Physiology of coordination in sponges

Abstract

All multicellular organisms need a means of communicating between cells and between regions of the body. The evolution of a nervous system, by the Cnidaria, provided a fast means of communication and enabled the colonization of rapidly changing environments. Sponges, the descendants of the first multicellular animals, lack nerves but nevertheless have a number of different systems that allow coordinated behaviour, albeit rather slow coordinated behaviour. It is from elements within these systems that the origins of the nervous and endocrine systems, the grand organizing principles of higher animals, seem likely to have appeared. Electrical activity has not been found in cellular sponges, yet local contractions are elicited in response to a variety of stimuli and, in some cases, contractions propagate across the body to control the hydrodynamics of the feeding current. The mechanism of propagation is thought to involve hormones or a combination of other signaling molecules and direct mechanical action of one cell on the next, leading to increased intracellular calcium. In other instances cellular sponges respond to stress, such as heat shock, by elevating intracellular calcium by way of second messengers such as cyclic ADP-ribose. Electrical communication, well known in plants and protists, was first demonstrated in a sponge in 1997. Hexactinellids (glass sponges), which arrest their feeding current within 20 s of mechanical or electrical stimulation, do so via an electrical impulse that propagates through syncytial tissues. These unusual syncytial tissues are cytoplasmically coupled from outside to inside and top to bottom so that there are no membrane boundaries to impede the electrical currents. Pharmacological tests suggest that Ca2+, rather than Na+, drives the action potential. The conduction velocity is slow (0.27 cm·s–1) and is highly temperature sensitive (Q10~3). At present, glass sponges are the only poriferans known to have propagated electrical signals. In addition, reports of directional swimming in sponge larvae, of the rapid and coordinated changes in the tensile strength of the extracellular matrix in Chondrosia Nardo, 1847, and of the rapid closure of ostia of some cellular sponges in response to mechanical stimuli further illustrate the variety of coordinating mechanisms that evolved in the Porifera in the absence of a nervous system.