Porifera
Abstract
Poriferans (sponges) are sessile aquatic (largely marine) animals that are found in almost all benthic habitats. There are an estimated 15,000 species living today, although many have not been described (reviewed in Hooper and Van Soest 2002). The sponge body plan is amongst the simplest in the animal kingdom and lacks nerve and muscle cells and a centralised gut (reviewed in Simpson 1984; Ereskovsky 2010; Leys and Hill 2012). Their body plan and ecology, and thus their evolution, appear to be intimately associated with the diversity of microbial symbionts they harbour (reviewed in Hentschel et al. 2012; Thacker and Freeman 2012), as is the case with other metazoans.
Keywords
Pigment Cell Body Plan Inner Cell Mass Nurse Cell Posterior PoleNotes
Acknowledgements
Because of space limitations, we are unable to cite many important contributions to the field of sponge developmental biology – we acknowledge these here. We also acknowledge the fine contributions of past and present members of the laboratories of B. Degnan, S. Degnan, and M. Adamska towards our understanding of Amphimedon and Sycon biology. Research presented in this chapter was made possible by the generous support of the Australian Research Council to BMD, SMD, and MA and the Sars International Centre for Marine Molecular Biology to MA.
References
- Adamska M, Degnan SM, Green KM, Adamski M, Craigie A, Larroux C, Degnan BM (2007a) Wnt and TGF-β expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS ONE 2:e1031PubMedCentralPubMedCrossRefGoogle Scholar
- Adamska M, Matus DQ, Adamski M, Green K, Rokhsar DS, Martindale MQ, Degnan BM (2007b) The evolutionary origin of hedgehog proteins. Curr Biol 17:R836–R837PubMedCrossRefGoogle 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 12:492–518CrossRefGoogle Scholar
- Adamska M, Zwafink C, Green K, Degnan BM (2011) What sponges can tell us about the evolution of developmental processes. Zoology 114:1–10PubMedCrossRefGoogle Scholar
- Amano S, Hori I (1992) Metamorphosis of calcareous sponges. 1. Ultrastructure of free-swimming larvae. Invert Reprod Dev 21:81–90CrossRefGoogle Scholar
- Amano S, Hori I (1993) Metamorphosis of calcareous sponges. 2. Cell rearrangement and differentiation in metamorphosis. Invert Reprod Dev 24:13–26CrossRefGoogle Scholar
- Amano S, Hori I (2001) Metamorphosis of coeloblastula performed by multipotential larval flagellated cells in the calcareous sponge Leucosolenia laxa. Biol Bull 200:20–32PubMedCrossRefGoogle Scholar
- Anavy L, Levin M, Khair S, Nakanishi N, Fernandez-Valverde SL, Degnan BM, Yanai I (2014) BLIND ordering of large-scale transcriptomic developmental timecourses. Development 141:1161–1166PubMedCrossRefGoogle Scholar
- Bergquist PR, Green CR (1977) Ultrastructural-study of settlement and metamorphosis in sponge larvae. Cahiers Biol Mar 18:289–302Google Scholar
- Boury-Esnault N, Efremova S, Bézac C, Vacelet J (1999) Reproduction of a hexactinellid sponge: first description of gastrulation by cellular delamination in the Porifera. Invert Reprod Dev 35:187–201Google Scholar
- Bridgham JT, Eick GN, Larroux C, Deshpande K, Harms MJ, Gauthier ME, Ortlund EA, Degnan BM, Thornton JW (2010) Protein evolution by molecular tinkering: diversification of the nuclear receptor superfamily from a ligand-dependent ancestor. PLoS Biol 8:e1000497PubMedCentralPubMedCrossRefGoogle Scholar
- Degnan SM, Degnan BM (2006) The origin of the pelagobenthic metazoan life cycle: what’s sex got to do with it? Integr Comp Biol 46:683–690PubMedCrossRefGoogle Scholar
- Degnan SM, Degnan BM (2010) The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life cycle evolution. Phil Trans R Soc B 365:641–651PubMedCentralPubMedCrossRefGoogle Scholar
- Degnan BM, Leys SP, Larroux C (2005) Sponge development and antiquity of animal pattern formation. Integr Comp Biol 45:335–341PubMedCrossRefGoogle Scholar
- De Vos L, Rutzler K, Boury-Esnault N, Donadey C, Vacelet J (1991) Atlas of sponge morphology. Smithsonian Institution Press, Washington D.C. 128 ppGoogle Scholar
- Eerkes-Medrano DI, Leys SP (2006) Ultrastructure and embryonic development of a syconoid calcareous sponge. Invert Biol 125:177–194CrossRefGoogle Scholar
- Ereskovsky AV, Boury-Esnault N (2002) Cleavage pattern in Oscarella species (Porifera, Demospongiae, Homoscleromorpha): transmission of maternal cells and symbiotic bacteria. J Nat Hist 36:1761–1775CrossRefGoogle Scholar
- Ereskovsky A (2010) The comparative embryology of sponges. Springer, NetherlandsGoogle Scholar
- Ereskovsky AV, Tokina DB, Bezac C, Boury-Esnault N (2007) Metamorphosis of cinctoblastula larvae (Homoscleromorpha, Porifera). J Morphol 268:518–528PubMedCrossRefGoogle Scholar
- Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D, Peterson KJ (2011) The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334:1091–1097PubMedCrossRefGoogle Scholar
- Fahey B (2011) Origin of animal epithelia: insights from the genome of the demosponge Amphimedon queenslandica. PhD Thesis The University of QueenslandGoogle Scholar
- Fahey B, Degnan BM (2010) Origin of animal epithelia: insights from the sponge genome. Evol Dev 12:601–617PubMedCrossRefGoogle Scholar
- Fahey B, Larroux C, Woodcroft BJ, Degnan BM (2008) Does the high gene density in the sponge NK homeobox gene cluster reflect limited regulatory capacity? Biol Bull 214:205–217PubMedCrossRefGoogle Scholar
- Fell PE (1969) The involvement of nurse cells in oogenesis and embryonic development in the marine sponge, Haliclona ecbasis. J Morph 127:133–150.Google Scholar
- Fortunato SAV (2014) Gene loss, lineage specific expansions and dynamic expression of developmental transcription factors in calcareous sponges. PhD Thesis University of BergenGoogle 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 23:142012Google Scholar
- Fortunato S, Leininger S, Adamska M (2014) Evolution of the Pax-Six-Eya-Dach network: the calcisponge case study. EvoDevo 5:23PubMedCentralPubMedCrossRefGoogle Scholar
- Fortunato S, Adamski M, Mendivil O, Leininger S, Liu J, Ferrier DEK, Adamska M. Calcisponges have a ParaHox gene and dynamic expression of dispersed NK homeobox genes. Nature 514:620–623Google Scholar
- Franzen W (1988) Oogenesis and larval development of Scypha ciliata (Porifera, Calcarea). Zoomorphology 107:349–357CrossRefGoogle Scholar
- Funayama N (2012) The stem cell system in demosponges: suggested involvement of two types of cells: archeocytes (active stem cells) and choanocytes (food-entrapping flagellated cells). Dev Genes Evol 223:23–38PubMedCrossRefGoogle Scholar
- Gauthier MEA (2010) Developing a sense of self: exploring the evolution of immune and allorecognition mechanisms in metazoans using the demosponge Amphimedon queenslandica. PhD Thesis The University of QueenslandGoogle Scholar
- Gauthier M, Degnan BM (2008) The transcription factor NF-κB in the sponge Amphimedon queenslandica: insights into the evolutionary origin of the Rel homology domain. Dev Genes Evol 218:23–32PubMedCrossRefGoogle Scholar
- Gauthier MEA, Du Pasquier L, Degnan BM (2010) The genome of the sponge Amphimedon queenslandica provides new perspectives into the origin of Toll-like and Interleukin1 receptor pathways. Evol Dev 12:519–533PubMedCrossRefGoogle Scholar
- Gazave E, Lapebie P, Ereskovsky AV, Vacelet J, Renard E, Cardenas P, Borchiellini C (2012) No longer demospongiae: homoscleromorpha formal nomination as a fourth class of Porifera. Hydrobiologia 687:3–10CrossRefGoogle Scholar
- Gonobobleva EL, Ereskovsky AV (2004) Metamorphosis of the larva of Halisarca dujardini (Demospongiae, Halisarcida). Bull Inst R Sci Nat.Belg 74:101–114Google Scholar
- Haeckel E (1870). Ueber den Organismus der Schwame und ihre Verwndtschaft mit den Corallen. Jena Zeitsch Naturwiss 5:207–235Google Scholar
- Haeckel E (1874) Die Gastrae Theorie, die phylogenetische Classification des Thierreichs und die Homologie der Keimblatter. Jena Zeitsch Naturwiss 8:1–55Google Scholar
- Hayward DC, Samuel G, Pontynen PC, Catmull J, Saint R, Miller DJ, Ball EE (2002) Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc Natl Acad Sci USA 99:8106–8111Google Scholar
- Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nature Rev Microbiol 10:641–654CrossRefGoogle Scholar
- Hill MS, Hill AL, Lopez J, Peterson KJ, Pomponi S, Diaz MC, Thacker RW, Adamska M, Boury-Esnault N, Cárdenas P, Chaves-Fonnegra A, Danka E, De Laine BO, Formica D, Hajdu E, Lobo-Hajdu G, Klontz S, Morrow CC, Patel J, Picton B, Pisani D, Pohlmann D, Redmond NE, Reed J, Richey S, Riesgo A, Rubin E, Russell Z, Rützler K, Sperling EA, di Stefano M, Tarver JE, Collins AG (2013) Reconstruction of family-level phylogenetic relationships within Demospongiae (Porifera) using nuclear encoded housekeeping genes. PLoS ONE 8:e50437PubMedCentralPubMedCrossRefGoogle Scholar
- Hooper JNA, Van Soest RWM (eds) (2002) Systema Porifera, vol 1, A guide to the classification of sponges. Kluwer Academic/Plenum Publishers, New York, xlvii, 1708Google Scholar
- Kaye HR (1990) Reproduction in West Indian commercial sponges: oogenesis, larval development, and behavior. In: new Perspectives in sponge biology. Rützler K, ed., Smithsonian Institution Press, Washington DC:161–169Google Scholar
- Kaye HR, Reiswig HM (1991) Sexual reproduction in four Caribbean commercial sponges. II. Oogenesis and transfer of bacterial symbionts. lnvert Reprod Dev 19:1–11Google Scholar
- Knoblich JA (2010) Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 11:849–860Google Scholar
- Larroux C (2007) Genome content and developmental expression of transcription factor genes in the demosponge Amphimedon queenslandica: insights into the Ancestral Metazoan Developmental Program. PhD Thesis The University of QueenslandGoogle Scholar
- Larroux C, Fahey B, Liubicich D, Hinman VF, Gauthier M, Gongora M, Green K, Wörheide G, Leys SP, Degnan BM (2006) Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evol Dev 8:150–173PubMedCrossRefGoogle 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 17:706–710PubMedCrossRefGoogle Scholar
- Leininger S, Adamski M, Bergum B, Guder C, Liu J, Laplante M, Bråte J, Hoffmann F, Fortunato S, Jordal S, Rapp HT, Adamska M (2014) Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans. Nat Commun 5:3905PubMedCrossRefGoogle Scholar
- Leys SP (2004) Gastrulation in sponges. In Gastrulation, From Cells to Embryo. Edited by Stern CD. New York: cold Spring Harbor Laboratory Press:23–31Google Scholar
- Leys SP, Degnan BM (2001) The cytological basis of photoresponsive behavior in a sponge larva. Biol Bull 201:323–338PubMedCrossRefGoogle Scholar
- Leys SP, Degnan BM (2002) Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes. Invert Biol 121:171–189CrossRefGoogle Scholar
- Leys SP, Eerkes-Medrano D (2005) Gastrulation in calcareous sponges: in search of Haeckel’s gastraea. Integ Comp Biol 45:342–351CrossRefGoogle Scholar
- Leys SP, Ereskovsky AV (2006) Embryogenesis and larval differentiation in sponges. Can. J. Zool. 84:262–287Google Scholar
- Leys SP, Hill A (2012) The physiology and molecular biology of sponge tissues. Adv Mar Biol 62:1–56PubMedCrossRefGoogle Scholar
- Leys SP, Cronin TW, Degnan BM, Marshall JN (2002) Spectral sensitivity in a sponge larva. J Comp Physiol A 188:199–202CrossRefGoogle Scholar
- Maldonado M, Bergquist PR (2002) Phylum Porifera. In: atlas of marine invertebrate larvae. Young CM, ed, Academic press, London:21–50Google Scholar
- Manuel M (2001) Origine et évolution des mécanismes moléculaires contrôlant la morphogenèse chez les Métazoaires: un nouveau modèle spongiaire, Sycon raphanus (Calcispongia, Calcaronea). PhD Thesis Université de Paris XIGoogle Scholar
- Maritz K, Calcino A, Fahey B, Degnan BM, Degnan SM (2010) Remarkable consistency of larval supply in the spermcast-mating demosponge Amphimedon queenslandica (Hooper and van Soest). Open Mar Biol J 4:57–64CrossRefGoogle Scholar
- Matus DQ, Pang K, Marlow H, Dunn CW, Thomsen GH, Martindale MQ (2006) Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc Natl Acad Sci USA 103:11195–11200Google Scholar
- McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 110:3229–3236PubMedCentralPubMedCrossRefGoogle Scholar
- Medioni C, Mowry K, Besse F (2012) Principles and roles of mRNA localization in animal development. Development 139:3263–3276Google Scholar
- Meewis H (1939) Contribution a l’étude de l’embryogenése de Chalinulidae: haliclona limbata. Ann Soc R Zool Belg 70:201–243Google Scholar
- Misevic GN SV, Burger MM (1990) Larval metamorphosis of Microciona prolifera: evidence against the reversal of layers. In: Rt K (ed) New perspectives in sponge biology. Smithsonian Institution Press, Washington, DC, pp 182–187Google Scholar
- Misevic GN, Burger MM (1982) The molecular basis of species specific cell-cell recognition in marine sponges, and a study on organogenesis during metamorphosis. Prog Clin Biol Res B 85:193–209Google Scholar
- Moroz LL, Kocot KM, Citarella MR, Dosung S, Norekian TP, Povolotskaya IS, Grigorenko AP, Dailey C, Berezikov E, Buckley KM, Ptitsyn A, Reshetov D, Mukherjee K, Moroz TP, Bobkova Y, Yu F, Kapitonov VV, Jurka J, Bobkov YV, Swore JJ, Girardo DO, Fodor A, Gusev F, Sanford R, Bruders R, Kittler E, Mills CE, Rast JP, Derelle R, Solovyev VV, Kondrashov FA, Swalla BJ, Sweedler JV, Rogaev EI, Halanych KM, Kohn AB (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature 510:109–114PubMedCentralPubMedCrossRefGoogle Scholar
- Nakanishi N, Sogabe S, Degnan BM (2014) Evolutionary origin of gastrulation: insights from sponge development. BMC Biol 12:26PubMedCentralPubMedCrossRefGoogle Scholar
- Nosenko T, Schreiber F, Adamska M, Adamski M, Eitel M, Hammel J, Maldonado M, Müller WE, Nickel M, Schierwater B, Vacelet J, Wiens M, Wörheide G (2013) Deep metazoan phylogeny: when different genes tell different stories. Mol Phylogenet Evol 67:223–233PubMedCrossRefGoogle Scholar
- Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Quéinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Wörheide G, Manuel M (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:706–712PubMedCrossRefGoogle Scholar
- Redmond NE, Morrow CC, Thacker RW, Diaz MC, Boury-Esnault N, Cárdenas P, Hajdu E, Lôbo-Hajdu G, Picton BE, Pomponi SA, Kayal E, Collins AG (2013) Phylogeny and systematics of Demospongiae in light of new small-subunit ribosomal DNA (18S) sequences. Integ Comp Biol 53:388–415CrossRefGoogle Scholar
- Richards GS (2010) The origins of cell communication in the animal kingdom: notch signalling during embryogenesis and metamorphosis of the demosponge Amphimedon queenslandica. PhD Thesis The University of QueenslandGoogle 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:e15CrossRefGoogle Scholar
- Richards GS, Simionato E, Perrron M, Adamska M, Vervoort M, Degnan BM (2008) Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit. Curr Biol 18:1156–1161PubMedCrossRefGoogle Scholar
- Rivera AS, Ozturk N, Fahey B, Plachetzki DC, Degnan BM, Sancar A, Oakley TH (2012) Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin. J Exp Biol 215:1278–1286PubMedCentralPubMedCrossRefGoogle Scholar
- Robinson JM, Sperling EA, Bergum B, Adamski M, Nichols SA, Adamska M, Peterson KJ (2013) The identification of microRNAs in calcisponges: independent evolution of microRNAs in basal metazoans. J Exp Zool B Mol Dev Evol 320:84–93PubMedCrossRefGoogle Scholar
- Ryan JF, Pang K, Schnitzler CE, Nguyen AD, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, NISC Comparative Sequencing Program, Smith SA, Putnam NH, Haddock SH, Dunn CW, Wolfsberg TG, Mullikin JC, Martindale MQ, Baxevanis AD (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342:1242592PubMedCentralPubMedCrossRefGoogle Scholar
- Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, Degnan BM, Oakley TH, Kosik KS (2007) A post-synaptic scaffold at the origin of the animal kingdom. PLoS ONE 2:e506PubMedCentralPubMedCrossRefGoogle Scholar
- Saller U, Weissenfels N (1985) The development of Spongilla lacustris from the oocyte to the free larva (Porifera, Spongillidae). Zoomorph 105:252–277Google Scholar
- Schierwater B, Eitel M, Jakob W (2009) Concatenated analysis sheds light on early metazoan evolution and fuels a modern “urmetazoon” hypothesis. PLoS Biol 7:e20PubMedCrossRefGoogle Scholar
- Sebé-Pedrós A, Ariza-Cosano A, Weirauch MT, Leininger S, Yang A, Torruella G, Adamski M, Adamska M, Hughes TR, Gómez-Skarmeta JL, Ruiz-Trillo I (2013) Early evolution of the T-box transcription factor family. Proc Natl Acad Sci U S A 110:16050–16055PubMedCentralPubMedCrossRefGoogle Scholar
- Simpson TL (1984) The cell biology of sponges. Springer, New YorkCrossRefGoogle 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 26:2261–2274PubMedCrossRefGoogle Scholar
- Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010a) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726PubMedCentralPubMedCrossRefGoogle Scholar
- Srivastava M, Larroux C, Lu DR, Mohanty K, Chapman J, Degnan BM, Rokhsar DS (2010b) Early evolution of the LIM homeobox gene family. BMC Biol 8:e4CrossRefGoogle Scholar
- Steinmetz PRH, Kraus JEM, Larroux C, Hammel JU, Amon-Hassenzahl A, Houliston E, Wörheide G, Nickel M, Degnan BM, Technau U (2012) Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487:231–234PubMedCentralPubMedCrossRefGoogle Scholar
- Thacker RW, Freeman CJ (2012) Sponge-microbe symbioses: recent advances and new directions. Adv Mar Biol 62:57–111PubMedCrossRefGoogle Scholar
- Thacker RW, Hill AL, Hill MS, Redmond NE, Collins AG, Morrow CC, Spicer L, Carmack CA, Zappe ME, Pohlmann D, Hall C, Diaz MC, Bangalore PV (2013) Nearly complete 28S rRNA gene sequences confirm new hypotheses of sponge evolution. Integ Comp Biol 53:373–387CrossRefGoogle Scholar
- Tuzet O (1973) Éponges calcaires. In: Grassé P-P (ed) Traité de Zoologie Anatomie, Systématique, Biologie Spongiaires, vol 3. Masson et Cie, Paris, pp 27–132Google Scholar
- Worheide G, Dohrmann M, Erpenbeck D, Larroux C, Maldonado M, Voigt O, Borchiellini C, Lavrov DV (2012) Deep phylogeny and evolution of sponges (phylum Porifera). Adv Mar Biol 61:1–78PubMedCrossRefGoogle Scholar
- Zakrzewski A-C, Weigert A, Helm C, Adamski M, Adamska M, Bleidorn C, Raible F, Hausen H (2014) Early divergence, broad distribution and high diversity of animal chitin synthases. Genome Biol Evol 6:316–325PubMedCentralPubMedCrossRefGoogle Scholar