Skip to main content
Book cover

Evolution, Origin of Life, Concepts and Methods pp 135–160Cite as

A Look Back Over 20 Years of Evo-Devo Studies on Sponges: A Challenged View of Urmetazoa

Abstract

The majority of extant metazoans are animals with bilateral symmetry, a gut, a central nervous system and a head; they are grouped in a taxon named Bilateria. As a consequence, most of the zoological definitions are based on observations in bilaterian animals. To understand how these anatomical features emerged, it is now necessary for the Evo-Devo field to undertake studies on the four extant lineages that emerged earlier, namely Cnidaria, Placozoa, Ctenophora and Porifera. Being the sister group of bilaterians, cnidarians have received much attention compared to the other three phyla but, given the disparity of body plans between these four non-bilaterian phyla, comparative analyses are needed not only to trace back the origin and evolution of genetic mechanisms involved in animal development but also to understand the evolutionary processes that gave rise to such a huge animal body plan diversity. This chapter focuses on the evo-devo approaches applied to Porifera and how the data have changed our view of these uncommon animals and how it challenges previous concepts of the last common metazoan ancestor. We discuss here the current and future steps that need to be undertaken to ensure that sponges join the laboratory “model organisms club.”

Keywords

  • Bilaterians
  • Non-bilaterians
  • Body plan evolution
  • Animal evolution
  • Phylogenetic
  • Genomics
  • Model organisms

This is a preview of subscription content, access via your institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-3-030-30363-1_7
  • Chapter length: 26 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   169.00
Price excludes VAT (USA)
  • ISBN: 978-3-030-30363-1
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Softcover Book
USD   219.99
Price excludes VAT (USA)
Hardcover Book
USD   219.99
Price excludes VAT (USA)
Learn about institutional subscriptions
Fig. 7.1
Fig. 7.2
Fig. 7.3
Fig. 7.4
Fig. 7.5
Fig. 7.6

References

  • Adams EDM, Goss GG, Leys SP (2010) Freshwater sponges have functional, sealing Epithelia with high transepithelial resistance and negative transepithelial potential. PLoS One 5(11):e15040.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Adamska M (2016) Sponges as models to study emergence of complex animals. Curr Opin Genet Dev 39:21–28

    CrossRef  CAS  PubMed  Google Scholar 

  • Adamska M, Matus DQ, Adamski M, Green K, Rokhsar DS, Martindale MQ, Degnan BM (2007a) The evolutionary origin of hedgehog proteins. Curr Biol 17:R836–R837

    CrossRef  CAS  PubMed  Google Scholar 

  • Adamska M, Degnan SM, Green KM, Adamski M, Craigie A, Larroux C, Degnan BM (2007b) Wnt and TGF-beta expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS ONE 2:e1031

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Adamska M, Larroux C, Adamski M, Green K, Lovas E, Koop D, Richards GS, Zwafink C, Degnan BM (2010) Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evol Dev 12:494–518

    CrossRef  CAS  PubMed  Google Scholar 

  • Adamska M, Degnan BM, Green K, Zwafink C (2011) What sponges can tell us about the evolution of developmental processes. Zoology (Jena) 114:1–10

    CrossRef  Google Scholar 

  • Adell T, Thakur AN, Müller WEG (2007) Isolation and characterization of Wnt pathway-related genes from Porifera. Cell Biol Int 31:939–949

    CrossRef  CAS  PubMed  Google Scholar 

  • Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown MW, Burki F, et al (2018) Revisions to the classification, nomenclature, and diversity of Eukaryotes. J Eukaryot Microbiol

    Google Scholar 

  • Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud’homme B, de Rosa R (2000) The new animal phylogeny: reliability and implications. Proc Natl Acad Sci USA 97:4453–4456

    CrossRef  CAS  Google Scholar 

  • Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493

    CrossRef  CAS  PubMed  Google Scholar 

  • Alexander BE, Liebrand K, Osinga R, van der Geest HG, Admiraal W, Cleutjens JPM, Schutte B, Verheyen F, Ribes M, van Loon E et al (2014) Cell turnover and detritus production in marine sponges from tropical and temperate benthic ecosystems. PLoS ONE 9:e109486

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Alexander BE, Achlatis M, Osinga R, van der Geest HG, Cleutjens JPM, Schutte B, de Goeij JM (2015) Cell kinetics during regeneration in the sponge Halisarca caerulea: how local is the response to tissue damage? Peer J 3:e820

    CrossRef  PubMed  CAS  PubMed Central  Google Scholar 

  • Alié A, Hayashi T, Sugimura I, Manuel M, Sugano W, Mano A, Satoh N, Agata K, Funayama N (2015) The ancestral gene repertoire of animal stem cells. Proc Nat Acad Sci 201514789

    Google Scholar 

  • Atkinson SD, Bartholomew JL, Lotan T (2018) Myxozoans: ancient metazoan parasites find a home in phylum Cnidaria. Zoology (Jena) 129:66–68

    CrossRef  Google Scholar 

  • Babonis LS, Martindale MQ (2017) Phylogenetic evidence for the modular evolution of metazoan signalling pathways. Philos Trans R Soc Lond B Biol Sci 372

    CrossRef  CAS  Google Scholar 

  • Belahbib H, Renard E, Santini S, Jourda C, Claverie J-M, Borchiellini C, Bivic AL (2018). New genomic data and analyses challenge the traditional vision of animal epithelium evolution. BMC Genomics 228452

    Google Scholar 

  • Booth DS, Szmidt-Middleton H, King N (2018) Choanoflagellate transfection illuminates their cell biology and the ancestry of animal septins. Mol Biol Cell mbcE18080514

    Google Scholar 

  • Borchiellini C, Boury-Esnault N, Vacelet J, Le Parco Y (1998) Phylogenetic analysis of the Hsp70 sequences reveals the monophyly of Metazoa and specific phylogenetic relationships between animals and fungi. Mol Biol Evol 15:647–655

    CrossRef  CAS  PubMed  Google Scholar 

  • Borchiellini C, Chombard C, Lafay B, Boury-Esnault N (2000) Molecular systematics of sponges (Porifera). Hydrobiologia 420:15–27

    CrossRef  CAS  Google Scholar 

  • Borchiellini C, Manuel M, Alivon E, Boury-Esnault N, Vacelet J, Parco YL (2001) Sponge paraphyly and the origin of Metazoa. J Evol Biol 14:171–179

    CrossRef  CAS  PubMed  Google Scholar 

  • Borisenko I, Adamski M, Ereskovsky A, Adamska M (2016) Surprisingly rich repertoire of Wnt genes in the demosponge Halisarca dujardini. BMC Evol Biol 16:123

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Boute N, Exposito J-Y, Boury-Esnault N, Vacelet J, Noro N, Miyazaki K, Yoshizato K, Garrone R (1996) Type IV collagen in sponges, the missing link in basement membrane ubiquity. Biol Cell 88:37–44

    CrossRef  CAS  PubMed  Google Scholar 

  • Brien P (1967) Les éponges: leur nature métazoaire-leur gastrulation-leur état colonial. Ann Soc Roy Zool Belg 97:197–235

    Google Scholar 

  • Brosius J (2018) Exaptation at the molecular genetic level. Sci China Life Sci

    Google Scholar 

  • Brunet T, King N (2017) The origin of animal multicellularity and cell differentiation. Dev Cell 43:124–140

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Brusca RC, Brusca GJ (2003). Invertebrates (Sinauer Associates)

    Google Scholar 

  • Carroll S (2005) Bringing Evo Devo to Life. PLOS Biol. W. W. Norton and Company, New York 350 p. ISBN (hardcover) 0-393-06016-0

    Google Scholar 

  • Cavalier-Smith T (2017) Origin of animal multicellularity: precursors, causes, consequences—the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion. Philos Trans R Soc Lond B Biol Sci 372

    CrossRef  Google Scholar 

  • Cavalier-Smith T, Allsopp MTEP, Chao EE, Boury-Esnault N, Vacelet J (1996) Sponge phylogeny, animal monophyly, and the origin of the nervous system: 18S rRNA evidence. Can J Zool 74:2031–2045

    CrossRef  CAS  Google Scholar 

  • Collins AG (1998) Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence. Proc Natl Acad Sci USA 95:15458–15463

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • De Vos L, Rützler K, Boury-Esnault N, Donadey C, Vacelet J (1991) Atlas of sponge morphology. Smithsonian Institution Press, Washington. J Mar Biol Assoc UK 71(4):915–915 

    Google Scholar 

  • Degnan BM, Degnan SM, Naganuma T, Morse DE (1993) The ets multigene family is conserved throughout the Metazoa. Nucleic Acids Res 21:3479–3484

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Degnan BM, Vervoort M, Larroux C, Richards GS (2009) Early evolution of metazoan transcription factors. Curr Opin Genet Dev 19:591–599

    CrossRef  CAS  PubMed  Google Scholar 

  • Deutsch J, Le Guyader H (1998) The neuronal zootype. An hypothesis. Comptes Rendus de l’Académie Des Sciences—Series III—Sciences de La Vie 321:713–719

    CrossRef  CAS  Google Scholar 

  • Dohrmann M, Wörheide G (2017) Dating early animal evolution using phylogenomic data. Sci Rep 7

    Google Scholar 

  • Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749

    CrossRef  CAS  PubMed  Google Scholar 

  • Dunn CW, Leys SP, Haddock SHD (2015) The hidden biology of sponges and ctenophores. Trends Ecol Evol 30:282–291

    CrossRef  PubMed  Google Scholar 

  • Dunning LT, Olofsson JK, Parisod C, Choudhury RR, Moreno-Villena JJ, Yang Y, Dionora J, Quick WP, Park M, Bennetzen JL, et al (2019) Lateral transfers of large DNA fragments spread functional genes among grasses. Proc Natl Acad Sci USA

    Google Scholar 

  • Dunning Hotopp JC (2018) Grafting or pruning in the animal tree: lateral gene transfer and gene loss? BMC Genom 19:470

    CrossRef  CAS  Google Scholar 

  • Eddy SR (2012) The C-value paradox, junk DNA and ENCODE. Curr Biol 22:R898–R899

    CrossRef  CAS  PubMed  Google Scholar 

  • Eerkes-Medrano DI, Leys SP (2006) Ultrastructure and embryonic development of a syconoid calcareous sponge. Invertebr Biol 125:177–194

    CrossRef  Google Scholar 

  • Eitel M, Francis WR, Varoqueaux F, Daraspe J, Osigus H-J, Krebs S, Vargas S, Blum H, Williams GA, Schierwater B et al (2018) Comparative genomics and the nature of placozoan species. PLoS Biol 16:e2005359

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Elliott GRD, Leys SP (2010) Evidence for glutamate, GABA and NO in coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae, Spongillidae). J Exp Biol 213:2310–2321

    CrossRef  CAS  PubMed  Google Scholar 

  • Ellwanger K, Nickel M (2006) Neuroactive substances specifically modulate rhythmic body contractions in the nerveless metazoon Tethya wilhelma (Demospongiae, Porifera). Front Zool 3:7

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Ellwanger K, Eich A, Nickel M (2007) GABA and glutamate specifically induce contractions in the sponge Tethya wilhelma. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:1–11

    CrossRef  CAS  PubMed  Google Scholar 

  • Ereskovsky A (2010) The comparative embryology of sponges, pp 209–230

    CrossRef  Google Scholar 

  • Ereskovsky AV, Borisenko IE, Lapébie P, Gazave E, Tokina DB, Borchiellini C (2015) Oscarella lobularis (Homoscleromorpha, Porifera) regeneration: epithelial morphogenesis and metaplasia. PLoS ONE 10:e0134566

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Fahey B, Degnan BM (2010) Origin of animal epithelia: insights from the sponge genome: evolution of epithelia. Evol Dev 12:601–617

    CrossRef  CAS  PubMed  Google Scholar 

  • Fahey B, Degnan BM (2012) Origin and evolution of laminin gene family diversity. Mol Biol Evol 29:1823–1836

    CrossRef  CAS  PubMed  Google Scholar 

  • Fairclough SR, Chen Z, Kramer E, Zeng Q, Young S, Robertson HM, Begovic E, Richter DJ, Russ C, Westbrook MJ et al (2013) Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol 14:R15

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410

    CrossRef  Google Scholar 

  • Fernandez-Valverde SL, Degnan BM (2016) Bilaterian-like promoters in the highly compact Amphimedon queenslandica genome. Sci Rep 6:22496

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrier DEK (2016) The origin of the Hox/ParaHox genes, the ghost locus hypothesis and the complexity of the first animal. Brief Funct Genomics 15:333–341

    CrossRef  PubMed  Google Scholar 

  • Feuda R, Dohrmann M, Pett W, Philippe H, Rota-Stabelli O, Lartillot N, Wörheide G, Pisani D (2017) Improved modeling of compositional heterogeneity supports sponges as sister to all other animals. Curr Biol 0

    Google Scholar 

  • Fidler AL, Darris CE, Chetyrkin SV, Pedchenko VK, Boudko SP, Brown KL, Gray Jerome W, Hudson JK, Rokas A, Hudson BG (2017) Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues. Elife 6

    Google Scholar 

  • Fierro-Constaín L, Schenkelaars Q, Gazave E, Haguenauer A, Rocher C, Ereskovsky A, Borchiellini C, Renard E (2017) The conservation of the germline multipotency program, from sponges to vertebrates: a stepping stone to understanding the somatic and germline origins. Genome Biol Evol 9:474–488

    PubMed  PubMed Central  Google Scholar 

  • Fortunato S, Adamski M, Bergum B, Guder C, Jordal S, Leininger S, Zwafink C, Rapp HT, Adamska M (2012) Genome-wide analysis of the sox family in the calcareous sponge Sycon ciliatum: multiple genes with unique expression patterns. EvoDevo 3:14

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Fortunato SAV, Adamski M, Ramos OM, Leininger S, Liu J, Ferrier DEK, Adamska M (2014) Calcisponges have a ParaHox gene and dynamic expression of dispersed NK homeobox genes. Nature 514:620–623

    CrossRef  CAS  PubMed  Google Scholar 

  • Fortunato SAV, Adamski M, Adamska M (2015) Comparative analyses of developmental transcription factor repertoires in sponges reveal unexpected complexity of the earliest animals. Mar Genomics 24:121–129

    CrossRef  PubMed  Google Scholar 

  • Fortunato SAV, Vervoort M, Adamski M, Adamska M (2016) Conservation and divergence of bHLH genes in the calcisponge Sycon ciliatum. EvoDevo 7

    Google Scholar 

  • Francis WR, Eitel M, Vargas S, Adamski M, Haddock SH, Krebs S, Blum H, Erpenbeck D, Wörheide G (2017) The genome of the contractile demosponge Tethya wilhelma and the evolution of metazoan neural signalling pathways. BioRxiv 120998

    Google Scholar 

  • Fu X, Adamski M, Thompson EM (2008) Altered miRNA repertoire in the simplified chordate, Oikopleura dioica. Mol Biol Evol 25:1067–1080

    CrossRef  CAS  PubMed  Google Scholar 

  • Funayama N (2018) The cellular and molecular bases of the sponge stem cell systems underlying reproduction, homeostasis and regeneration. Int J Dev Biol 62:513–525

    CrossRef  CAS  PubMed  Google Scholar 

  • Funayama N, Nakatsukasa M, Kuraku S, Takechi K, Dohi M, Iwabe N, Miyata T, Agata K (2005a) Isolation of Ef silicatein and Ef lectin as molecular markers sclerocytes and cells involved in innate immunity in the freshwater sponge Ephydatia fluviatilis. Jzoo 22:1113–1122

    CrossRef  CAS  Google Scholar 

  • Funayama N, Nakatsukasa M, Hayashi T, Agata K (2005b) Isolation of the choanocyte in the fresh water sponge, Ephydatia fluviatilis and its lineage marker. Ef annexin Dev Growth Differ 47:243–253

    CrossRef  CAS  PubMed  Google Scholar 

  • Funayama N, Nakatsukasa M, Mohri K, Masuda Y, Agata K (2010) Piwi expression in archeocytes and choanocytes in demosponges: insights into the stem cell system in demosponges. Evol Dev 12:275–287

    CrossRef  CAS  PubMed  Google Scholar 

  • Galliot B (2012) Hydra, a fruitful model system for 270 years. Int J Dev Biol 56:411–423

    CrossRef  CAS  PubMed  Google Scholar 

  • Ganot P, Zoccola D, Tambutté E, Voolstra CR, Aranda M, Allemand D, Tambutté S (2015) Structural molecular components of septate junctions in cnidarians point to the origin of epithelial junctions in eukaryotes. Mol Biol Evol 32:44–62

    CrossRef  CAS  PubMed  Google Scholar 

  • Gazave E, Lapébie P, Renard E, Bézac C, Boury-Esnault N, Vacelet J, Pérez T, Manuel M, Borchiellini C (2008) NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges. Dev Genes Evol 218:479–489

    CrossRef  CAS  PubMed  Google Scholar 

  • Gazave E, Lapébie P, Richards GS, Brunet F, Ereskovsky AV, Degnan BM, Borchiellini C, Vervoort M, Renard E (2009) Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes. BMC Evol Biol 9:249

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Gazave E, Lavrov DV, Cabrol J, Renard E, Rocher C, Vacelet J, Adamska M, Borchiellini C, Ereskovsky AV (2013) Systematics and molecular phylogeny of the family oscarellidae (homoscleromorpha) with description of two new oscarella species. PLoS ONE 8:e63976

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Gazave E, Guillou A, Balavoine G (2014) History of a prolific family: the Hes/Hey-related genes of the annelid Platynereis. EvoDevo 5:29

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Gilbert SF (2010) Developmental biology, 9th edn. Sinauer Associates Inc, Sunderland, MA

    Google Scholar 

  • Glenner H, Hansen AJ, Sørensen MV, Ronquist F, Huelsenbeck JP, Willerslev E (2004) Bayesian inference of the metazoan phylogeny: a combined molecular and morphological approach. Curr Biol 14:1644–1649

    CrossRef  CAS  PubMed  Google Scholar 

  • Grau-Bové X, Torruella G, Donachie S, Suga H, Leonard G, Richards TA, Ruiz-Trillo I (2017). Dynamics of genomic innovation in the unicellular ancestry of animals. ELife 6

    Google Scholar 

  • Hadzi J (1953) An attempt to reconstruct the system of animal classification. Syst Zool 2(4):145–154

    CrossRef  Google Scholar 

  • Haeckel E (1874) Die Gastraea-Theorie, die phylogenetische Classification des Thierreichsund die Homologie der Keimblätter. Jenaische Zeitschrift für Naturwissenschaft 8:1–55

    Google Scholar 

  • Hahn MW, Wray GA (2002) The g-value paradox. Evol Dev 4:73–75

    CrossRef  PubMed  Google Scholar 

  • Halanych KM (2015) The ctenophore lineage is older than sponges? That cannot be right! Or can it? J Exp Biol 218:592–597

    CrossRef  PubMed  Google Scholar 

  • Halanych KM, Bacheller JD, Aguinaldo AM, Liva SM, Hillis DM, Lake JA (1995) Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267:1641–1643

    CrossRef  CAS  PubMed  Google Scholar 

  • Halanych KM, Whelan NV, Kocot KM, Kohn AB, Moroz LL (2016) Miscues misplace sponges. Proc Natl Acad Sci USA 113:E946–E947

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall C, Rodriguez M, Garcia J, Posfai D, DuMez R, Wictor E, Quintero OA, Hill MS, Rivera AS, Hill AL (2019) Secreted frizzled related protein is a target of PaxB and plays a role in aquiferous system development in the freshwater sponge Ephydatia muelleri. PLoS ONE 14:e0212005

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanelt B, Van Schyndel D, Adema CM, Lewis LA, Loker ES (1996) The phylogenetic position of Rhopalura ophiocomae (Orthonectida) based on 18S ribosomal DNA sequence analysis. Mol Biol Evol 13:1187–1191

    CrossRef  CAS  PubMed  Google Scholar 

  • Hestetun JT, Tompkins-Macdonald G, Rapp HT (2017) A review of carnivorous sponges (Porifera: Cladorhizidae) from the Boreal North Atlantic and Arctic. Zool J Linn Soc 181:1–69

    CrossRef  Google Scholar 

  • Hinck AP, Mueller TD, Springer TA (2016). Structural biology and evolution of the TGF-β Family. Cold Spring Harb Perspect Biol 8

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Hoffmeyer TT, Burkhardt P (2016) Choanoflagellate models—Monosiga brevicollis and Salpingoeca rosetta. Curr Opin Genet Dev 39:42–47

    CrossRef  CAS  PubMed  Google Scholar 

  • Holland LZ (2016) Tunicates. Curr Biol 26:R146–R152

    CrossRef  CAS  PubMed  Google Scholar 

  • Hyman LH (1940). The invertebrates: mollusca I. McGraw-Hill

    Google Scholar 

  • Hyman LH (1951) The invertebrates: Platyhelminthes and Rhynchocoela, the acoelomate Bilateria. Invertebr. Platyhelminthes Rhynchocoela Acoelomate Bilateria 2

    Google Scholar 

  • Jékely G, Paps J, Nielsen C (2015) The phylogenetic position of ctenophores and the origin (s) of nervous systems. EvoDevo 6:1

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Jenner RA, Wills MA (2007) The choice of model organisms in evo-devo. Nat Rev Genet 8:311–314

    CrossRef  CAS  PubMed  Google Scholar 

  • Johnson TA, Milan-Lobo L, Che T, Ferwerda M, Lambu E, McIntosh NL, Li F, He L, Lorig-Roach N, Crews P et al (2017) Identification of the first marine-derived opioid receptor “balanced” agonist with a signaling profile that resembles the endorphins. ACS Chem Neurosci 8:473–485

    CrossRef  CAS  PubMed  Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TK, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Kim W, Cunningham CW (1999) A new perspective on lower metazoan relationships from 18S rDNA sequences. Mol Biol Evol 16:423–427

    CrossRef  CAS  PubMed  Google Scholar 

  • King N, Carroll SB (2001) A receptor tyrosine kinase from choanoflagellates: molecular insights into early animal evolution. PNAS 98:15032–15037

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • King N, Rokas A (2017) Embracing uncertainty in reconstructing early animal evolution. Curr Biol 27:R1081–R1088

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi M, Wada H, Satoh N (1996) Early evolution of the Metazoa and phylogenetic status of diploblasts as inferred from amino acid sequence of elongation factor-1 alpha. Mol Phylogenet Evol 5:414–422

    CrossRef  CAS  PubMed  Google Scholar 

  • Kotpal RL (2012). Modern text book of Zoology: Invertebrates. Rastogi Publications

    Google Scholar 

  • Kruse M, Leys SP, Müller IM, Müller WE (1998) Phylogenetic position of the Hexactinellida within the phylum Porifera based on the amino acid sequence of the protein kinase C from Rhabdocalyptus dawsoni. J Mol Evol 46:721–728

    CrossRef  CAS  PubMed  Google Scholar 

  • Lanna E (2015) Evo-devo of non-bilaterian animals. Genet Mol Biol 38:284–300

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Lapébie P, Gazave E, Ereskovsky A, Derelle R, Bézac C, Renard E, Houliston E, Borchiellini C (2009) WNT/beta-catenin signalling and epithelial patterning in the homoscleromorph sponge Oscarella. PLoS ONE 4:e5823

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Larroux C, Fahey B, Degnan SM, Adamski M, Rokhsar DS, Degnan BM (2007) The NK Homeobox gene cluster predates the origin of Hox genes. Curr Biol 17:706–710

    CrossRef  CAS  PubMed  Google Scholar 

  • Larroux C, Luke GN, Koopman P, Rokhsar DS, Shimeld SM, Degnan BM (2008) Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol 25:980–996

    CrossRef  CAS  PubMed  Google Scholar 

  • Le Bivic A (2013) Evolution and cell physiology. 4. Why invent yet another protein complex to build junctions in epithelial cells? Am J Physiol Cell Physiol 305:C1193–C1201

    CrossRef  PubMed  CAS  Google Scholar 

  • Leger MM, Eme L, Stairs CW, Roger AJ (2018) Demystifying eukaryote lateral gene transfer. BioEssays 40:1700242 (Response to Martin 2017 https://doi.org/10.1002/bies.201700115)

    CrossRef  Google Scholar 

  • Leininger S, Adamski M, Bergum B, Guder C, Liu J, Laplante M, Bråte J, Hoffmann F, Fortunato S, Jordal S, et al (2014) Developmental gene expression provides clues to relationships between sponge and Eumetazoan body plans. Nat Commun 5:ncomms4905

    Google Scholar 

  • Leys SP (2015) Elements of a “nervous system” in sponges. J Exp Biol 218:581–591

    CrossRef  PubMed  Google Scholar 

  • Leys SP, Hill A (2012) The physiology and molecular biology of sponge tissues. In: Advances in marine biology. Elsevier, pp 1–56

    Google Scholar 

  • Leys SP, Riesgo A (2012) Epithelia, an evolutionary novelty of metazoans. J Exp Zool (Mol Dev Evol) 318:438–447

    CrossRef  Google Scholar 

  • Leys SP, Nichols SA, Adams EDM (2009) Epithelia and integration in sponges. Integr Comp Biol 49:167–177

    CrossRef  PubMed  Google Scholar 

  • Ludeman DA, Farrar N, Riesgo A, Paps J, Leys SP (2014) Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges. BMC Evol Biol 14:3

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Mah JL, Leys SP (2017) Think like a sponge: the genetic signal of sensory cells in sponges. Dev Biol 431:93–100

    CrossRef  CAS  PubMed  Google Scholar 

  • Manuel M (2001) Origine et evolution des mecanismes moleculaires controlant la morphogenese chez les metazoaires : un nouveau modele spongiaire, Sycon raphanus (calcispongia, calcaronea) thesis. Paris 11

    Google Scholar 

  • Manuel M, Le Parco Y (2000) Homeobox gene diversification in the calcareous sponge, Sycon raphanus. Mol Phylogenet Evol 17:97–107

    CrossRef  CAS  PubMed  Google Scholar 

  • Marlow H, Arendt D (2014) Evolution: ctenophore genomes and the origin of neurons. Curr Biol 24:R757–R761

    CrossRef  CAS  PubMed  Google Scholar 

  • Martin WF (2017) Too much eukaryote LGT. Bioessays 39

    CrossRef  Google Scholar 

  • Medina M, Collins AG, Silberman JD, Sogin ML (2001) Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc Natl Acad Sci USA 98:9707–9712

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller PW, Clarke DN, Weis WI, Lowe CJ, Nelson WJ (2013) The Evolutionary origin of epithelial cell-cell adhesion mechanisms. Curr Top Membr 72:267–311

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller PW, Pokutta S, Mitchell JM, Chodaparambil JV, Clarke DN, Nelson WJ, Weis WI, Nichols SA (2018) Analysis of a vinculin homolog in a sponge (phylum Porifera) reveals that vertebrate-like cell adhesions emerged early in animal evolution. J Biol Chem 293:11674–11686

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Mills DB, Francis WR, Vargas S, Larsen M, Elemans CP, Canfield DE, Wörheide G (2018) The last common ancestor of animals lacked the HIF pathway and respired in low-oxygen environments. Elife 7

    Google Scholar 

  • Mohri K, Nakatsukasa M, Masuda Y, Agata K, Funayama N (2008) Toward understanding the morphogenesis of siliceous spicules in freshwater sponge: differential mRNA expression of spicule-type-specific silicatein genes in Ephydatia fluviatilis. Dev Dyn 237:3024–3039

    CrossRef  CAS  PubMed  Google Scholar 

  • Moroz LL (2015) Convergent evolution of neural systems in ctenophores. J Exp Biol 218:598–611

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Moroz LL, Kohn AB (2015) unbiased view of synaptic and neuronal gene complement in Ctenophores: are there pan-neuronal and pan-synaptic genes across Metazoa? Integr Comp Biol 55:1028–1049

    PubMed  PubMed Central  Google Scholar 

  • Moroz LL, Kohn AB (2016) Independent origins of neurons and synapses: insights from ctenophores. Philos Trans R Soc Lond B Biol Sci 371

    CrossRef  CAS  Google Scholar 

  • Moroz LL, Kocot KM, Citarella MR, Dosung S, Norekian TP, Povolotskaya IS, Grigorenko AP, Dailey C, Berezikov E, Buckley KM et al (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature 510:109–114

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris PJ (1993) The developmental role of the extracellular matrix suggests a monophyletic origin of the kingdom animalia. Evolution 47:152–165

    CrossRef  PubMed  Google Scholar 

  • Mouchel-Vielh E, Rigolot C, Gibert JM, Deutsch JS (1998) Molecules and the body plan: the Hox genes of Cirripedes (Crustacea). Mol Phylogenet Evol 9:382–389

    CrossRef  CAS  PubMed  Google Scholar 

  • Müller WE (1995) Molecular phylogeny of Metazoa (animals): monophyletic origin. Naturwissenschaften 82:321–329

    CrossRef  PubMed  Google Scholar 

  • Müller WEG (1998) Molecular phylogeny of Eumetazoa: genes in sponges (Porifera) give evidence for monophyly of animals. In: Molecular evolution: evidence for monophyly of metazoa. Springer, pp 89–132

    Google Scholar 

  • Müller WEG, Wang X, Grebenjuk VA, Korzhev M, Wiens M, Schlossmacher U, Schröder HC (2012) Common genetic denominators for Ca++-based skeleton in Metazoa: role of osteoclast-stimulating factor and of carbonic anhydrase in a calcareous sponge. PLoS ONE 7:e34617

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Murray PS, Zaidel-Bar R (2014) Pre-metazoan origins and evolution of the cadherin adhesome. Biol Open 3:1183–1195

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Nakanishi N, Sogabe S, Degnan BM (2014) Evolutionary origin of gastrulation: insights from sponge development. BMC Biol 12:26

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakanishi N, Stoupin D, Degnan SM, Degnan BM (2015) Sensory flask cells in sponge larvae regulate metamorphosis via calcium signaling. Integr Comp Biol 55:1018–1027

    CrossRef  CAS  PubMed  Google Scholar 

  • Nedelcu AM (2019) Independent evolution of complex development in animals and plants: deep homology and lateral gene transfer. Dev Genes Evol 229:25–34

    CrossRef  PubMed  Google Scholar 

  • Nichols SA, Dirks W, Pearse JS, King N (2006) Early evolution of animal cell signaling and adhesion genes. Proc Natl Acad Sci USA 103:12451–12456

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Nichols SA, Roberts BW, Richter DJ, Fairclough SR, King N (2012) Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/β-catenin complex. Proc Natl Acad Sci USA 109:13046–13051

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Nickel M (2010) Evolutionary emergence of synaptic nervous systems: what can we learn from the non-synaptic, nerveless Porifera? Invertebr Biol 129:1–16

    CrossRef  Google Scholar 

  • Nosenko T, Schreiber F, Adamska M, Adamski M, Eitel M, Hammel J, Maldonado M, Müller WEG, Nickel M, Schierwater B et al (2013) Deep metazoan phylogeny: when different genes tell different stories. Mol Phylogenet Evol 67:223–233

    CrossRef  PubMed  Google Scholar 

  • Oakley TH (2017) Furcation and fusion: the phylogenetics of evolutionary novelty. Dev Biol 431:69–76

    CrossRef  CAS  PubMed  Google Scholar 

  • Oxusoff L, Préa P, Perez Y (2018) A complete logical approach to resolve the evolution and dynamics of mitochondrial genome in bilaterians. PLoS ONE 13:e0194334

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Parra-Acero H, Ros-Rocher N, Perez-Posada A, Kożyczkowska A, Sánchez-Pons N, Nakata A, Suga H, Najle SR, Ruiz-Trillo I (2018) Transfection of Capsaspora owczarzaki, a close unicellular relative of animals. Development 145

    Google Scholar 

  • Pastrana CC, DeBiasse MB, Ryan JF (2019) Sponges lack ParaHox genes. Genome Biol Evol

    Google Scholar 

  • Pawlowski J, Montoya-Burgos JI, Fahrni JF, Wüest J, Zaninetti L (1996) Origin of the Mesozoa inferred from 18S rRNA gene sequences. Mol Biol Evol 13:1128–1132

    CrossRef  CAS  PubMed  Google Scholar 

  • Peña JF, Alié A, Richter DJ, Wang L, Funayama N, Nichols SA (2016) Conserved expression of vertebrate microvillar gene homologs in choanocytes of freshwater sponges. Evodevo 7:13

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Peterson KJ, Butterfield NJ (2005) Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proc Natl Acad Sci USA 102:9547–9552

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson KJ, Eernisse DJ (2001) Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evol Dev 3:170–205

    CrossRef  CAS  PubMed  Google Scholar 

  • Pett W, Adamski M, Adamska M, Francis WR, Eitel M, Pisani D, Wörheide G (2019) The role of homology and orthology in the phylogenomic analysis of metazoan gene content. Mol Biol Evol 36:643–649

    CrossRef  PubMed  Google Scholar 

  • Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Quéinnec E et al (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:706–712

    CrossRef  CAS  PubMed  Google Scholar 

  • Philippe H, Brinkmann H, Lavrov DV, Littlewood DTJ, Manuel M, Wörheide G, Baurain D (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9:e1000602

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Pick KS, Philippe H, Schreiber F, Erpenbeck D, Jackson DJ, Wrede P, Wiens M, Alié A, Morgenstern B, Manuel M et al (2010) Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 27:1983–1987

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Pisani D, Pett W, Dohrmann M, Feuda R, Rota-Stabelli O, Philippe H, Lartillot N, Wörheide G (2015) Genomic data do not support comb jellies as the sister group to all other animals. Proc Natl Acad Sci USA 112:15402–15407

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramulu HG, Raoult D, Pontarotti P (2012) The rhizome of life: what about metazoa? Front Cell Infect Microbiol 2:50

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Renard E, Vacelet J, Gazave E, Lapébie P, Borchiellini C, Ereskovsky AV (2009) Origin of the neuro-sensory system: new and expected insights from sponges. Integr Zool 4:294–308

    CrossRef  PubMed  Google Scholar 

  • Renard E, Eve G, Fierro-Constain L, Schenkelaars Q, Ereskovsky A, Vacelet JV, Borchiellini CB (2013). Porifera (Sponges): recent knowledge and new perspectives. In eLS, John Wiley & Sons, Ltd (Ed.). https://doi.org/10.1002/9780470015902.a0001582.pub2  

  • Renard E, Leys SP, Wörheide G, Borchiellini C (2018) Understanding animal evolution: the added value of sponge transcriptomics and genomics. BioEssays 40:1700237

    CrossRef  Google Scholar 

  • Rentzsch F, Layden M, Manuel M (2017) The cellular and molecular basis of cnidarian neurogenesis. Wiley Interdisc Rev Dev Biol 6:e257

    CrossRef  Google Scholar 

  • Revilla-I-Domingo R, Schmidt C, Zifko C, Raible F (2018) Establishment of transgenesis in the demosponge Suberites domuncula. Genetics 210:435–443

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds AS (2019) Ernst Haeckel and the philosophy of sponges. Theory Biosci

    Google Scholar 

  • Richards GS, Degnan BM (2009) The dawn of developmental signaling in the metazoa. Cold Spring Harb Symp Quant Biol 74:81–90

    CrossRef  CAS  PubMed  Google Scholar 

  • Richards GS, Degnan BM (2012) The expression of delta ligands in the sponge Amphimedon queenslandica suggests an ancient role for Notch signaling in metazoan development. Evodevo 3:15

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Richards GS, Simionato E, Perron M, Adamska M, Vervoort M, Degnan BM (2008) Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit. Curr Biol 18:1156–1161

    CrossRef  CAS  PubMed  Google Scholar 

  • Richter DJ, Fozouni P, Eisen MB, King N (2018) Gene family innovation, conservation and loss on the animal stem lineage. Elife 7

    Google Scholar 

  • Riesgo A, Farrar N, Windsor PJ, Giribet G, Leys SP (2014) The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges. Mol Biol Evol 31:1102–1120

    CrossRef  CAS  PubMed  Google Scholar 

  • Rivera A, Winters I, Rued A, Ding S, Posfai D, Cieniewicz B, Cameron K, Gentile L, Hill A (2013) The evolution and function of the Pax/Six regulatory network in sponges. Evol Dev 15:186–196

    CrossRef  CAS  PubMed  Google Scholar 

  • Rivera AS, Hammel JU, Haen KM, Danka ES, Cieniewicz B, Winters IP, Posfai D, Wörheide G, Lavrov DV, Knight SW et al (2011) RNA interference in marine and freshwater sponges: actin knockdown in Tethya wilhelma and Ephydatia muelleri by ingested dsRNA expressing bacteria. BMC Biotechnol 11:67

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Russell JJ, Theriot JA, Sood P, Marshall WF, Landweber LF, Fritz-Laylin L, Polka JK, Oliferenko S, Gerbich T, Gladfelter A, et al (2017) Non-model model organisms. BMC Biol 15(1):55

    Google Scholar 

  • Ryan JF (2014) Did the ctenophore nervous system evolve independently? Zoology (Jena) 117:225–226

    CrossRef  Google Scholar 

  • Ryan JF, Chiodin M (2015) Where is my mind? How sponges and placozoans may have lost neural cell types. Philos Trans R Soc Lond B Biol Sci 370

    CrossRef  Google Scholar 

  • Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang I-F, Tidor B, Degnan BM, Oakley TH, Kosik KS (2007) A post-synaptic scaffold at the origin of the animal kingdom. PLoS ONE 2:e506

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Schenkelaars Q, Fierro-Constain L, Renard E, Hill AL, Borchiellini C (2015) Insights into Frizzled evolution and new perspectives. Evol Dev 17:160–169

    CrossRef  CAS  PubMed  Google Scholar 

  • Schenkelaars Q, Fierro-Constain L, Renard E, Borchiellini C (2016a) Retracing the path of planar cell polarity. BMC Evol Biol 16:69

    Google Scholar 

  • Schenkelaars Q, Quintero O, Hall C, Fierro-Constain L, Renard E, Borchiellini C, Hill AL (2016b) ROCK inhibition abolishes the establishment of the aquiferous system in Ephydatia muelleri (Porifera, Demospongiae). Dev Biol 412:298–310

    CrossRef  CAS  PubMed  Google Scholar 

  • Schenkelaars Q, Pratlong M, Kodjabachian L, Fierro-Constain L, Vacelet J, Le Bivic A, Renard E, Borchiellini C (2017) Animal multicellularity and polarity without Wnt signaling. Sci Rep 7:15383

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Schippers KJ, Nichols SA, Wittkopp P (2018) Evidence of Signaling and adhesion roles for β-Catenin in the sponge Ephydatia muelleri. Mol Biol Evol 35:1407–1421

    CrossRef  CAS  PubMed  Google Scholar 

  • Sebé-Pedrós A, Ruiz-Trillo I (2017) Evolution and classification of the T-Box transcription factor family. Curr Top Dev Biol 122:1–26

    CrossRef  PubMed  Google Scholar 

  • Sebé-Pedrós A, Ariza-Cosano A, Weirauch MT, Leininger S, Yang A, Torruella G, Adamski M, Adamska M, Hughes TR, Gómez-Skarmeta JL et al (2013) Early evolution of the T-box transcription factor family. Proc Natl Acad Sci USA 110:16050–16055

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Sebé-Pedrós A, Degnan BM, Ruiz-Trillo I (2017) The origin of Metazoa: a unicellular perspective. Nat Rev Genet 18:498–512

    CrossRef  PubMed  CAS  Google Scholar 

  • Sebé-Pedrós A, Chomsky E, Pang K, Lara-Astiaso D, Gaiti F, Mukamel Z, Amit I, Hejnol A, Degnan BM, Tanay A (2018) Early metazoan cell type diversity and the evolution of multicellular gene regulation. Nat Ecol Evol 2:1176–1188

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Simion P, Philippe H, Baurain D, Jager M, Richter DJ, Di Franco A, Roure B, Satoh N, Quéinnec É, Ereskovsky A et al (2017) A large and consistent phylogenomic dataset supports sponges as the sister group to all other animals. Curr Biol 27:958–967

    CrossRef  CAS  PubMed  Google Scholar 

  • Simpson TL (1984) The cell biology of sponges. Springer-Verlag New York Inc.

    Google Scholar 

  • Slack JM, Holland PW, Graham CF (1993) The zootype and the phylotypic stage. Nature 361:490–492

    CrossRef  CAS  PubMed  Google Scholar 

  • Sogabe S, Nakanishi N, Degnan BM (2016) The ontogeny of choanocyte chambers during metamorphosis in the demosponge Amphimedon queenslandica. EvoDevo 7:6. https://doi.org/10.1186/s13227-016-0042-x

  • Sperling EA, Pisani D, Peterson KJ (2007) Poriferan paraphyly and its implications for Precambrian palaeobiology. Geol Soc 286:355–368 London, Special Publications

    CrossRef  Google Scholar 

  • Sperling EA, Peterson KJ, Pisani D (2009) Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Mol Biol Evol 26:2261–2274

    CrossRef  CAS  PubMed  Google Scholar 

  • Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U et al (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Stolfi A, Christiaen L (2012) Genetic and genomic toolbox of the chordate Ciona intestinalis. Genetics 192:55–66

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Suga H, Ono K, Miyata T (1999) Multiple TGF-beta receptor related genes in sponge and ancient gene duplications before the parazoan-eumetazoan split. FEBS Lett 453:346–350

    CrossRef  CAS  PubMed  Google Scholar 

  • Suga H, Chen Z, de Mendoza A, Sebé-Pedrós A, Brown MW, Kramer E, Carr M, Kerner P, Vervoort M, Sánchez-Pons N et al (2013) The capsaspora genome reveals a complex unicellular prehistory of animals. Nat Commun 4:2325

    CrossRef  PubMed  CAS  Google Scholar 

  • Syvanen M (1984) The evolutionary implications of mobile genetic elements. Annu Rev Genet 18:271–293

    CrossRef  CAS  PubMed  Google Scholar 

  • Tickle C, Urrutia AO (2017) Perspectives on the history of evo-devo and the contemporary research landscape in the genomics era. Philos Trans Roy Soc B: Biol Sci 372:20150473

    CrossRef  Google Scholar 

  • Tompkins-Macdonald GJ, Gallin WJ, Sakarya O, Degnan B, Leys SP, Boland LM (2009) Expression of a poriferan potassium channel: insights into the evolution of ion channels in metazoans. J Exp Biol 212:761–767

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueda N, Richards GS, Degnan BM, Kranz A, Adamska M, Croll RP, Degnan SM (2016) An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge. Sci Rep 6:37546

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Uzzell T, Corbin KW (1971) Fitting discrete probability distributions to evolutionary events. Science 172:1089–1096

    CrossRef  CAS  PubMed  Google Scholar 

  • Voigt O, Adamski M, Sluzek K, Adamska M (2014) Calcareous sponge genomes reveal complex evolution of α-carbonic anhydrases and two key biomineralization enzymes. BMC Evol Biol 14:230

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Wells GD, Tang Q-Y, Heler R, Tompkins-MacDonald GJ, Pritchard EN, Leys SP, Logothetis DE, Boland LM (2012) A unique alkaline pH-regulated and fatty acid-activated tandem pore domain potassium channel (K2P) from a marine sponge. J Exp Biol 215:2435–2444

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Whelan NV, Kocot KM, Halanych KM (2015) Employing phylogenomics to resolve the relationships among Cnidarians, Ctenophores, Sponges, Placozoans, and Bilaterians. Integr Comp Biol 55:1084–1095

    CrossRef  PubMed  Google Scholar 

  • Whelan NV, Kocot KM, Moroz TP, Mukherjee K, Williams P, Paulay G, Moroz LL, Halanych KM (2017). Ctenophore relationships and their placement as the sister group to all other animals. Nat Ecol Evol 1(11):1737-1746. Epub 2017 Oct 9. https://doi.org/10.1038/s41559-017-0331-3

    CrossRef  Google Scholar 

  • Whittaker RH (1959) On the broad classification of organisms. Q Rev Biol 34:210–226

    CrossRef  CAS  PubMed  Google Scholar 

  • Windsor PJ, Leys SP (2010) Wnt signaling and induction in the sponge aquiferous system: evidence for an ancient origin of the organizer. Evol Dev 12:484–493

    CrossRef  CAS  PubMed  Google Scholar 

  • Windsor Reid PJ, Matveev E, McClymont A, Posfai D, Hill AL, Leys SP (2018) Wnt signaling and polarity in freshwater sponges. BMC Evol Biol 18:12

    CrossRef  PubMed  PubMed Central  CAS  Google Scholar 

  • Zrzavý J, Mihulka S, Kepka P, Bezděk A, Tietz D (1998) Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics 14:249–285

    CrossRef  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the Région Provence Alpes Côte d’Azur and the French Research ministry for the PhD funding they provided to L. Fierro Ph.Ds of L. Fierro-Constain’s and the Q. Schenkelaars respectively. The authors thank Prof. Stephen Prime (University of Bristol) and Mr. Thomas Smith, two native English speakers, for providing proofreading services. The authors are grateful to Dr. Pierre Pontarotti and Dr. Anne Chenuil-Maurel for constructive comments for Sect. 7.2. The authors thank the French National Center for Scientific Research (CNRS), Aix-Marseille University and the Amidex foundation for providing funds to support fundamental research.

Author information

Authors and Affiliations

  1. Aix Marseille Univ, Avignon Université, CNRS, IRD, IMBE, Marseille, France, Station Marine d’Endoume, Rue de la Batterie des Lions, 13007, Marseille, France

    Quentin Schenkelaars, Amélie Vernale, Laura Fierro-Constaín, Carole Borchiellini & Emmanuelle Renard

  2. Department of Genetics and Evolution, Faculty of Sciences, Institute of Genetics and Genomics in Geneva (IGe3), University of Geneva, Geneva, Switzerland

    Quentin Schenkelaars

  3. Aix Marseille Univ, CNRS, IBDM, UMR 7288, Marseille, France

    Amélie Vernale & Emmanuelle Renard

Authors
  1. Quentin Schenkelaars
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amélie Vernale
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura Fierro-Constaín
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carole Borchiellini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Emmanuelle Renard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emmanuelle Renard .

Editor information

Editors and Affiliations

  1. CNRS and IHU, Aix-Marseille University, Marseille, France

    Pierre Pontarotti

Rights and permissions

Reprints and Permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Verify currency and authenticity via CrossMark

Cite this chapter

Schenkelaars, Q., Vernale, A., Fierro-Constaín, L., Borchiellini, C., Renard, E. (2019). A Look Back Over 20 Years of Evo-Devo Studies on Sponges: A Challenged View of Urmetazoa. In: Pontarotti, P. (eds) Evolution, Origin of Life, Concepts and Methods. Springer, Cham. https://doi.org/10.1007/978-3-030-30363-1_7

Download citation