3 P or i f era
Sally P. Leys and Nathan Farrar
Introduction
Porifera is a taxon of morphologically diverse benthic animals
that inhabit marine and freshwater environments from desert ponds to caves, from abyssal to littoral, and from arctic to
tropical oceans. About 8500 species are recognized of some
11,000 described, but more than twice that number are estimated to exist based on current trends of discovery (Appeltans
et al. 2012, Van Soest et al. 2012). Four classes are presently
recognized, with Hexactinellida and Demospongiae (together
loosely termed the Silicea) forming a sistergroup to Calcarea and
Homoscleromorpha (Fig. 3.1A–D). Although some analyses
have suggested sponges may be paraphyletic, the current consensus is that the phylum Porifera is monophyletic (Nosenko
et al. 2013).
In contrast to the great range of gross morphologies of
Porifera, the taxon is united in sharing a common internal form,
consisting of flagellated cells whose beating action drives water
from microscopic openings on the animal’s surface, through discrete epithelial-lined canals in the body, and out of larger collecting vents (Fig. 3.1A–E). Filtration of water is the primary mode
of food uptake and excretion, and nutrient and gas exchange,
and this strategy has only been lost in a few members of one
deep-sea group of demosponges, which have turned to carnivory
(these are not discussed in this chapter).
The ‘aquiferous’ or canal system forms the central polarizing structure of any sponge. Incurrent openings, termed ostia,
litter the surface tissue and are invisible to the naked eye. The
excurrent vent or osculum, in contrast, is a millimetre to half
a metre in diameter and usually lies at the upper surface of the
animal such that water filtered, as visualized by food colouring
or fluorescent dye, is ejected in a jet above and directly away
from the sponge body. The body of a sponge consists of (a) the
aquiferous system (Fig. 3.1E–F), (b) soft tissues, including a
compressible collagenous middle layer (mesohyl) and, where
it is present, (c) an elastic and/or brittle skeleton of collagen
and minerals.
The soft tissues of sponges vary in density from cobweb thin
to massively thick (Fig. 3.1G). In all instances they consist of
an outer epithelial layer formed by plate-like or in some cases
T-shaped cells—both exopinacocytes—that enclose a collagenous region with wandering cells. Internally, bordering canals and
feeding chambers, endopinacocytes form the inner epithelium.
Sponges attach to substrates by a third type of epithelial ­cell—
basopinacocytes—which also secrete a particular adhesive extracellular matrix. The collagenous middle region of sponge tissues
is partly what gives the sponge body its elasticity. Elasticity (sponginess) is also provided by a type of collagenous skeleton called
spongin that is found in the class Demospongiae. Three classes
(Demospongiae, Hexactinellida, and Homoscleromorpha) have
skeletal components, called spicules, made of silica—in contrast
to the fourth class Calcarea, in which the spicules are made of
calcium carbonate. There is one unusual group of coralline demosponges which, in addition to producing a siliceous skeleton,
also constructs a massive skeleton of aragonite. Skeletogenesis
differs so much in each of the groups that it is considered that the
use of silica to form spicules arose independently in at least the
Silicea and Homoscleromorpha, as did calcification in Calcarea
and coralline demosponges.
Sponges are suspension feeders that filter water to extract bacteria and other picoplankton. Some species obtain a large portion of their nutrition from bacterial or algal symbionts, much
as do stony corals, but generally a complement of food sources is
required. The apparent simplicity of filtration as a process belies
the complexity of having the precise dimensions of filtration
system to maintain the correct pressure drop across the filter.
The sponge’s principal sensory system is epithelial and where it
is concentrated at particular locations in the aquiferous system
as ‘organs’ (Ludeman et al. 2014), it allows modifications of the
canal dimensions to either prevent uptake of bad water by closing ostia, or eject particles taken in inadvertently, by contracting.
In some cases contractions are complicated behaviours involving coordinated inflations and contractions of the whole animal, which have been described as ‘sneezing’ (Elliott and Leys
Structure and Evolution of Invertebrate Nervous Systems Edited by Andreas Schmidt-Rhaesa, Steffen Harzsch,
and Günter Purschke © Oxford University Press 2016. Published 2016 by Oxford University Press.
9
S t ru c t ure a n d E volu t i o n o f I n vert e b rat e Nervous S y s t e m s
Fig. 3.1. General morphology of sponges. A–D: Representatives of the
four classes of Porifera: A: Aphrocallistses vastus, Hexactinellida, B: Ephydatia
muelleri, Demospongiae, C: Sycon coactum, Calcarea, D: Oscarella n.sp.
Homosleromorpha (C,D, courtesy of J. Chu and S. Nichols). E, F: The aquiferous system with canals (E) and a single choanocyte chamber (F) shown
by scanning electron microscopy (SEM) (ch: choanocyte chamber, ca:
canal, arrows: apopyle exits from chambers to the canals). G: A schematic
of the differences in epithelia and mesohyl cell density in a gradient from
thin- (1) to thick- (3) walled sponges (from Pavans de Ceccatty 1974a,
with kind permission by Oxford University Press) (ic: incurrent canal; ec:
excurrent canal; ch: choanocytes). H: A larva of Amphimedon queenslandica.
2007, Meech 2008). These sensory and responsive systems are
described later in ‘Architecture’.
Porifera reproduce sexually and asexually. Sexual reproduction is by production of gametes—some species are hermaphroditic and others have separate sexes—and while the majority of
species studied brood the fertilized egg and release a fully developed ciliated swimming larva (Fig. 3.1H), in other instances
both males and females release gametes. In the latter case oocyte
fertilization and development into a swimming larva occur in
the water column. Sperm can be taken up by feeding chambers
of conspecifics or, if released as sperm packets, can be ‘caught’
on the surface of conspecifics allowing sperm to penetrate the
body wall and fertilize oocytes. There is some indication that
like other metazoans sponges have and use pheromones, which
sperm use to locate conspecifics and recognize gametes (Riesgo
et al. 2014).
Sponge larvae are ciliated propagules 20 µm to 2 mm in
length (Fig. 3.1H). They are all non-feeding and can stay in the
water column for a month, but in laboratory settings larvae commonly metamorphose within 1–2 days of release from the parent. Sponge larvae can respond to gravity and light (Warburton
1966); where it has been identified, the sensory organ is a ringlike arrangement of cilia and pigment at one pole (Leys and
Degnan 2001, Leys et al. 2002, Maldonado et al. 2003, Collin
et al. 2010).
Prior to molecular studies, Hexactinellida were proposed to
form a separate subphylum (or even phylum) because of their
unusual syncytial tissues and ability to arrest the feeding current
with a speed indicative of electrical signalling (Bergquist 1978,
Reiswig and Mackie 1983). Modern molecular phylogenies have
confirmed that hexactinellids and demosponges form a clade
that is sister to the other two classes, but hexactinellids remain as
the only group with syncytial tissues, and so far they are the only
group known to use electrical signalling. Glass sponges, which
comprise 8% of described species, are also unusual in being
restricted to deep marine habitats where silica levels are high and
temperatures low and stable. Demosponges (83% of sponge species) inhabit the greatest range of ecosystems, from freshwater
to marine, and have even adapted to the deep sea by adopting
carnivory in addition to filtration. Calcarea, which comprise 8%
of described sponges, and Homoscleromorpha (1% of sponge
species), the newest sponge class, are both marine groups with
wide distribution but often cryptic morphologies (Van Soest
et al. 2012).
10
Historical Investigations
Of Nervous Systems
It is unclear exactly when people began to consider sponges
in the light of the evolution of nervous systems. From Parker
(1919), we know that Aristotle wondered at the mechanism of
the responsiveness of sponges, but Lendenfeld (1885) was one
of the first to publish a study of the histology of nerve-like cells
of sponges and to suggest that sponges should no longer be considered to be protists. The late 1800s was a time of reflection
P or i f era
on the origins of coordination and while most of those writing had studied cnidarians not sponges, they all contemplated
the early origin of, and connection between, nerves and muscle, receptor, and effector (Moroz 2009, and references therein).
Parker tied these thoughts together in a seminal review in 1919,
but importantly he also carried out the first systematic experiments on sponge responsiveness to stimuli (Parker 1910). With
that work there began a series of investigations on responsiveness to chemicals and histological evidence of nervous tissues in
sponges, beginning with McNair (1923) and ending in Jones’
(1962) conclusion that there is no nervous system in sponges.
This work included important contributions by Prosser (1967),
Emson (1966), Lentz (1966), as well as Pavans de Ceccatty
(1955, 1960, 1971, 1974b), and Pavans de Ceccatty et al.
(1960). In recent years a very similar approach has been applied
(histological studies, as well as effects of chemicals on behaviour)
with little further advance in cellular sponges.
A major breakthrough was made in syncytial sponges (hexactinellids), however, with the discovery that they arrest their
feeding current upon touch (Lawn et al. 1981) and that this
is carried out by an electrically propagated action potential
(Leys and Mackie 1997). This is not to say that there is no
electrical signalling in demosponges. Loewenstein (1967)
claims to have recorded coupling between cells in Microciona
prolifera and Haliclona occulata, and although this work has
not been reproduced, Reiswig also reported a rapid (<1 s)
response of tissues covering the ostial (incurrent) pore fields
in Phorbas amaranthas (formerly Hymedesmia) (Reiswig
1979). The recent finding of ionotropic glutamate receptors in expressed transcripts from several sponges (Riesgo
et al. 2014), and functional work which shows that inward
rectifying potassium channels have ionic properties that suggest they may function to rapidly reset membrane potential
in demosponges (Tompkins-MacDonald et al. 2009), indicates there may be a more rapid mechanism of signalling in
cellular sponges than is currently understood.
Architecture
Sponges lack conventional nerves—but do sense and respond to
stimuli. As Parker noted, the most obvious activity of a sponge
is its filtration of vast volumes of water—up to 1000 times the
body volume each day—which from some sponges pours out
like ‘a vigorous spring’ (Parker 1919). The flagellated pump
cells form one set of effectors. Another more gradual activity
is contraction and relaxation of part of or the whole sponge
body. This behaviour, which has been noted since the time of
Aristotle, is controlled by a second set of effectors, cells forming the epithelia and/or cells of the middle layer (mesohyl) (e.g.
Pavans de Ceccatty et al. 1970, Pavans de Ceccatty 1976, Nickel
et al. 2011). It is easiest to address the architecture of the effectors in cellular and syncytial sponges separately, for although
there is evidence that both effectors respond in both types of
sponge, we know far more about the epithelial and mesohyl conduits in cellular sponges, and far more about flagella as effectors
in hexactinellids.
Conduction Pathways
And Effectors: Epithelia
Cellular sponges carry out contractions in response to a broad
selection of stimuli; these are not just reflex responses, as
described by Aristotle, in response to being torn off a rock (cited
by Parker, 1919); they are also able to propagate contractions in a
coordinated manner (Weissenfels 1990, Elliott and Leys 2007).
Most past work has focused on instant responses to stimuli, but
it is clear that there are much longer responses involving contraction of both epithelia and mesohyl cells, and that cells crawling
in the mesohyl are also affected because they stop crawling during contractions (Elliott and Leys 2007). Studies have shown
these contractions are propagated, and, most importantly, they
are stereotypical and can be triggered by a threshold of stimuli
(Elliott and Leys 2010, Ludeman et al. 2014).
The speed of contraction is typically slow—ranging from less
than 1 to 130µm/s (McNair 1923, Nickel 2004, Elliott and Leys
2007, Bond 2013)—well below the speed of electrically propagated events. This is what we fully expect for a signalling system
based on membrane-bound receptors. Propagation requires divalent cations and in particular calcium (Elliott and Leys 2007).
There are a couple of instances where more rapid propagation
occurs: McNair (1923) reported that waves of contraction can
move down the osculum of the freshwater sponge at 0.35 mm/s;
the other is the rapid dropping of flaps over the ostial pore fields,
previously discussed, as reported briefly by Reiswig (1979).
Except for those two instances we have no expectation of electrical signalling in cellular sponges. Even in Calcarea the types of
motility measured are extremely slow (Bond 2013).
Conduction Pathways
And Effectors: Syncytia
And Flagella
Glass sponge syncytia provide uninterrupted conduits for electrical
signalling. While it is quite certain sponges lack nerves, the glass
sponge syncytium functions analogously. About 75% of the glass
sponge body consists of a single syncytial tissue that penetrates all
parts of the sponge (Leys 1995, 1999). The few cellular regions
are also joined to the syncytium by a continuous ‘cell’ membrane,
but remain separated only by a protein plug in a narrow junction,
which offers no impedance to electrical impulses (Mackie and
Singla 1983). A stimulus to any part of the syncytium propagates
via calcium channels at a rate of 0.17–0.3 cm/s throughout the
syncytium and causes the flagellated pump units to stop beating
(Leys et al. 1999). The 5 s-long action potential is slightly retarded
by a 25–75% reduction in sodium concentration, but is completely blocked by the divalent ions Co2+ and Mn2+, and by the
potassium channel blocker TEA (Leys et al. 1999). It is thought
that calcium is the principal ion involved and that the slow rate of
propagation is due to slow restoration of the membrane potential
and or low channel abundance. The action potential is also sensitive to temperature with a Q10 of 3 (Leys and Meech 2006),
11
S t ru c t ure a n d E volu t i o n o f I n vert e b rat e Nervous S y s t e m s
(1) The first is simple stretch sensitive channels. The epithelium
of any sponge is probably sensitive as a whole, via channels
that sense changes in tension. This must be the case in
Hexactinellida, which respond to sharp jabs and to clogging
of the filtration system by arresting the flagella pumps (Lawn
et al. 1981, Leys et al. 1999). In cellular sponges, a fish bite
or clogging of the sponge filter by a sudden increase in particulate concentration may affect stretch sensitive channels,
triggering the contraction responses noted above. McNair’s
(1923) early work with freshwater sponges showed that the
osculum contracted rapidly if pin pricks were applied to the
top or to the bottom of the osculum chimney (Fig. 3.2A).
(2) Sensory cilia. Often cilia and flagella are considered identical
organelles, but in sponges the different modes of function of
flagella on choanocytes and of motile and non-motile cilia
on epithelia reflect hidden ultrastructural differences (Linck
1973). In contrast to the flagella pumps, cells at the exit
Fig. 3.2. Sensory systems in adult and larval sponges. A: McNair’s 1923
drawings of the response of the osculum of Ephydatia to touch, showing
presumed contraction of sphincter-like bands (a,b) equally along the osculum, (c,d) only at the tip of the osculum, and (e,f ) in two places along the
osculum and at its base (modified from McNair 1923, with kind permission
of the Marine Biological Laboratory, Woods Hole). B, C: Primary cilia in
the osculum of Ephydatia muelleri, shown in (B) thin section transmission
electron microscopy (TEM), and (C) scanning electron microscopy (SEM).
D: Relaxed and contracted Tethya wilhelma (from Ellwanger et al. 2007,
with kind permission by Springer). E: Primary cilium from the osculum of
Tethya wilhelma (from Nickel 2010, with kind permission by John Wiley
and Sons). F: The ciliary response to a rapid increase (I) and decrease (II)
in light intensity in a larva from Amphimedon queenslandica (from Leys
et al. 2002, with kind permission by Springer). H: Cross-section through
the posterior pole of the larva of Amphimedon queenslandica (TEM) (inset
shows an SEM of the posterior pole of the larva). I,J: Cytoplasmic bridges
connect pigment-filled projections at the posterior pole of the larva of
Sigmadocia caerulea (TEM). The presence of microtubules stabilizing the
bridges is visible in panel J (from Maldonado et al. 2003, with kind permission by Springer).
and this is given as one reason why, globally, hexactinellid sponges
might be restricted to deeper, cooler waters.
Sensory Structures
A sensory organ by definition receives stimuli from the environment and signals to nerves. As sponges do not have nerves,
they are also not usually considered to possess sense organs, but
recently this has come into question (Ludeman et al. 2014). If
sponges respond, then they are able to sense, and experimental
work has shown three ways in which this can happen.
12
P or i f era
of choanocyte chambers in many sponges have cilia, which
beat in a single direction with a single recovery stroke (SPL
personal observation), as do most metazoan cilia. In addition, non-motile cilia occur in discrete locations in the
aquiferous system. Careful study of specimens, preserved
and dissected so as to open their canal system to viewing
by scanning electron microscopy, shows that there are nonmotile cilia 4–6 µm long here and there along the aquiferous system (Ludeman 2010) (Fig. 3.2B,C). The inner lining
of the osculum in all demosponges studied so far possesses
cilia (Nickel 2001, Ludeman et al. 2014) (Fig. 3.2D,E)—
even glass sponge oscula have 6µm-long cilia (Ludeman
et al. 2014). Experimental work now shows that the oscula
cilia may function as sensory hair cells. These cilia label with
dyes used to label ion channels in primary cilia, and chemicals used to block sensation by hair cells or lateral line cilia
in fish, and also block propagated contractions that are usually easily triggered by mechanical stimuli or by L-glutamate
(Ludeman et al. 2014). The defined location and specific
function of the ciliary epithelium suggest that it is a region
that receives signals from the environment and transmits
them to the animal, and so in essence it functions as a sensory organ.
(3) ‘Photosensory’ organelles. Almost all sponge larvae are covered with cilia, which beat unidirectionally and constantly
to move the larva forward or prevent it from sinking. These
‘swimming cilia’ are approximately 20 µm long. In some
sponge species, towards the posterior swimming pole of the
larva, cilia vary in length from extremely short to those that
are ten times the length of ‘swimming cilia’ (Leys and Degnan
2001, Collin et al. 2010). The ‘pole’ cilia are also responsive to changes in light. In some larvae, when light intensity
is suddenly increased they straighten without beating, and
when light intensity decreases they bend over the posterior
pole (Leys and Degnan 2001). In other larvae the pole cilia
do the reverse, bending under high light and straightening
when light dims (Collin et al. 2010) (Fig. 3.2F,G). The cells
from which long cilia arise have unusual bulbous extensions
of the cell surface filled with pigment granules. It seems that
these are well positioned to block light to the lower portion
of the cilium (Fig. 3.2H). Maldonado et al. (2003) showed
that in some larvae cytoplasmic bridges connected neighbouring cytoplasmic extensions, raising the possibility that
there might exist some need for rapid (electrical) signalling
around the ciliary ring (Fig. 3.2I,J). Sponge larvae respond
not only to light but also to gravity (Warburton 1966) and
chemicals (Jackson et al. 2002), so other roles for cilia on the
surface of sponges cannot be ruled out.
Neuro -Molecules
And Neurotransmitters
Sponges may not have nerves but they do possess genes that
suggest they either have the potential to carry out synapticlike signalling or carry it out in an unconventional way. This
would not be unexpected in light of the behavioural repertoire
listed above. A near classic post-synaptic density (PSD) scaffold
could be present in sponges based on what is present in their genomes and transcriptomes (Sakaraya et al. 2007, Alie and Manuel
2010)—even rapid acting channel receptors (ionotropic glutamate receptors or iGluRs) were found in three sponge transcriptomes (Riesgo et al. 2014). For synaptic signalling one would
expect to see clusters of vesicles at the sites of contact of two
cells. Several good examples of vesicle exchange between cells
were shown by Pavans de Ceccatty et al. (1970) in a survey of
cell–cell connections in demosponges, but so far a clear example
of a PSD structure has yet to be found in a sponge (Sakaraya
et al. 2007, Alie and Manuel 2010).
There is some evidence that sponges use molecules associated
with synaptic transmission, though many of these studies are
difficult to assess. Early histochemical work by Lentz (1966) on
mesohyl cells in the osculum of Sycon showed serotonin (5HT),
epinephrine (Epi), and norepinephrine (NE) staining in vesicles
situated throughout the cytoplasm and near the cell membrane
(Fig. 3.3A,B). Acetylcholinesterase activity was also demonstrated
in cells near the osculum using a thiolacetic acid and lead nitrate
assay, although those vesicles were located in the perinuclear area
rather than at the cell membrane (Fig. 3, Lentz 1966). Recent
analysis of several sponge transcriptomes has identified enzymes
that synthesize these molecules including 5HT (e.g. tryptophan
hydroxylase) (Riesgo et al. 2014), albeit none have been found
so far in Sycon, the genus in which Lentz’s work was carried out.
Transmission electron micrographs (EM) showing exchange
of vesicles between cells strongly suggest that sponges do
have vesicle-based transmitter signalling (Pavans de Ceccatty
et al. 1970) (Fig. 3.3C,D). More recent work has used immunohistochemical methods, which give staining patterns that are
more diffuse, with labels seen generally throughout many cells
(e.g. Ramoino et al. 2007). While antibodies are a promising
technique for exploring ultrastructure, because sponge proteins
are highly divergent from even their closest metazoan relatives,
the use of antibodies raised against non-sponge antigens suffers
from lack of cross-reactivity, so that in the absence of rigorous
controls the results are difficult to interpret. Antibodies raised
against sponge-specific epitopes and coupled to EM imaging
(immunogold) in regions of cell–cell contact, such as those
shown by de Ceccatty (Fig. 3C–E), promise to be informative, and controls, such as those carried out by Lentz (1966) by
depleting 5HT, Epi, and NE, will be essential.
Reports of other neuroactive molecules in sponges have come
from physiological experiments where behaviours such as contractions and alteration of pumping rate have been monitored
(e.g. Emson 1966, Ellwanger and Nickel 2006). One question
that emerges from these findings is why sponges would require
signalling components typically associated with fast signalling
at synapses, since few sponge responses are rapid. The simplest
reason would be that molecules are involved in vesicle-based
endo- and exocytosis, such as occurs during feeding, as explored
by Ramoino et al. (2011). But it is also likely that contractions
of the whole sponge body in response to irritants in the water
would require coordination of all canals and therefore a signal
that would travel across all epithelia within seconds to minutes.
13
S t ru c t ure a n d E volu t i o n o f I n vert e b rat e Nervous S y s t e m s
Fig. 3.3. Evidence for cell–cell signalling sponges. A, B: Stains for (A)
serotonin and (B) acetylcholinesterase activity label vesicles around the
nucleus (N) and near the plasma membrane in cells of the osculum of
Sycon sp. (from Lentz 1966, with kind permission by John Wiley and
Sons). C: Vesicular exchange between two cells in Hippospongia communis.
D: Vesicle exchange via a potential cathrin-coated vesicle (C,D, from
Pavans de Ceccatty et al. 1970, with kind permission by Academic Press).
E: Particles on the membrane of pinacocytes in Ephydatia muelleri shown
by freeze fracture deep etch (from Lethias et al. 1983, with kind permission by Elsevier).
In spite of the difficulty in localizing distribution of molecules in tissues, glutamatergic signalling has nonetheless been
shown unequivocally to occur in freshwater sponges—where a
threshold concentration of 60–80µM L-glutamate (L-Glu) triggers a propagated contraction behaviour of the whole sponge
(Elliott and Leys 2007, Ludeman et al. 2014). Lower concentrations cause smaller, uncoordinated contractions ‘flinches’, and
higher concentrations cause the entire surface of the animal to
rupture due to the force of the contraction. While many chemicals trigger slight contractions of sponges (e.g. Ellwanger and
Nickel 2006), so far L-Glu alone has been shown to cause this
predictable, stereotypical response to precise concentrations.
That glutamate signalling is somehow involved in coordinating
whole animal behaviour is also supported by the demonstration
that incubation in gamma-aminobutyric acid (GABA) inhibits
all behaviour, whether triggered by L-Glu or by mechanical disturbance (Elliott and Leys 2010). Glutamate was shown by high
pressure liquid chromatography to be present in the freshwater
sponge and glutamate decarboxylase is also present, as are a
number of glutamate and GABA receptors, and even ionotropic
glutamate receptors (Elliott and Leys 2010, Riesgo et al. 2014).
Experiments to test for immunoreactivity of regions around the
osculum to custom antibodies to these receptors and molecules
are needed.
14
Evolutionary
Considerations
Of Neurogenesis
The expression of genes involved in neural development in
sponges, which do not have neurons, is intriguing. Probably the
most interesting of these is bHLH, which has been shown to
convert cells of a non-neuronal fate to a neuronal phenotype;
but bHLH also has roles in muscle development (and mesodermal cell differentiation), hematopoeisis, and skeleton development (Simionato et al. 2007). A sponge bHLH, AmqbHLH1,
was shown to have neurogenin-like activity in Xenopus and
proneural activity in Drosophila, where it was able to induce the
formation of more sensory bristles than in wild types (Richards
et al. 2008). In the Amphimedon demosponge embryo, bHLH
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genes are expressed in cells populating an unusual ‘middle layer’
of cells which differentiate into ciliated swimming cells, flaskshaped cells, and cells that contain mucous inclusions, all of
which populate the outer epithelium of the swimming larva.
Notch Delta expression was also studied in the homoscleromorph sponge Oscarella lobularis and found to largely occur in
choanocytes, the pump cells of the feeding chambers (Gazave
et al. 2008). It is not possible to draw inferences about neurogenic cell lineages from these data without additional characterization of the signalling properties of the cells that these genes
go on to define. This sort of work has not yet been done, but is
likely to yield exciting data, especially if coupled with studies
following the histogenesis of cells that form oscula and sensory
structures in the sponge.
In the absence of a link between neurogenic genes and functional sensory systems in sponges, we can imagine that, as with
the PSD scaffold, neurogenic proteins may be involved in developing some aspect of the sponge that is not specifically involved
with coordination (beyond the usual need for each cell to signal to its neighbours), which could have been co-opted to construct more rigid designs for signalling in later evolving animals.
Immunogold-EM studies with custom antibodies to sponge proteins will help clarify some of the PSD proteins’ roles in sponges.
There are other genes such as the axon guidance molecules
(AGMs), however, that must play alternative roles in sponges
because clearly neural patterning and synapse formation are
not required. Homologues of plexinA1, semaphorin3B, and
EphB1 are AGMs expressed in A. queenslandica larvae (Conaco
et al. 2012). AGMs create permissive and repulsive zones for
migrating cells and processes during development, and are
known to contribute to the formation of the vertebrate vascular
system, itself an elaborate set of interconnected tubes (Carmeliet
and Tessier-Lavigne 2005). It may be that AGMs participate in
the patterning and formation of the aquiferous canals in sponges
by restricting the ways in which the canal system can develop.
Why do sponges have a large set of genes typically associated
with nervous systems? If ctenophores are basal even to sponges,
as recently suggested (Ryan et al. 2013), then sponges may be
secondarily simplified having lost a nervous system. The residual
components may have been used in a simpler, non-neural signalling system that is well suited to the sponge’s physiological
needs, and is less energetically costly. Alternatively, the signalling
genes possessed by sponges may be used in a more conventional
way, and these ‘signalling units’ have been co-opted into the later
evolving nervous systems. A third framework, not entirely separate from the former, is that sponges use ‘neural’ components in
an unconventional manner. It may be that some sponge cells are
coupled through gap junctions which allow electrical signalling
through epithelia, and this system is linked to mesohyl cells via
slower vesicle-based signalling, as is suggested by some cell ultrastructure work. This would serve to effectively couple electrical
and chemical signalling, but at speeds far slower than seen in typical electrically coupled synapses, and more consistent with the
speed of behaviours observed in sponges. Unconventional use
of neural molecules may also point to convergent mechanisms,
though without a more complete characterization of the pathways this remains an open question. Sponges have no nervous
system, yet appear to respond to some neurotransmitters and
encode genes used to build and maintain nervous systems. How
these genes shape the morphology and physiology of the sponge
remains an active area of research.
R e f ere n c es
Alié, A. and Manuel, M. (2010). The backbone of the post-synaptic
density originated in a unicellular ancestor of choanoflagellates and
metazoans. BMC Evolutionary Biology, 10, 34.
Appeltans, W., Ahyong, S.T., Anderson, G., et al. (2012). The magnitude of global marine species diversity. Current Biology, 22,
2189–2202.
Bergquist, P.R. (1978). Sponges. Hutchinson and Co., London.
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