacara organisms. Proc. Natl Acad. Sci. USA 106, 14 438– 14 443. (10.1073/pnas.0904836106) PMC2732876 19706530 source

In the paper

“Similar ideas have been put forward repeatedly [5,66,67] and imply that the first synapse arose from the aggregation of vesicle-related intercellular signalling modules, including synaptotagmin, SNARE-complex components and postsynaptic receptor complexes, as extensively reviewed elsewhere [15,32,34,46,60].”

What the sources say

• Not checked yetcites [15] Leys SP 2015 Elements of a ‘nervous system’ in sponges. J. Exp. Biol. 218, 581– 591. (10.1242/jeb.110817) 25696821 source
• Not checked yetcites [32] Burkhardt P 2015 The origin and evolution of synaptic proteins—choanoflagellates lead the way. J. Exp. Biol. 218, 506– 514. (10.1242/jeb.110247) 25696814 source
• Not checked yetcites [34] Ryan TJ, Grant SG 2009 The origin and evolution of synapses. Nat. Rev. Neurosci. 10, 701– 712. (10.1038/nrn2717) 19738623
• Not checked yetcites [46] Jacobs DK, Nakanishi N, Yuan D, Camara A, Nichols SA, Hartenstein V 2007 Evolution of sensory structures in basal metazoa. Integr. Comp. Biol. 47, 712– 723. (10.1093/icb/icm094) 21669752
• Not checked yetcites [60] Nickel M 2010 Evolutionary emergence of synaptic nervous systems: what can we learn from the non-synaptic, nerveless Porifera? Invertebrate Biol. 129, 1– 16. (10.1111/j.1744-7410.2010.00193.x) source

In the paper

“In cerianthids, these are the only neurons to directly receive sensory innervation, to connect to each other, and to directly innervate, via multiple collaterals, the underlying myofibres [128]; they can thus be regarded as the core of the ancestral nerve net [130].”

What the sources say

• Not checked yetcites [128] Peteya DJ 1973 A light and electron microscope study of the nervous system of Ceriantheopsis americanus (Cnidaria, Ceriantharia). Z. Zellforsch. 141, 301– 317. (10.1007/BF00307408) 4147590
• Not checked yetcites [130] McFarlane ID 1984 Nerve nets and conducting systems in sea anemones: two pathways excite tentacle contractions in Calliactis parasitica. J. Exp. Biol. 108, 137– 149.

In the paper

“These data suggest that glutamate was the first excitatory transmitter in nerve net neurons, and that GABA acted as an inhibitory signal, possibly released in a refractory manner by the innervated muscle cells themselves.”

What the sources say

• Not checked yetcites [15] Leys SP 2015 Elements of a ‘nervous system’ in sponges. J. Exp. Biol. 218, 581– 591. (10.1242/jeb.110817) 25696821 source
• Not checked yetcites [156] Moroz LL et al. 2014 The ctenophore genome and the evolutionary origins of neural systems. Nature 510, 109– 114. (10.1038/nature13400) 24847885 PMC4337882 source
• Not checked yetcites [158] Delgado LM, Couve E, Schmachtenberg O 2010 GABA and glutamate immunoreactivity in tentacles of the sea anemone Phymactis papillosa (LESSON 1830). J. Morphol. 271, 845– 852. 20309875

In the paper

“First, external digestion with the mucociliary sole would have enabled external digestion and thus enhanced the concentration of nutrients in the gastric cavity.”

In the paper

“The medial section corresponds to the tissue of the former mucociliary sole; this tissue most probably evolved into the medial motor column of the bilaterian nerve cord [44], and the more lateral section into the lateral sensory-integrative columns.”

What the sources say

• Not checked yetcites [44] Arendt D, Tosches MA, Marlow H In press From nerve net to nerve ring, nerve cord and brain—evolution of animal nervous systems. Nat. Rev. Neurosci. 26675821

In the paper

“It has long been suggested that the invention of gastric pouches predated the CBA [164]; this notion can now be revived based on molecular evidence [44].”

What the sources say

• Not checked yetcites [164] Sedgwick A 1884 On the origin of metameric segmentation and some other morphological questions. Q. J. Microsc. Sci. 24, 43– 82.
• Not checked yetcites [44] Arendt D, Tosches MA, Marlow H In press From nerve net to nerve ring, nerve cord and brain—evolution of animal nervous systems. Nat. Rev. Neurosci. 26675821

In the paper

“Second, the substantial increase of the internal nutrient-resorbing surface via folding into gastric pouches might have boosted physiology and, consequently, energy supply for locomotion, thus triggering the regionalization and specialization of parts of the nerve net needed for the control of more sophisticated and targeted movements.”

In the paper

“Plausibly, body movement changed from multidirectional to unidirectional towards the new anterior end. This would have allowed more targeted food search and avoided passing through areas that had already been grazed (cf. figure 4a).”