Porifera (Sponges):Recent Knowledge andNew PerspectivesEmmanuelle Renard, Institut Mediterraneen de Biodiversite et d’Ecologie marine et

continentale (IMBE), UMR CNRS IRD Avignon Universite, Aix-Marseille Universite, Marseille, France

Eve Gazave, Institut Mediterraneen de Biodiversite et d’Ecologie marine et continentale

(IMBE), UMR CNRS IRD Avignon Universite, Aix-Marseille Universite, Marseille, France

Laura Fierro-Constain, Institut Mediterraneen de Biodiversite et d’Ecologie marine et

continentale (IMBE), UMR CNRS IRD Avignon Universite, Aix-Marseille Universite, Marseille, France

Quentin Schenkelaars, Institut Mediterraneen de Biodiversite et d’Ecologie marine et

continentale (IMBE), UMR CNRS IRD Avignon Universite, Aix-Marseille Universite, Marseille, France

Alexander Ereskovsky, Institut Mediterraneen de Biodiversite et d’Ecologie marine et

continentale (IMBE), UMR CNRS IRD Avignon Universite, Aix-Marseille Universite, Marseille, France

Jean Vacelet, Institut Mediterraneen de Biodiversite et d’Ecologie marine et continentale

(IMBE), UMR CNRS IRD Avignon Universite, Aix-Marseille Universite, Marseille, France

Carole Borchiellini, Institut Mediterraneen de Biodiversite et d’Ecologie marine et

continentale (IMBE), UMR CNRS IRD Avignon Universite, Aix-Marseille Universite, Marseille, France

Based in part on the previous version of this eLS article ‘Porifera’ (2001)by Patricia R Bergquist.

Porifera, commonly named sponges, are true animals or

metazoan despite their anatomical and morphological

simplicity that had led to a long-time debate about their

nature (animal versus vegetal) and constitution (colonies

of unicellular organisms versus multicellular organisms).

Sponges are a successful group of mostly marine filter

feeder organisms that represent a major life form of sev-

eral ecosystems. Devoid of organs, the main character-

istics of their body plan are the presence of a network of

pores (at the origin of their name), choanocyte chambers

and canals devoted to water filtration and spicules (when

present) allowing tissue physical support. Currently con-

sidered as the sister group to all the other animals, these

organisms have a key phylogenetic position. Recent stu-

dies have shown that they possess an unexpected

molecular complexity raising exciting questions about

early animal evolution.

Introduction

Sponges or Porifera were already described by Aristotle,and for almost 4000 years they have been used for humanbathing and cleaning purposes. As adults, sponges aresedentary filter feeder animals that have considerableecological, commercial andbiopharmaceutical value. Theycan be found in all marine habitats and some of themcolonised freshwater. Filtration is performed by highlyspecialised flagellated cells: the choanocytes, which enableto pump the water unidirectionally through the body. Thewater flow is canalised in an aquiferous system composedof pores (ostia), canals and choanocyte chambers. Theaquiferous system not only ensures nutritive functionsbut is also involved in other vital physiological functions,such as reproduction and excretion. Sponges are devoid ofdigestive cavity and gonads, and despite the lack of neu-rons and muscles, they have the capacity to react toenvironmental changes. Because of this anatomical sim-plicity, they have been set apart fromothermetazoans for along time. They have also been considered as primitiveanimals with a cellular instead of tissular organisationlevel unlike other animals. Recent phylogenetic, cellular,

Introductory article

Article Contents

. Introduction

. Diversity and Phylogeny

. Ecology

. General Organisation of the Body and the Aquiferous

System

. Cell Plasticity, Stem Cells and Cell Renewal

. Reproduction and Development

. New Insights and Perspectives on Early Animal

Evolution

Online posting date: 9th December 2013

eLS subject area: Evolution & Diversity of Life

How to cite:Renard, Emmanuelle; Gazave, Eve; Fierro-Constain, Laura;

Schenkelaars, Quentin; Ereskovsky, Alexander; Vacelet, Jean; and

Borchiellini, Carole (December 2013) Porifera (Sponges): RecentKnowledge and New Perspectives. In: eLS. John Wiley & Sons, Ltd:

Chichester.

DOI: 10.1002/9780470015902.a0001582.pub2

eLS & 2013, John Wiley & Sons, Ltd. www.els.net 1

molecular and developmental data tend to propose are-evaluation of these classical interpretations.

Diversity and Phylogeny

Sponges are knownandusedby humans since the antiquity(Pronzato and Manconi, 2008). According to the fossilrecord, Porifera were already present and diversified in thelower Cambrian (Rigby and Hou, 1995). In present time,sponges have colonised allmarine habitats and ecosystems,and some species even managed to colonise freshwater.Their diversity in terms of species number is quite difficultto estimate precisely, notably not only because of thescarcity and the variability of morphological charactersthey harbour but also due to the difficulties to access theirdiverse habitats until recently. As a result, recognition anddescription of new species is a highly specialist task. In thiscontext, molecular data, in addition to the more classicmorphological, embryological, and cytological data, havebeen shown to be an invaluable tool for species delimita-tion (Boury-Esnault et al., 2013; Gazave et al., 2013). Atpresent, the number of formally described sponge species iscomprised between 8000 and 9000, with an estimated 4000species awaiting discovery and/or formal description(Word Porifera Database, http://www.marinespecies.org/porifera/).In recent years, several contradicting hypotheses about

relationships at the basis of the metazoan tree and soamong nonbilaterian animals (Porifera, Cnidaria, Cteno-phora and Placozoa) and among poriferan groups have

been published (Dunn et al., 2008; Erwin et al., 2011;Nosenko et al., 2013; Philippe et al., 2009, 2011; Pick et al.,2010; Schierwater et al., 2009; Sperling et al., 2009; Wor-heide et al., 2012). Although the majority of them supportthe hypothesis of Porifera as a monophyletic group, sistergroup of all other animals (commonly named Eumetazoa),the debate is still open and the resolution of the base of themetazoan tree remains among the most important openquestions in zoology. Sponges are nowdivided into 4 clades(classes according to the Linnaean-ranked classification)instead of the 3 recognised before 2009 (Gazave et al., 2012;Figure 1). These 4 taxa – Hexactinellida, Demospongiae,Calcarea and Homoscleromorpha – are distinguished bydifferent tissular, skeletal and developmental character-istics, which will not be detailed here (main features aresummarised in Table 1).

TheCalcarea are exclusivelymarine sponges and includeapproximately 675 marine species (Word Porifera Data-base). They have calcareous (calcite) spicular skeleton.Spicules, littlemineral pieces of variable size and shape, aresecreted in the extracellular space contrary to the intra-cellularly formed siliceous spicules in other sponge taxa.The skeleton is composed of free spicules, but some specieshave a massive basal skeleton. Nevertheless, hypercalci-fied, solid basal calcareous skeletons also occur in somedemosponges, but the crystalline structure is more oftenaragonitic rather than calcitic as in Calcarea.The Hexactinellida (or glass sponges) are also exclu-

sively marine sponges with siliceous skeleton. They arelargely restricted to the deep sea and cold waters. For thisreason, the diversity of this group (623 extant speciesaccording to the World Porifera Database) is probably

Homoscleromorpha

Metazoa

Calcispongiae

Demospongiae

Hexactinellida (b)

Metazoa

(a)

Eumetazoa

Figure 1 Two main hypotheses currently proposed concerning nonbilaterian phylogenetic relationships: (a) paraphyly of sponges, (b) monophyly of

sponges. Modified from Ereskovsky et al. (2013). & Springer.

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Porifera (Sponges): Recent Knowledge and New Perspectives

underestimated. These sponges differ from the three otherclasses in many aspects of their biology (Leys et al., 2007,2011), mainly by a syncitial organisation instead of acellular one, and by 6-rayed spicules.The Homoscleromorpha form the smallest group of

marine sponges (5100 described species). They can bedistinguished from others mainly by the presence of abasement membrane (Boute et al., 1996; Ereskovsky et al.,2009; Gazave et al., 2012) resulting in epithelial level orga-nisation and tissue morphogenesis more similar to otheranimals (Eumetazoa). The skeleton can be entirely absent.When present, the spicules are peculiar tetractines (with 4axes) and their derivatives secreted not only within scler-ocytes as in demosponges but also within epithelial cells.The Demosponges represent the most diversified taxa

not only in terms of species (85% of all sponge species)but also regarding habitats conquered with noteworthyadaptations to freshwater (temporary ecosystem in somecases) and nutrient-depleted deep sea or caves (loss ofthe aquiferous system and acquisition of macrophagy). Themineral skeleton of siliceous spicules can be partially orentirely replaced by an organic skeleton consisting ofabundant collagen fibres (spongin), as in bath sponges. Theskeleton can be totally absent, with a mesohyl containingonly abundant collagen fibrils. See also: Cambrian Explo-sion; Cnidaria (Coelenterates); Ctenophora (Sea Walnutsand Comb Jellies); Eukaryotes and Multicells: Origin;Evolution of the Metazoan Extracellular Matrix; Placozoa

Ecology

Sponges have a worldwide distribution and can be foundfrom tropics to polar regions. In some habitats, they canrepresent the dominant macrobenthic organisms, con-tributing up to 80% of the biomass. Their activities impacton marine ecological processes at macro- and microlevelsby different ways:

1. Interactions with substrate: Boring sponges can exca-vate calcareous substrates, such as mollusk shells, cor-alline rhodophyta, coral reefs, etc. Some sponges arethus actors of bioerosion (Carballo et al., 2012).

2. Trophic ecology: Most sponges feed on microorganismsby a very effective filtration system. Exercising littleselection (except size limit imposed by ostia diameter),they pump a large volume of water, cycling a volumeequivalent to their body volume every 7 s (Bergquist,1978; Reiswig, 1971). Their presence thus impacts themicrobial abundance and diversity. Moreover, manyspecies of unicellular eukaryotes, archaea and eubacteriaare hosted symbiotically by sponges (for illustration:pinkish colour visible on Figure 3e corresponds to thepresence of cyanobacteria), which can be considered as areservoir of microbial diversity. Some of them hostingsymbiotic cyanobacteria can become net primary pro-ducers and contribute to oxygen production (Websterand Taylor, 2012). A few sponge species that live in deep

Table 1 Summary of the main characteristics of each clade of Porifera

Character Hexactinellida Demospongiae Calcarea Homoscleromorpha

Number of actual

accepted species

601 6835 676 93

Distribution All marine, mostly

deep waters

Marine, brackish and

freshwaters, all

depths

All marine All marine

Nature of spicules Siliceous Siliceous when

present

Calcium carbonate Siliceous when

present

Types of spicules Megascleres/

microscleres with

usually 6 or 3 axes

Megascleres/

microscleres with 1–4

axes

Megascleres/

microscleres with 1–4

axes

No megascleres/

microscleres

distinction

Reproduction Viviparous Oviparous or

viviparous more

common

parenchymula larvae

Viviparous coelo- or

amphiblastula larvae

Viviparous

cinctoblastula larvae

Cell sheets The greater part of

soft tissue consists of

a single,

multinucleate

syncytium

Cellular organisation Cellular organisation Cellular organisation,

flagellated

pinacocytes, presence

of a basement

membrane with type-

IV collagen

Types of aquiferous

system

Syconoid, sylleibid or

leuconoid pattern

Leuconoid Asconoid, syconoid

or leuconoid

Sylleibid or leuconoid

Types of symmetry Radial Asymmetric or radial Asymmetric or radial Asymmetric

Source: According to Brusca and Brusca (2003); Word Porifera Database (http://www.marinespecies.org/porifera/); and Gazave et al., (2012).# Elsevier.

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Porifera (Sponges): Recent Knowledge and New Perspectives

sea, a food-poor environment, have become carnivoresand prey mainly on small crustaceans (Vacelet andBoury-Esnault, 1995; Vacelet and Duport, 2004).

3. Interactions with other organisms: Sponges also oftenhost small metazoans or their larvae (arthropods,nematodes, annelids, echinoderms and cnidaria) forwhich they offer shelters.

The defences of sponges against pathogens, competitorsand predators (such as echinoderms, mollusks, fishes, etc.)mainly consist in the presence of spicules (mechanicdefence) and production of toxic secondary metabo-lites (chemical defence). Sponge secondary metabolitesobviously present a defensive role against predation,infections and fouling. Indeed, they exhibit antibacterial,antifungal, antiplasmodial, antihelminthic, antiamoebitic,antileishmanial as well as anti-inflammatory and anticanceractivities. Among the chemical compounds isolated so farfrom sponges (more than 5000), 800 present antibioticproperties, thus opening up future medical applications(Darah et al., 2011; Torres et al., 2002; Touati et al., 2007).Moreover, these chemicals play an important role in

competition for space, indeed some of them are lethalweapons to fight against other sessile and encrusting inver-tebrates (such as other sponge species, cnidarians, bryozo-ans, ascidians, etc.).

General Organisation of the Body andthe Aquiferous System

The cell layer responsible for the main delimitation of thebody is called pinacoderm, which is composed of flattenedcells named pinacocytes (baso-, exo- and endopinacocytesaccording to their position). Internally, the pinacodermlines (inhalant) canals that carry the water to the filteringcells – the choanocytes (often organised in chambers,see Figure 2). Choanocytes (forming a cell layer namedchoanoderm) are highly specialised collar cells. Water flowis ensured by the beating of choanocyte flagella while themicrovilli of the collar trap unicellular organisms that willbe phagocytised. The filtered water leaves the spongeby (exhalant) canals lined by pinacoderm. Choanocytes

Ascon Sycon Leucon

(a)

(b)

Flagellum

Microvillosities

Choanocyte chamber

Choanocyte

Mesohyl

Exhalant pore(Osculum)

Exhalant canal

Inhalant pore(Ostium)

Spicule

Exopinacoderm

Endopinacoderm

Inhalant canal

Choanoderm

OsculumOsculumOsculum

Figure 2 (a) General organisation of sponges. (b) The three main levels of complexity of the aquiferous system. Modified with permission from Philippe

et al. (2009). & Elsevier.

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Porifera (Sponges): Recent Knowledge and New Perspectives

account for 80% of organic carbon uptake; nevertheless,surface- and canal-lining pinacocytes can phagocytiseparticles directly. The canals and choanocyte chambersnetwork form together the aquiferous system. The aqui-ferous system can be more or less complex, leading to apeculiar terminology. Figure 2 provides a schema of thegeneral organisation of a sponge (Figure 2a) and the maintypes of aquiferous systems (asconoid, syconoid andleuconoid used for species identification and classification,Figure 2b). The water flow can be regulated, in responseto environmental changes, by dilatation or restrictionof inhalant pores (ostia), canals and exhalant pores(oscula) diameter. In addition, active pulsatile contrac-tions observed by time-laps imaging are supposed to par-ticipate to the efficiency of pumping (Nickel et al., 2011).The mechanisms of signal transduction mediating per-ception and regulation of pumping are nevertheless stillmisunderstood, even if neuromediators are supposed to beinvolved (for review seeRenard et al., 2009).One exceptionis worth noting: the aquiferous system and its choanocytes,long considered as characteristic of sponges, are absent(maybe lost) in most carnivorous sponges.Between pinacoderm and choanoderm, a fibril-rich,

looser and less organised layer is found: the mesohyl, whichcontains various types of cells (thenumberofwhichdependson the group considered), notably totipotent cells calledarchaeocytes (see Cell Plasticity, Stem Cells and CellRenewal), cells involved in mineral and/or organic skeletonsynthesis (such as sclerocytes, spongocytes and lophocytes),cells supposed to be implicated in chemical synthesisand exocytosis (granular and spherulous cells) as well asgametes, skeleton elements and symbiotic microorganisms.Mineral skeleton, when present, is either siliceous or

calcareous, usually in the form of spicules that have abewildering range of shapes, sizes and patterns of organi-sation (at the basis of species identification and classifica-tion). The larger elements (megascleres) maintain theoverall form of the sponge, whereas tiny spicules (micro-scleres) line the surfaces or are dispersed without order.This part can be concluded saying that as sponges are

devoid of organs, their individual cells or cell layers ensurevital functions. Feeding involves choanoderm and pina-coderm; most of other activities involve mesohyl cells, forexample, the synthesis of organic and mineral skeleton.See also: Evolution of the Metazoan Extracellular Matrix

Cell Plasticity, Stem Cells and CellRenewal

Regarding the lownumber of cell types in sponges (rangingfrom 4 to 12 (Ereskovsky, 2010)), some authors considerthat one cell type may have several functions even if con-crete proof sometimes lacks: for example, choanocytes areobviously involved in nutrition and reproduction (see‘Reproduction and Development’) but may also play sen-sorial roles (Jacobs et al., 2007;Gazave et al., 2008; Renard

et al., 2009) and pinacoderm is involved in body lining andnutrition but also ensures contractility (Nickel et al., 2011).In addition to cell plurifunctionality, the functional plas-ticity of sponges also relies on a high capacity of celltransdifferentiation.Indeed, as in other metazoans, cell renewal involves

pluripotent cells. In text books, archaeocytes are generallyconsidered as demosponge stem cells based on morpholo-gical observations, and this was recently supported bymolecular data (Funayama, 2013). But in addition, it wasshown that choanocytes also express stem cell gene mar-kers, which suggests that these specialised cells retainpluripotency. This is consistent with the fact that they areoften involved in gamete formation by transdifferentiation(Funayama, 2013).This cellular plasticity may explain the sponge’s great

capacity to regenerate or reaggregate, which offers veryinteresting technical possibilities to study cell differentia-tion processes. Sponges possess remarkable reconstitutiveand regenerative abilities ranging from not only the com-mon wounds cicatrisation to body part regeneration butalso to functional body regeneration from dissociatedcells. Indeed, sponge cells can be dissociated into cell sus-pensions (chemically or mechanically) and then, underappropriate ionic conditions, cells can reaggregate andreconstitute either organised structures named primorphsor, in some cases, entirely functional individuals. If mix-tures of cells of different species are realised, they recon-stitute separately, proving that cell recognition complexesalso exist in these organisms (also shown by graft experi-ments; for review see Simpson, 1984). See also: AdhesiveSpecificity and the Evolution of Multicellularity

Reproduction and Development

Reproduction and development was more largely studiedin Demospongiae and Calcarea, but nevertheless theyshowa great diversity of strategies. Indeed, both sexual andasexual reproductions are commonly used by sponges,with a large diversity of reproductive processes.Like in other metazoans, sexual reproduction involves

gametogenesis processes leading to the formation of ani-sogamic gametes with typical mobile spermatozoids andoocytes containing vitellus. Sponges can be either gono-choristic or hermaphroditic (in this case both protandryand protogyny have been described), hermaphroditismbeing considered as more frequent. Gametes are notproduced in gonads but result either from archaeocytesdifferentiation or choanocytes transdifferentiation. Ferti-lisation can occur either internally in the mesohyl orexternally in the water column. In the first case, sperma-tozoids enter the oocyte coating by the aquiferous system.An impressive mechanism has been described in Calcarea:spermatozoids are captured by choanocytes that dediffer-entiate to become carrier cells transporting them tooocytes. In all cases, the obtained zygote enters in devel-opmental processes leading to a mobile, ciliated larval

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Porifera (Sponges): Recent Knowledge and New Perspectives

stage characteristic of each sponge groups. After a shortfree life (2 h to 4 days), the larva settles on a selected sub-strate and metamorphoses to give rise to a sessile filtratingadult (Ereskovsky, 2010). For some species, the embryos ofdifferent stages develop in brood chambers until they reacha certain size and then disperse.Asexual reproduction can occur by external (budding)

or internal (gemmules) tissular reorganisation processes aswell as fragmentation. Formation of buds, which subse-quently detach, is a common asexual process in marinesponges, whereas the formation of gemmules, a state ofquiescence consisting in archaeocyte aggregates encapsu-lated within a spongin coat, characterises most offreshwater sponges. For the latter case, on hatching, alladult cells derive from the archaeocytes, an excellentillustration of their totipotency. Gemmules formationsometimes also occurs in some shallow-water marine

sponges (Simpson, 1984). They show impressive resistancefeatures allowing the colonisation of temporary waters andhigh possibilities of adaptation to fluctuating environments(Schill et al., 2006).Thereby, according to the few well-described sponge

life cycles, it seems that sponges often use both asexualand sexual reproduction during their lifespan. See also:Reproduction and Life Cycles in Invertebrates

New Insights and Perspectives onEarly Animal Evolution

Because of their morphoanatomical simplicity, Poriferahave not been considered as true animals for a long time,sometimes regarded as colonial organisms and a step

Dem

osp

ongi

ae

(a)

(d)

(g) (h) (i)

(b)

(e)

(c)

(f)

Cal

care

aH

exac

tinel

lida

Hom

oscl

erom

orp

ha

Figure 3 Pictures illustrating the diversity of forms, colours and sizes in Porifera, with a few chosen examples from the four clades. (a) Aplysina cavernicola,

(b) Ephydatia fluviatilis, (c) Xestospongia muta, (d) Sycon ciliatum, (e) Clathrina contorta, (f) Leucosolenia complicata, (g) Rosella nuda, (h) Oopsacas minuta and

(i) Oscarella species (�Oscarella tuberculata and ��Oscarella lobularis). & Elsevier.

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Porifera (Sponges): Recent Knowledge and New Perspectives

between uni- and multicellular organisms. Molecular,phylogenetic and embryological data accumulated sincethe end of the twentieth century have closed this debateshowing that they are bona fide Metazoa. The moremolecular (transcriptomic and genomic) data are acquired,the more the complexity of sponge genome content raisesexciting questions. Indeed,most of key transcription factorfamilies and main signalling pathways required for eume-tazoan development and body patterning are presentin sponges, suggesting that the last common ancestor ofMetazoa (named Urmetazoa) already owned a complexmolecular toolkit (Ereskovsky et al., 2013). Thenext step inprogress to be reached is determining the roles of all thesegenes in sponges and comparing them to eumetazoan inorder to propose evolutionary scenarios of gene functionevolution and try to correlate them with body plan evolu-tion (Figure 3 proposes scenarios of character acquisitions).So far, only two whole sponge genomes are at presentpublicly available and few others are in progress. Therecent rising interest for Porifera is expected to allow abetter understanding of early animal evolution by thegrowing amount of cellular, molecular and functionaldata:WasUrmetazoa a sponge-like simple organism or, incontrast, a more complex animal; the simplicity of spongesthen being the result of a secondary simplification, asobserved several times in animal evolution (e.g. cirripeda

and tunicates)? (Figure 4; Nielsen, 2008; Philippe et al.,2009; Worheide et al., 2012). See also: Animals and TheirUnicellular Ancestors; Nuclear Receptor Genes: Evolu-tion; Origin of Bilaterian Hox Patterning System

References

Bergquist PR (1978) Sponges. Hutchinson & Co., London, 268 p.

Boury-Esnault N, Lavrov DV, Ruiz CA and Perez T (2013) The

integrative taxonomic approach applied to porifera: A case

study of the Homoscleromorpha. Integrative and Comparative

Biology 24. 10.1093/icb/ict042.

Boute N, Exposito JY, Boury-Esnault N et al. (1996) Type IV

collagen in sponges, the missing link in basement membrane

ubiquity. Biology of the Cell 88: 37–44.

Brusca RC and Brusca GJ (2003) Invertebrates, 2nd edn.

Sunderland, MA: Sinaeur.

Carballo JL, Bautista E, Nava H, Cruz-Barraza JA and Chavez

JA (2012) Boring sponges, an increasing threat for coral reefs

affected by bleaching events. Ecology and Evolution. 10.1002/

ece3.452

Darah I,LimCL,Nurul-Aili Z,Nor-AfifahSandShaida-Fariza S

(2011) Effects of methanolic extract of a soft sponge,Haliclona

sp. on bacterial cells: structural degeneration study. Interna-

tional Journal of Comprehensive Pharmacy 2: 1–6.

Hexactinellida Demospongiae Calcarea Homoscleromorpha Eumetazoa

3

3

3

3

1

2

3

4

4

4

4

5

Figure 4 Possible scenarios of character evolution during animal history, according to the (currently most accepted) hypothesis of monophyly of sponges.

Lines represent acquisition of characters, crosses represent losses of characters, red or green colours represent alternative scenarios for a same character.

Characters are coded by the following numbers: 1: multicellularity; 2: aquiferous system; 3: basement membrane and true epithelia; 4: siliceous spicules;

5: neurones, muscle cells and digestive system. & Elsevier.

eLS & 2013, John Wiley & Sons, Ltd. www.els.net 7

Porifera (Sponges): Recent Knowledge and New Perspectives

Dunn CW, Hejnol A, Matus DQ et al. (2008) Broad phyloge-

nomic sampling improves resolution of the animal tree of life.

Nature 452: 745–749.

Ereskovsky AV (2010) The comparative embryology of sponges.

Springer. Dordrecht.

Ereskovsky AV, Borchiellini C, Gazave E et al. (2009). The

Homoscleromorph sponge Oscarella lobularis, a promising

sponge model in evolutionary and developmental biology.

Bioessays 31: 89–97.

Ereskovsky AV, Renard E and Borchiellini C (2013) Cellular

and molecular processes leading to embryo formation in

sponges: evidences for high conservation of processes

throughout animal evolution. Developmental Genes and Evo-

lution 223(1–2): 5–22.

Erwin DH, LaflammeM, Tweedt SM et al. (2011) The Cambrian

conundrum: early divergence and later ecological success in the

early history of animals. Science 334: 1091–1097.

Funayama N (2013) The stem cell system in demosponges: sug-

gested involvement of two types of cells: archeocytes (active

stem cells) and choanocytes (food-entrapping flagellated cells).

Developmental Genes and Evolution 223(1–2): 23–38.

Gazave E, Lapebie P, Renard E et al. (2008) NKhomeobox genes

with choanocyte-specific expression in homoscleromorph

sponges. Developmental Genes and Evolution 218: 479–489.

Gazave E, Lapebie P, Ereskovsky AV et al. (2012) No longer

Demospongiae: Homoscleromorpha formal nomination as a

fourth class of Porifera. Hydrobiologia 687(1): 3–10.

Gazave E, Lavrov DV, Cabrol J et al. (2013) Systematics and

molecular phylogeny of the family oscarellidae (homo-

scleromorpha) with description of two new Oscarella species.

PLoS One 8(5): e63976.

Jacobs DK, Nakanishi N, Yuan D et al. (2007) Evolution of

sensory structures in basal metazoa. Integrative and Compara-

tive Biology 47: 712–723.

Leys SP,MackieGOandReiswigHM(2007) The biology of glass

sponges. Advances in Marine Biology 52: 1–145.

Leys SP, YahelG,ReidenbachMA et al. (2011) The sponge pump:

The role of current induced flow in the design of the sponge body

plan. PLoS One 6: e27787. 10.1371/journal.pone.0027787

NickelM,ScheerC,Hammel JU,Herzen J andBeckmannF (2011)

The contractile sponge epithelium sensu lato-body contraction

of the demosponge Tethya wilhelma is mediated by the pinaco-

derm. Journal of Experimental Biology 15; 214(10): 1692–1698.

Nielsen C (2008) Six major steps in animal evolution: are we

derived sponge larvae. Evolution and Development 10: 241–257.

NosenkoT, Schreiber F,AdamskaM et al. (2013)Deepmetazoan

phylogeny: when different genes tell different stories.Molecular

Phylogenetics and Evolution 67(1): 223–233.

PhilippeH,DerelleR,LopezP et al. (2009)Phylogenomics revives

traditional views on deep animal relationships.Current Biology

19: 706–712.

Philippe H, Brinkmann H, Lavrov DV et al. (2011) Resolving

difficult phylogenetic questions: why more sequences are not

enough. PLoS Biology 9(3): e1000602. 10.1371/journal.pbio.

1000602.

Pick KS, Philippe H, Schreiber F et al. (2010). Improved phylo-

genomic taxon sampling noticeably affects nonbilaterian rela-

tionships. Molecular Biology and Evolution 27: 1983–1987.

Pronzato R and Manconi R (2008) Mediterranean commercial

sponges: over 5000 years of natural history and cultural heri-

tage. Marine Ecology 29: 146–166.

Reiswig HM (1971) In situ pumping activities of tropical

Demospongiae.Marine Biology 9: 38–50.

Renard E, Vacelet J, Gazave E et al. (2009) Origin of the neuro-

sensory system: new and expected insights from sponges. Inte-

grative Zoology 4: 294–308.

Rigby JK and Hou XG (1995) Lower Cambrian demosponges

and hexactinellid sponges from Yunnan. Chinese Journal of

Paleontology 69: 1009–1019.

Schierwater B, Eitel M, Jakob W et al. (2009) Concatenated ana-

lysis sheds light on early metazoan evolution and fuels a modern

‘‘urmetazoan’’ hypothesis. PLoS Biology 7(1): e1000020.

Schill RO, PfannkuchenM, Fritz G, Kohler HR and Brummer F

(2006) Quiescent Gemmules of the Freshwater Sponge, Spon-

gilla lacustris (Linnaeus, 1759), Contain Remarkably High

Levels of Hsp70 Stress Protein and Hsp70 Stress Gene mRNA.

Journal of Experimental Zoology part A: Comparative Experi-

mental Biology 305A, 5. 10.1002/jez.a.281

Simpson TL (1984) The Cell Biology of Sponges. Springer Verlag.

New York.

Sperling EA, Peterson KJ and Pisani D (2009) Phylogenetic-sig-

nal dissection of nuclear housekeeping genes supports the

paraphyly of sponges and the monophyly of Eumetazoa.

Molecular Biology and Evolution 26: 2261–2274.

Torres YR, Berlinck RGS, Nascimento GGF et al. (2002) Anti-

bacterial activity against resistant bacteria and cytotoxicity of

four alkaloid toxins isolated from marine sponge Arenosclera

brasiliensis. Toxicon 40: 885–891.

Vacelet J and Boury-Esnault N (1995) Carnivorous sponges.

Nature (London) 373: 333–335.

Vacelet J and Duport (2004) Prey capture and digestion in the

carnivorous sponge Asbestopluma hypogea (Porifera: Demos-

pongiae). Zoomorphology 123: 179–190.

Touati I, ChaiebK,BakhroufA andGaddourK (2007) Screening

of antimicrobial activity of marine sponge extracts collected

fromTunisian coast. Journal ofMedicalMycology 17: 183–187.

Webster NS and Taylor MW (2012) Marine sponges and their

microbial symbionts: love and other relationships. Environ-

mental Microbiology 14(2): 335–346. 10.1111/j.1462-2920.

2011.02460.x

Worheide G, Dohrmann M, Erpenbeck D et al. (2012) Deep

phylogeny and evolution of sponges (phylum Porifera).

Advances in Marine Biology 61: 1–78.

Further Reading

Funayama N (2010) The stem cell system in demosponges:

Insights into the origin of somatic stem cells. Development,

Growth & Differentiation 52(1): 1–14.

Leys SP (2004) Gastrulation in Sponges. In: Stern CD (ed.) Gas-

trulation: From cell to embryo, pp 23–32. New York: Cold

Spring Harbor Lab Press.

Manuel M (2009) Early evolution of symmetry and polarity in

metazoan body plans. Comptes Rendus Biologies 332(2–3):

184–209.

eLS & 2013, John Wiley & Sons, Ltd. www.els.net8

Porifera (Sponges): Recent Knowledge and New Perspectives