Elements of a ‘nervous system’ in sponges

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 suspensionfeeding 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.

Osculum dynamics and filtration activity in small single-osculum explants of the demosponge Halichondria panicea

“…Therefore, and consistent with the suggestions of Hoffmann et al (2005), H. panicea may perhaps cease its pumping activity to establish internal body anoxia to maintain its endosymbiotic community (Althoff et al 1998, Wichels et al 2006, Schneemann et al 2010. Bacteria isolated from H. panicea are potential sources of neuro-active compounds (Perovic et al 1998), suggesting that sponge-associated microbes also play a functional role in coordinating contractile behavior of the sponge host (Meech 2008, Leys 2015.…”

“…Recent studies suggest the osculum senses external stimuli by means of primary cilia that line its inner epithelium (Ludeman et al 2014, Leys 2015. Osculum contractions appear to be stimulated by air exposure (Parker 1910), electrical, mechanical and chemical stimuli (Parker 1910, Prosser et al 1962, Elliott & Leys 2007, and changes in light intensity (Reiswig 1971b) and water flow dynamics .…”

“…Osculum contractions appear to be stimulated by air exposure (Parker 1910), electrical, mechanical and chemical stimuli (Parker 1910, Prosser et al 1962, Elliott & Leys 2007, and changes in light intensity (Reiswig 1971b) and water flow dynamics . Exposure to clay also triggers oscular contraction (Gerrodette & Flechsig 1979, Bannister et al 2012, indicating that sponges can protect and clean their filter-feeding apparatus from unwanted particles (Elliott & Leys 2007, Tompkins-MacDonald & Leys 2008, Leys 2015. Furthermore, opening and closure of oscula in a tropical demosponge indicate an intrinsic species-specific rhythm possibly coordinated by changes in the flagellar activity of choanocytes (Reiswig 1971b).…”

Structure, Distribution, and Function of Neuronal/Synaptic Spinules and Related Invaginating Projections

“…Among the basal metazoan groups, definitive neuronal tissue and synapses are found in the cnidarians (jellyfish, corals, sea anemones, hydras) and ctenophores (comb jellies); no definitive neuronal tissue is yet known for placozoans and sponges (Jorgensen 2014; Halanych 2015; Leys 2015). The simplest bilaterians, the flatworms (acoels, planarians, flukes, tapeworms), have definitive brains.…”

Sponges as models to study emergence of complex animals

“…The initial analyses focused on gene content, with emphasis on genes considered to be related to animal multicellularity and complexity, such as those involved in embryonic development, immunity and sensory functions [47][48][49][50][51][52][53][54][55][56][57][58][59][60][61][62]. These studies, along with insights from transcriptomes of several other sponge species [63][64][65][66][67], demonstrated that sponges possess representatives of overwhelming majority of animal developmental gene families, including developmental transcription factors [53,54] and components of signalling pathways [6,48-50,55,62].…”