The Journal of Experimental Biology

The Journal of Experimental Biology

588

reversibly. These results suggest that the AP relies on influx of

calcium and repolarization of the membrane by potassium.

(3) The action potential is temperature sensitive. Rhabdocalyptus

dawsoni studied in tanks at the Bamfield Marine Sciences Centre,

B.C., had a Q

10

of ~3; the sponges did not pump at temperatures

below 7°C, and would not arrest pumping at temperatures above

12.5°C. Presumably, other glass sponges have a slightly wider

temperature tolerance because they inhabit colder waters in Hecate

Strait, B.C. (5–7°C) and in Antarctica, but a limited range of

function is still expected based on the constraints of calcium channel

operation (Leys and Meech, 2006).

These characteristics do not seem to reflect a prior history of

nerves that have been lost and replaced by syncytia. Although

syncytia are common in animals, their method of formation by

fusion during embryogenesis is not seen in other sponges or other

animals. Epithelial conduction in the comb plates of ctenophores has

similar velocities and is also calcium based (Moss and Tamm,

1987), but travels through cells connected by gap junctions. The

temperature dependence of the action potential in glass sponges is

thought to reflect an adaptation to deep, cold water. Recently, we

have wondered whether syncytia and electrical conduction may have

arisen as a low-cost system to prevent damage to tissues by

clogging. Glass sponges can contract but very slowly (Nickel, 2010),

and contraction may not be effective to prevent damage by a sudden

resuspension event. Our recent work (Leys et al., 2011) suggests that

the high cost of pumping may have led, over time, to reducing the

resistance through the sponge by evolving very large canals. Could

the cost of filtering in the deep sea have triggered the evolution of

syncytia concurrent with electrical signalling as a way to prevent

intake of materials that might damage the filter? Ongoing work by

A. Kahn (Kahn and Leys, 2013) on the energetics of filtration

promises new data on this question.

Common elements in different coordination systems

The sum of knowledge of sponge coordination systems shows that

sponges are largely epithelial animals, with sensory cells that are

epithelial, effectors that are contractile epithelial cells as well as

flagellated collar bodies lining the feeding chambers of glass

sponges; signalling pathways also seem to use the epithelia. There

is evidence for slow signalling in cellular sponges, probably using

metabotropic receptors and calcium waves, which are slow, but

effective at closing the intake system to prevent damage to feeding

chambers and sufficiently fast to eject inedible material that may

have entered and clogged chambers. In glass sponges, electrical

signalling is by action potentials which travel via syncytia and also

prevent damage to feeding chambers.

The sort of signalling seen in sponges is simple in comparison to

a nervous system, but the main need for signalling seems to be

protection of choanocytes and tissues from clogging and damage.

The sponge sensory system also provides a highly tuned control of

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The Journal of Experimental Biology (2015) doi:10.1242/jeb.110817

Conduction velocity (m s

–1

)

0.0001 0.001 0.01

0.1

10

100

1000

Ephydatia muelleri

Ephydatia fluviatilis

Rhabdocalyptus dawsoni

Nitella

Zea mays

Mimosa pudica

Ctenophore – Pleurobrachia

Ctenophore – Beroe

Ctenophore – Euplokamis 

Hydrozoan – epithelial

Hydrozoan – nervous

Loligo peleai

Mammalian nerves

Nimodipine

1 mmol l

–1

 TEA

25% Na

+

A

D

B

E

C

1

i

ii

iii

vi

R

R

T

50 s

500 µV

T

S

Fig. 4. Electrical conduction in glass sponges. (A) Conduction velocities in plants and animals. (B) Microtubules (green) and nuclei (blue) in giant syncytia

of the glass sponge Rhabdocalyptus dawsoni. (C) Adherent aggregates fusing with the syncytial tissue of R. dawsoni, a preparation that allows extracellular

recording from the sponge. (D) Diagram of the recording setup and records of action potentials in R. dawsoni (from Leys et al., 1999). S, stimulating electrode;

R, recording electrode; T, thermistor flow probe. Top traces, electrical records; bottom traces, thermistor flow records: (i) a single stimulus causes and AP and

arrest of flow; (ii,iii) repeated stimuli cause further APs even though the flow is still arrested; (iv) after pumping resumes a second stimulus causes a second AP

and arrests the flow again. (E) Effect of sodium, calcium and potassium on the action potential in R. dawsoni (after Leys et al., 1999). Top, 75% reduction of

sodium (replacement with choline chloride); middle, the calcium blocker nimodipine (24 μmol l

−1

) delays and blocks the AP, reversibly; bottom, the potassium

channel blocker TEA reduces, delays and then blocks the AP, also reversibly. Scale bars: 20 μm (B); 1 mm (C).

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The Journal of Experimental Biology

canal diameter to vary the amount of water processed, and this

suggests that there may be an energetic benefit to reduce filtration

if food is limited, for example during winter months. Larvae have

other sensory needs, which are attuned to helping them find the best

settlement sites, but even these are morphologically simple

compared with those of Cnidaria or Ctenophora. If one compares

just the sensory systems of sponges and ctenophores, it hardly seems

likely that sponges have lost nerves. Sensory organs in ctenophores

are sophisticated – both the balancer organ of the cydippid larva and

of the adult in Pleurobrachia (Tamm and Tamm, 2002) and the

photosensory molecules, including opsins of Mnemiopsis (Schnitzler

et al., 2012) reflect a complexity not seen in any sponge. Ctenophore

nerves use glutamate in signalling, while GABA appears in muscle

(Ryan et al., 2013; Moroz et al., 2014). Serotonin is apparently

absent, but ctenophores have a broad range of neuropeptides and

clearly identifiable nerves with synapses; they also have gap

junctions with a large number of innexin molecules used in

epithelial conduction (Moroz et al., 2014). These innovations both

enhance the agility of ctenophores and their ability to respond to and

capture prey. In short, the two systems are not easily compared.

The fossil record does not give any insight into early ctenophore

body plans – except for the idea that frond-like animals of the

Ediacaran may have had ctenophoran affinities (Dzik, 2002) – but

if ctenophores were predatory as extant species are, then what would

they have eaten? The environment in which the first multicellular

animals evolved was presumably oxygenated at the surface, as a

result of photosynthesis and turbulence, but the only food would

have been picoplankton – flagellates, bacteria and viruses (Lenton

et al., 2014). It is difficult to think of an animal that could have

existed prior to sponges and which would also have fed on bacteria

and or unicellular flagellates, but which did not have a sponge-like

body plan. If efficient filtering without damaging the filter was

important to early animals, then mechanisms to protect the filter

would have arisen and these would probably have been the first type

of signalling system to use elements that are now recognized from

nervous systems. The next step would have involved innovation of

more agile movement, including muscle and signalling systems

(possibly epithelial); these body plans may have co-opted the

elements found in sponges but would have required more

sophisticated gene regulatory networks (Peter and Davidson, 2011)

to build. A study of these networks in both sponges and ctenophores

might shed some light on this transition.

Acknowledgements

I thank members of my research group, in particular N. Farrar, A. Kahn and J.

Mah, and my colleague J. Paps (Oxford University) for stimulating discussions that

helped formulate the ideas presented in this paper. This work was presented at the

‘Evolution of the First Nervous Systems II’ meeting, which was supported by the

National Science Foundation (NSF).

Competing interests

The authors declare no competing or financial interests. 

Funding

Funding for the research described here that was carried out by the author’s group

came from a Natural Science and Engineering Research Council, Canada,

Discovery Grant to the author.

References

Adams, E. D. M. (2010).  Physiology and Morphology of Epithelia in the Freshwater

Demosponge, Spongilla lacustris. MSc thesis, University of Alberta, Edmonton, AB,

Canada.

Adams, E. D. M., Goss, G. G. and Leys, S. P. (2010). Freshwater sponges have

functional, sealing epithelia with high transepithelial resistance and negative

transepithelial potential. PLoS ONE 5, e15040. 

Adamska, M., Larroux, C., Adamski, M., Green, K., Lovas, E., Koop, D., Richards,

G. S., Zwafink, C. and Degnan, B. M. (2010). Structure and expression of

conserved Wnt pathway components in the demosponge Amphimedon

queenslandica. Evol. Dev. 12, 494-518. 

Alié, A. and Manuel, M. (2010). The backbone of the post-synaptic density originated in

a unicellular ancestor of choanoflagellates and metazoans. BMC Evol. Biol. 10, 34. 

Anctil, M. (1987). Bioactivity of FMRFamide and related peptides on a contractile

system of the coelenterate Renilla köllikeri. J. Comp. Physiol. B 157, 31-38. 

Antcliffe, J. B., Callow, R. H. T. and Brasier, M. D. (2014). Giving the early fossil

record of sponges a squeeze. Biol. Rev. Camb. Philos. Soc. 89, 972-1004. 

Bagby, R. M. (1966). The fine structure of myocytes in the sponges Microciona

prolifera (Ellis and Solander) and Tedania ignis (Duchassaing and Michelotti). J.

Morphol. 118, 167-181. 

Bassot, J.-M., Bilbaut, A., Mackie, G. O., Passano, L. M. and Pavans De Ceccatty,

M. (1978). Bioluminescence and other responses spread by epithelial conduction in

the siphonophore Hippodius. Biol. Bull. 155, 473-498. 

Boenigk, J. and Arndt, H. (2002). Bacterivory by heterotrophic flagellates: community

structure and feeding strategies. Antonie van Leeuwenhoek 81, 465-480. 

Bond, C. (2013). Locomotion and contraction in an asconoid calcareous sponge.

Invertebr. Biol. 132, 283-290. 

Boury-Esnault, N. and Rützler, K. (1997).  Thesaurus of Sponge Morphology.

Washington, DC: Smithsonian Institution.

Boury-Esnault, N. and Vacelet, J. (1994). Preliminary studies on the organization and

development of a hexactinellid sponge from a Mediterranean cave, Oopsacas

minuta. In Sponges in Time and Space. Proceedings of the Fourth International

Porifera Congress (ed. R. W. M. van Soest, T. M. G. van Kempen and J. Braekman),

pp. 407-416. Rotterdam: AA Balkema.

Burkhardt, P., Grønborg, M., McDonald, K., Sulur, T., Wang, Q. and King, N.

(2014). Evolutionary insights into premetazoan functions of the neuronal protein

homer. Mol. Biol. Evol. 31, 2342-2355. 

Claessen, D., Rozen, D. E., Kuipers, O. P., Søgaard-Andersen, L. and van Wezel,

G. P. (2014). Bacterial solutions to multicellularity: a tale of biofilms, filaments and

fruiting bodies. Nat. Rev. Microbiol. 12, 115-124. 

Collin, R., Mobley, A. S., Lopez, L. B., Leys, S. P., Diaz, M. C. and Thacker, R. W.

(2010). Phototactic responses of larvae from the marine sponges Neopetrosia

proxima and Xestospongia bocatorensis (Haplosclerida: Petrosiidae). Invertebr. Biol.

129, 121-128. 

Conaco, C., Bassett, D. S., Zhou, H., Arcila, M. L., Degnan, S. M., Degnan, B. M.

and Kosik, K. S. (2012). Functionalization of a protosynaptic gene expression

network. Proc. Natl. Acad. Sci. USA 109 Suppl. 1, 10612-10618. 

Degnan, B. M., Adamska, M., Craigie, A., Degnan, S. M., Fahey, B., Gauthier, M.,

Hooper, J. N. A., Larroux, C., Leys, S. P., Lovas, E. et al. (2008). The

demosponge  Amphimedon queenslandica: Reconstructing the ancestral metazoan

genome and deciphering the origin of animal multicellularity. Cold Spring Harb.

Protoc. 3, pdb.emo108. 

Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A.,

Seaver, E., Rouse, G. W., Obst, M., Edgecombe, G. D. et al. (2008). Broad

phylogenomic sampling improves resolution of the animal tree of life. Nature 452,

745-749. 

Dzik, J. (2002). Possible ctenophoran affinities of the Precambrian “sea-pen” Rangea.

J. Morphol. 252, 315-334. 

Elliott, G. R. D. and Leys, S. P. (2007). Coordinated contractions effectively expel

water from the aquiferous system of a freshwater sponge. J. Exp. Biol. 210, 3736-

3748. 

Elliott, G. R. D. and Leys, S. P. (2010). Evidence for glutamate, GABA and NO in

coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae,

Spongillidae). J. Exp. Biol. 213, 2310-2321. 

Elliott, G. R. D., Macdonald, T. A. and Leys, S. P. (2004). Sponge larval phototaxis: a

comparative study. In Sponge Science in the New Millennium, Vol. 68 (ed. M.

Pansini, R. Pronzato, G. Bavestrello and R. Manconi), pp. 291-300. Genoa, Italy:

Bollettino dei Musei e degli Istituti Biologici dell’Università di Genova.

Ellwanger, K. and Nickel, M. (2006). Neuroactive substances specifically modulate

rhythmic body contractions in the nerveless metazoon Tethya wilhelma

(Demospongiae, Porifera). Front. Zool. 3, 7. 

Ellwanger, K., Brümmer, F. and Nickel, M. (2004). Glutamate, GABA and serotonin

induce contractions in the sponge Tethya wilhelma (Porifera: Demospongiae). In

Jahrestagung der Deutschen Zoologischen Gesellschaft, Abstractband (ed. R.

Kinzelbach), pp. 157. Rostock: Zoologisches Institut der Universität Rostock. 

Ellwanger, K., Eich, A. and Nickel, M. (2007). GABA and glutamate specifically

induce contractions in the sponge Tethya wilhelma. J. Comp. Physiol. A 193, 1-11. 

Emson, R. H. (1966). The reactions of the sponge Cliona celata to applied stimuli.

Comp. Biochem. Physiol. 18, 805-827. 

Feuda, R., Hamilton, S. C., McInerney, J. O. and Pisani, D. (2012). Metazoan opsin

evolution reveals a simple route to animal vision. Proc. Natl. Acad. Sci. 109, 18868-

18872.

Fjerdingstad, E. J. (1961). The ultrastructure of choanocyte collars in Spongilla

lacustris (L.). Zeitschrift fur Zellforschung 53, 645-657. 

Fortunato, S., Adamski, M., Bergum, B., Guder, C., Jordal, S., Leininger, S.,

Zwafink, C., Rapp, H. T. and 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. 

Fromm, J. and Lautner, S. (2007). Electrical signals and their physiological

significance in plants. Plant Cell Environ. 30, 249-257. 

Fujiu, K., Nakayama, Y., Iida, H., Sokabe, M. and Yoshimura, K. (2011).

Mechanoreception in motile flagella of Chlamydomonas. Nat. Cell Biol. 13, 630-632. 

589

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The Journal of Experimental Biology (2015) doi:10.1242/jeb.110817

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