Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges

BMC Evolutionary Biology

Sally P Leys³  Jordi Paps²  Ana Riesgo¹  Nathan Farrar³  Danielle A Ludeman³ 

[1]Department of Animal Biology, Universitat de Barcelona, Avinguda Diagonal 643, Barcelona 08028, Spain

[2]Department of Zoology, University of Oxford, Oxford OX1 3PS, UK

[3]Department of Biological Sciences, University of Alberta, CW 405 Biological Sciences Building, Edmonton, Alberta T6G 2E9, Canada

关键词: PKD;    Sensory systems;    Evolution of nervous systems;    Primary cilia;    Porifera;   

Others  :  858129
DOI  :  10.1186/1471-2148-14-3

 received in 2013-09-04, accepted in 2013-12-11,  发布年份 2014

【 摘 要 】

Background

One of the hallmarks of multicellular organisms is the ability of their cells to trigger responses to the environment in a coordinated manner. In recent years primary cilia have been shown to be present as ‘antennae’ on almost all animal cells, and are involved in cell-to-cell signaling in development and tissue homeostasis; how this sophisticated sensory system arose has been little-studied and its evolution is key to understanding how sensation arose in the Animal Kingdom. Sponges (Porifera), one of the earliest evolving phyla, lack conventional muscles and nerves and yet sense and respond to changes in their fluid environment. Here we demonstrate the presence of non-motile cilia in sponges and studied their role as flow sensors.

Results

Demosponges excrete wastes from their body with a stereotypic series of whole-body contractions using a structure called the osculum to regulate the water-flow through the body. In this study we show that short cilia line the inner epithelium of the sponge osculum. Ultrastructure of the cilia shows an absence of a central pair of microtubules and high speed imaging shows they are non-motile, suggesting they are not involved in generating flow. In other animals non-motile, ‘primary’, cilia are involved in sensation. Here we show that molecules known to block cationic ion channels in primary cilia and which inhibit sensory function in other organisms reduce or eliminate sponge contractions. Removal of the cilia using chloral hydrate, or removal of the whole osculum, also stops the contractions; in all instances the effect is reversible, suggesting that the cilia are involved in sensation. An analysis of sponge transcriptomes shows the presence of several transient receptor potential (TRP) channels including PKD channels known to be involved in sensing changes in flow in other animals. Together these data suggest that cilia in sponge oscula are involved in flow sensation and coordination of simple behaviour.

Conclusions

This is the first evidence of arrays of non-motile cilia in sponge oscula. Our findings provide support for the hypothesis that the cilia are sensory, and if true, the osculum may be considered a sensory organ that is used to coordinate whole animal responses in sponges. Arrays of primary cilia like these could represent the first step in the evolution of sensory and coordination systems in metazoans.

【 授权许可】

   
2014 Ludeman et al.; licensee BioMed Central Ltd.

【 图 表 】

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