The Journal of Experimental Biology

---

The Journal of Experimental Biology

© 2015. Published by The Company of Biologists Ltd | The Journal of Experimental Biology (2015) 218, 581-591 doi:10.1242/jeb.110817

581

ABSTRACT

Genomic and transcriptomic analyses show that sponges possess a

large repertoire of genes associated with neuronal processes in other

animals, but what is the evidence these are used in a coordination or

sensory context in sponges? The very different phylogenetic

hypotheses under discussion today suggest very different scenarios

for the evolution of tissues and coordination systems in early animals.

The sponge genomic ‘toolkit’ either reflects a simple, pre-neural

system used to protect the sponge filter or represents the remnants

of a more complex signalling system and sponges have lost cell

types, tissues and regionalization to suit their current suspension-

feeding habit. Comparative transcriptome data can be informative but

need to be assessed in the context of knowledge of sponge tissue

structure and physiology. Here, I examine the elements of the sponge

neural toolkit including sensory cells, conduction pathways, signalling

molecules and the ionic basis of signalling. The elements described

do not fit the scheme of a loss of sophistication, but seem rather to

reflect an early specialization for suspension feeding, which fits with

the presumed ecological framework in which the first animals

evolved.

KEY WORDS: Porifera, Neuroid conduction, Neural signalling,

Nervous system evolution

Introduction

All animals and plants have tissues that conduct signals. Unicellular

eukaryotes have a huge number of complex behaviours (Boenigk

and Arndt, 2002) and even bacteria can coordinate to form

multicellular arrays (Claessen et al., 2014). Therefore the ability to

receive signals to coordinate behaviour and the mechanism of

transmitting signals between cells has come about many times in

very different lineages. But how related are the elements of these

systems? Neuroid or non-nervous conduction in giant plant or algal

cells such as Mimosa or  Nitella (Fromm and Lautner, 2007)

functions similarly to the neuroid conducting tissues of glass sponge

syncytia, and to the gap junction-coupled epithelia of cnidarians,

ctenophores and other animals (Mackie, 1965; Bassot et al., 1978;

Hernandez-Nicaise et al., 1980; Leys and Mackie, 1997). Different

ions form the basis of the action potentials (chloride and calcium

potentials in the plant and alga, calcium in the sponge, and sodium

or calcium in cnidarians and ctenophores) but the effect is similar –

generating a rapid signal that effects a behavioural response. More

specialized cellular conduction pathways – nerves – are suggested

to have originated from these sorts of excitable conducting epithelia

(Mackie, 1990; Mackie, 2004). Neuroid conduction is thought to

have come about independently in different lineages (Mackie, 1970),

but nerves appear to be a metazoan-specific feature, and are

considered so specialized for their function that the idea that

REVIEW

Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, 

Canada.

*Author for correspondence ([e-mail])

complex neural signalling may also have several independent or

parallel origins (Moroz, 2009; Moroz et al., 2014) is not easily

accepted.

For over a century our understanding of the evolution of complex

systems such as nerves and nervous tissues has been reconstructed

by studying elements found in extant representatives of the earliest

evolving phyla – especially sponges and cnidarians (Parker, 1919).

But recent phylogenetic analyses, which suggest that ctenophores

may have evolved before sponges (Dunn et al., 2008; Ryan et al.,

2013; Moroz et al., 2014) offer a new perspective because

ctenophores have complex nervous systems and behaviour. This

new scenario could mean there have been independent origins of

complex neural signalling, or that sponges have lost nerves and the

ability to send rapid directed signals. Other complex body systems

have evolved in parallel in different lineages (e.g. Steinmetz et al.,

2012), but whether the neuron could have evolved more than once

is the main question. More sponge genomes, with more complete

coverage and improved phylogenetic analysis will confirm in the

coming years which group is more basal. But the current genomic

data forces us to ask hard questions: what do sponges really have in

terms of a ‘neural toolkit’ and could it reflect the remnants of a

more-sophisticated coordination system? Alternatively, is the

presence in genomes, and even expression in tissues, of ‘neuronal’

genes in sponges enough to even warrant the label ‘pre-nervous

system’? In an attempt to address these questions, I first briefly

describe the nature of species from which data derives and then

evaluate whether what we now know of the molecules, tissues and

physiology of sponges best reflects elements of a potential

(pre)nervous system, loss of one, or elements of a distinct system

specialized for non-neural functions.

Model systems in Porifera

Marine sponges are typically difficult to maintain in tanks. Because

of the large volumes of water they filter, unless water exchange is

great, waste products quickly build up. Sponges rapidly detect poor

water quality and reduce their filtration rates. But even for those that

can be kept in tanks, few species release gametes (most of them

brood embryos) and spawning events are usually unpredictable; only

one, Tetilla serica (Watanabe, 1978) is known to have reproduced

in captivity. Tetilla has a 2 year life cycle, maturing one year and

spawning the next, and individuals can be separated into males and

females – an almost ideal subject. Watanabe (Watanabe, 1978)

reports that Tetilla was so abundant in the Aburatsubo Bay, Japan,

that the eggs ‘spawned by so many adults paint the sea surface red

every two years’. Unfortunately the species is no longer known in

those waters, and no other species has been found that is so

tractable; so workers use the most readily obtained species locally

(Fig. 1).

There are different reasons for selecting particular species for

different kinds of work: Amphimedon queenslandica produces large

numbers of embryos and larvae year round, larvae are large (up to

1 mm in length) and have differentiated morphology with anterior

and posterior ends, cell layers and sensory cells that are involved in

Elements of a ‘nervous system’ in sponges

Sally P. Leys*

---